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Microarthropod use as bioindicators of the environmental state: case of soil mites (Acari)
from Côte d’Ivoire.
Julien Kouadio N’Dri
1*, Thierry Hance
2, Henri Marc André
3, Jan Lagerlöf
4, Jérôme Ebagnérin Tondoh
11 UFR des Sciences de la Nature/Centre de Recherche en Ecologie, Université Nangui Abrogoua 02 BP 801 Abidjan 02, Côte d’Ivoire
2 Université Catholique de Louvain, Biodiversity Research Center, Earth and Life Institute, Place Croix du Sud 4, B-1348 Louvain-la-Neuve, Belgium.
3 Musée royal de l’Afrique centrale, Leuvensesteenweg 13, B-3080 Tervuren, Belgium.
4 Swedish University of Agricultural Sciences (SLU), Dept. of Ecology, P.O.Box 7044, SE-750 07 Uppsala, Sweden.
* Corresponding author: [email protected]
Keywords: Mite, forest, savannah, disturbance, indicator species.
1 SUMMARY
The aim of this study was to identify biological indicators of soil state under four agrosystem types. Therefore, Lamto savannah (SOM-poor sites), Oume primary forest (SOM-rich sites), Oume teak plantation (SOM-less sites) situated in Sudanese domain and Tai primary forest (SOM-moderate sites) localized in Guinean domain (Ivory Coast) were sampled twice during one year. The Indval software was used to identify the indicator species, through two analyses.
The first analysis separated level 1- climatic zones (Guinean vs. Sudanese), level 2- localities (Oumé vs. Lamto vs. Taï), level 3-segregated sites depending on the level of disturbance: A second analysis opposes litter dwelling to mineral soil dwelling mites. The results revealed that only one species was dominant and ubiquitous, particularly Afrotrachytes sp.1whereas three species, respectively Rhysoglyphus sp.1, Dendracarus sp.1and Acaridae sp.4 were dominant and specialist. Chemical elements Corg (g/kg), Ctot (%), Ntot (%), and SOM (g/kg) was higher in forest than in savannah and teak plantation. Dwelling mite indicator species characterizing the Guinean domain (Taï primary forest / undisturbed site) were highly different to those observed in Sudanese domain (disturbed sites). If the four sites were considered and distinguished between microhabitats, the essential species indicators were found in Oume primary forest where a moderate disturbance was observed. However, a lower number of indicator species were found in Oume teak plantation, characterized by a high disturbance. The value of Oribatida-Actinedida ratio ranged from 3.95 in teak plantation to 52.28 in Oume primary forest.
2 INTRODUCTION
Value of biodiversity conservation has been recognized worldwide (Bonn and Gaston, 2005;
Humphrey, 2005), notably because the erosion of biodiversity elements can cause impoverished ecosystem functioning (Mertz et al., 2007).
However, biodiversity indicators are still needed to assess changes due to ecosystems management and global change. Several indices have been
developed to measure the biological diversity (Shannon, 1962; Pielou, 1969; Whittaker, 1972);
however, they present some bias such as overestimating or underestimating the role of rare species. In that context, Dufrêne and Legendre (1997) renewed the notion of indicators by combining the relative abundance of a species with its relative frequency of occurrence in
defined groups of sites. This approach seems particularly sound for monitoring of soil ecosystem changes and biodiversity conditions because its cost-effective, indicators are easily and reliably identified, the indicators represent eco- functionally important species, and respond differently to disturbance regimes (Pearce and Venier, 2006; Guéi and Tondoh, 2012). Many definitions have been attributed to the notion of indicators (Maleque et al., 2009). Nevertheless, the biological indicators are recognized as being organisms or communities of organisms which reaction are observed representatively to evaluate the state or the health of an ecosystem (Ferris and Humphrey, 1999; Walz, 2000; Burger, 2006;
Gerhardt, 2012). According to the different applications of biological indicators, three groups can be distinguished: (1) environmental indicator, where species responding predictably to environmental disturbance or change,(2) ecological indicator, where species are known to be sensitive to pollution and habitat fragmentation,(3) biodiversity indicator, where species richness of an indicator taxon is used as indicator for species richness of a community (Gerhardt, 2012). Direct measurement of soil biodiversity is expensive, and therefore a substitution of measurement by indication is desirable (Ekschmitt et al., 2003). The different properties of soil animals, which can be potentially used as indicators of soils quality was listed by Linden et al. (1994). These include single organism level characteristics (behaviour, development), community characteristics (species
richness, trophic groups, functional groups), and characteristics of the biological process (bioaccumulation, soil modification). From this point of view, mites or others soil microarthropods species and species assemblages offer several advantages for assessing the quality of soil ecosystems (Behan-Pelletier, 1999; Parisi et al., 2005; Gulvik, 2007; Gergócs & Hufnagel, 2009; Proctor et al., 2011; Sabbatini-Peverieri et al., 2011; Zhao et al., 2013). Most soil mites live in the organic horizons, play an essential role in organic matter decomposition but also represent a trophically heterogenous group with predators, detripagous and mycopagous species. Previous study in South African soils showed that Oribatida dominate the forest soil while Trombidiform mites were more abundant in the savannah (Olivier and Ryke, 1965; Loots and Ryke, 1967). In contrast to the anaerobic process of fermentation and putrefaction causing an increase of Acaridida, a best porosity (aeration) of the soil promotes the development and emergence of Oribatida (Ducarme et al., 2004).
The identification of characteristic or indicator species is a current practice in ecology and biogeography. Field studies describing sites or habitats usually mention one or several species that characterize each habitat. However, there is a clear lack of data concerning the African soil mesofauna. Our aim was to provide a first insight into this field by extraction of potential indicator species of a completely new set of data sampled in well-contrasted ecosystems.
3 MATERIAL AND METHODS
3.1 Study sites and sampling design: Four sites located in Ivory Coast were studied: Lamto savannah (Coordinates: 6°13' N, 5°02' W;
altitude: 125 m asl) and Oumé primary forest and Teak plantation (Coordinates:6°31’ N, 5°30’ W;
altitude: 200 m asl) situated in Sudanese domain and the Tai primary forest (Coordinates:5°45’ N, 7°07 W; altitude: 150-200 m asl) based in Guinean domain. Each site was sampled twice during 2008 at different depth (Litter, 0-5 cm, 5- 10 cm, 10-15 cm, 15-20 cm, 20-25 cm, 25-30 cm,
30-35 cm, 35-40 cm), with a steel corer (∅ 3.5 cm). A total of 270 soil cores were taken at each site and along the entire soil profile for extracting. Another set of 240 soil cores were taken for physico-chemical analysis. More details concerning the sampling are given by N’Dri and André (2011), and other descriptions relative to the site such as climate regime, temperature, rainfall pattern, vegetation and soil type are presented in Table 1.
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Table 1: Ecological variables and levels of the disturbance from the different site investigated. Temperature and precipitation are annual mean values.
Habitats investigated (sites)
Oume primary forest Taï primary forest Lamto savannah Oume teak plantation
Variables description
Climate Subequatorial Subequatorial Intertropical humid Subequatorial
Temperature of the last 10 years
(1998-2007) 26°C 25.35°C (1993-2002) 34.58°C 26°C
Temperature of the study years
(2008) 25.9°C --- 36.99°C 25.9°C
Precipitation of the last 10 years
(1998-2007) 1447.9 mm 1853.2 mm (1993-2002) 1270.02 mm 1447.9 mm
Precipitation of the study years
(2008) 1592 mm --- 1211.4 mm 1592 mm
Vegetation characteristics Semi-deciduous forest Humid forest Discontinuous layer of trees and 14-year-old teak
(mesophile type) shrubs dominated by tall palm
trees (monospecies plantation)
(Borassus aethiopum) and
Chromolaena odorata (Asteraceae)
Sol type Ferralitic soil Desaturated ferrallitic Ferralsols Ferralitic soil
(sandy-clay) and hydromorphic soils (sandy loam)
Levels of the disturbance Moderately disturbed site
and Undisturbed site Less disturbed site Highly disturbed site and
limited to some tracks limited to clearing and
cutting --- No available
3.2 Mite extraction and identification:
The mesofauna was extracted during 1-week using a Berlese-Tullgren system. The extracted microarthropods were poured into a Petri-dish from where the mites were sorted from the rest of the microarthropods in 70% ethanol and counted under a binocular microscope.
Temporary mounts of specimens were made and examined thoroughly for fine taxonomic details under the compound microscope.In the absence of African keys, identification of mites was done at species level or as morphospecies (i.e., individuals that differed from morphological features), using keys and illustrations provided in Balogh and Balogh (1992), Krantz (1978), Dindal (1990) and Krantz and Walter (2009). Respective photographs were treated with AUTO-MONTAGE
and classified in a database. Reference collection and database were deposited in the African Museum of Tervuren, Belgium.
3.3 Mesological factors analysis: The pH- H2O (Baize, 1988) was measured with a pH meter (HANNA) in 960 mineral soil cores. Bulk density (g.cm-3) and soil water content (WC) from 960 mineral soil samples were measured after 48 h drying at 105°C (Baize, 1988). Other chemical analyses such as organic carbon (Corg), total carbon (Ctot), total nitrogen (Ntot), ratio carbon / nitrogen (C/N), soil organic matters (SOM) from extreme layers (0-5 cm and 35-40 cm) were realized on 80 samples by the “Centre Provincial de l’Agriculture et de la Ruralité” in La Hulpe (Belgium). Soil analyses were realized on the upper and bottom layers (0–5 cm and 35–40 cm) in order to assess correlation between soil characteristics and species indicators.
3.4 Data analysis: The indicator value (IndVal) was calculated for each morphospecies, as described by Dufrêne and Legendre (1997):
Specificity (Aij), Aij = Nindividualsij / Nindividuals i
where Nindividualsij is the mean number of species i across sites of group j, and
Nindividualsi is the sum of the mean number of individuals of species i over all groups.
Fidelity (Bij), Bij = Nsitesij/Nsitesj
where Nsitesij is the number of sites in-group j where species i is present, and Nsitesj is the total number of sites in that group. The percentage indicator value for species i in-group of sites j is:
IndValij = Aij × Bij × 100
The indicator value for species i is:
IndVali = max [IndValij]
Hierarchical classification of samples (clusters) based mostly on sites characteristic was used for data analysis whereas groups represent the different partitioning level (climatic zones, localities, sites and litter vs. mineral soil).
Contrary to Dufrêne and Legendre (1997), where only IndVal index significant at P ≤ 0.01 and superior to 25% have been taken in consideration, all species that have an index value significant at P < 0.05 are presented in the different tables. Two IndVal analyses were done.
According to the initial analysis, the first level of the classification separated climatic zones (Guinean vs. Sudanese) following the precipitation level and soil pH type. The second level separated localities (Oumé vs. Lamto vs.
Taï) according to vegetation type and Ctot (%), Ntot (%) content and distinguished high SOM- content sites (SOM-rich sites) from low Ctot (%), Ntot (%) content ones (SOM-poor sites). The level 3 segregated sites depending on the level of disturbance: undisturbed sites (Taï primary forest), less disturbed sites (Lamto savannah), moderately disturbed sites (Oume primary forest) and highly disturbed sites (Oume teak plantation). A second analysis opposes litter dwelling to mineral soil dwelling mites (microhabitat). As like to Badejo and Ola-adams (2000), Kaczmarek and Marquardt (2010), the Berger-Parker Dominance Index for each taxonomic group was done. This index is a measure of the percentage contribution of a taxonomic group to the total number of mites in each site. Generic level taxa that provided 3% or more of the total density of mites in a site are regarded as dominant. The mites were not named according to the Code of Zoological Nomenclature because the lack of taxonomic
4626 information for African soil mites.Soil mesological factors means were compared using a one-way ANOVA test. These tests were conducted using the software Statistica 7.0 (StatSoft Inc., 1984–2004). At last, a principal
component analysis (PCA) was done to analyze the effects of land-use type (sites) on both species indicators (listed in Table 3) and mesological factors. These analyses used the module ‘PCA’ of the software ADE-4 (Thioulouse et al., 1997).
4 RESULTS
4.1 Species indicator of the different sites: In all, 177 soil mites species were identified (Lamto savannah: 85, Oume primary forest: 98, Oume teak plantation: 52 and Taï primary forest: 66 species). On 66 species from the Guinean zone (Taï primary forest), only four species, three oribatids and one uropodid, can be considered as indicators of that zone where the precipitation level was high with an acid soil. In contrast, three species are indicators of the Sudanese zone with a low precipitation and a
basic soil, despite a richness estimated at 149 species. Nine species, four oribatids and five gamasids, are indicators of Lamto locality (SOM- poor site), whereas a single oribatid, Meristacarus sp.1, is indicator of the locality of Oumé (SOM- rich sites). If sites are considered, two species, a gamasid, Gamaside sp.3 and an acaridid, Rhysoglyphus sp.1, are indicators of the Teak plantation (highly disturbed site). 15 mites (Table 2) are also indicator species of Oume primary forest (moderately disturbed site).
Table 2: Species indicator found in the investigated habitats: Climatic zone, locality or study site. Only species significant at P ˂ 0.05 are indicated. IndVal indexes (IV) shown in the last column
2 ZONES
Group Species IndVal index (IV)
Sudanese (Oume and Lamto) Afrotrachytes sp.1 76.56
Uropodidae sp.2 42.22
Rhysotritia duplicata 35.56
Guinean (Taï) Oppiidae sp.1 32.14
Oribatulidae (Protonymphae) 31.03
Saxicolestes sp.1 20.00
Uropodidae sp.1 13.33
3 LOCALITIES
Group Species IndVal index (IV)
Oumé Meristacarus sp.1 41.11
Lamto Dendracarus sp.1 66.67
Trachyuropodide sp.3 49.93
Mycrogynium sp.1 46.67
Galumna sp.11 24.56
Gamaside sp.14 24.56
Damaeidae sp.3 24.24
Evimirus uropodinus 20.51
Macrochelidae sp.1 20.00
Oribate sp.49 20.00
Taï - -
4 SITES
Group Species IndVal index (IV)
Oume primary forest Mycobatidae sp.2 69.50
Galumna sp.10 61.11
Trachyuropodide sp.2 59.77
Afrotrachytes (larva) 53.33
Mesoplophora sp.1 48.00
Lamellobates palustris 45.71
Carabodes sp.1 44.33
Uropodidae sp.3 39.11
Galumna sp.5 38.62
Lopheremaeus mirabilis 33.33
Mixacarus sp.1 32.73
Dolicheremaeus sp.1 30.56
Sabahtritia sp.1 29.09
Carabodidae sp.2 25.64
Malacoangelia sp.1 25.00
Taï primary forest - -
Lamto savannah - -
Oume teak plantation Gamaside sp.3 30.00
Rhysoglyphus sp.1 26.67
4.2 Species indicator of microhabitats: A second partition in 2 microhabitats, litter vs.
mineral soil, was made in all sites (data from all site was pooled). A single oribatid is an indicator species of litter, Oppiidae sp.1. In contrast, Rhysotritia duplicata and two Mesostigmata Afrotrachytes sp.1 and Uropodidae sp.2 are indicator species of mineral soil. If sites are considered, i.e. if all samples are partitioned into 8 groups (litter and mineral soil from the four sites), the list of species indicator of microhabitats is much longer (Table 3). Three oribatids are species indicator of litter in Taï
primary forest, while only a single gamasid is indicator of litter in Oume teak plantation. In mineral soil, a single Actinedida, Actinedide sp.8 is indicator of Oume teak plantation. The number of indicator species rises to five in Lamto savannah and to 16 in Oume primary forest.
There is no indicator species of litter in Oume primary forest and Lamto savannah, neither of mineral soil in Taï primary forest. Whatever the partitioning and the type of habitats investigated, the indicators species represents 21% of the total species richness.
Table 3: Species indicator found in the observed microhabitat, litter (variable height) vs. mineral soil (0- 40 cm), in the four study sites. Only species significant at P ˂ 0.05 are indicated. IndVal indexes (IV) shown in the last column.
LITTER
Group Species IndVal index (IV)
Oume primary forest -1 - -
Taï primary forest -2 Oppia sp.2 12.69
Galumna sp.4 8.65
Oribatulidae (Protonymphae) 6.06
Lamto savannah -3 - -
Oume teak plantation -4 Gamaside sp.3 11.67
MINERAL SOIL
Species IndVal index (IV)
Oume primary forest -5 Afrotrachytes sp.1 27.91
Mesoplophora sp.1 25.00
Galumna sp.10 22.92
Galumna sp.5 21.15
Carabodes sp.1 18.67
Mycobatidae sp.2 17.87
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Trachyuropodide sp.2 17.70
Lamellobates palustris 15.56 Lopheremaeus mirabilis 11.11
Uropodidae sp.3 10.11
Acaridea sp.4 10.00
Dolicheremaeus sp.1 9.72
Meristacarus sp.1 9.11
Sabahtritia sp.1 9.09
Malacoangelia sp.1 8.33
Afrotrachytes (larva) 7.41
Taï primary forest -6 - -
Lamto savannah -7 Trachyuropodide sp.3 16.84
Macrochelidae sp.1 10.00
Dendracarus sp.1 9.52
Mycrogynium sp.1 9.26
Gamaside sp.14 7.14
Oume teak plantation -8 Actinedide sp.8 7.37
4.3 Taxonomic dominant groups: The Berger-Parker Dominance Index for each taxonomic group is presented in Table 4. The value of this number varied between five (Taï primary forest) and 12 (Oume teak plantation).
At the scale of the four sampling sites, 23 species were dominants: Actinedide sp.8 (6.39%), Trachyuropodide sp.2 (3.28%), Trachyuropodide sp.3 (7.17%), Uropodide sp.2 (4.57%), Afrotrachytes sp.1 (3.33-28.28%), Gamaside sp.3 (4.11%), Gamaside sp.14 (3.14%), Paralopheremaeus legendrei (3.20%), Mycobatidae sp.2 (3.65-4.42%), Oribatulidae (Protonymphae) (5.00%), Epilohmannia sp.1 (4.57%),
Meristacarus sp.1 (3.28-5.02%), Rhysotritia duplicata (3.20%), Galumna sp.4 (8.89%), Galumna sp.5 (3.03%), Dendracarus sp.1 (3.14%), Oribate sp.1 (3.65%), Oppiidae sp.1 (5.00%), Oppia sp.2 (4.48- 19.44%), Acaridae sp.4 (3.16%), Rhysoglyphus sp.1 (3.20%), Rhysoglyphus sp.2 (3.65%), Rhysoglyphus sp.3 (3.54-8.74%). In addition, only one species was dominant and ubiquitous, particularly Afrotrachytes sp.1 whereas three species, respectively Rhysoglyphus sp.1, Dendracarus sp.1 and Acaridae sp.4 were dominant and specialist. The dominant groups represent 13% of the total species richness.
Table 4: The Berger-Parker index (number of the species/total number of all species in the samples, expressed in percentage) of soil mites in the study site. Value in bold indicated the dominant species.
Species Oume primary forest Oume teak plantation Taï primary forest Lamto savannah Actinedida
Eupodidae sp.1 0.25 0.00 0.00 0.00
Erythraeidae sp.1 0.13 0.00 0.00 0.00
Microtrombidium sp.1 0.00 0.00 0.56 0.45
Microtrombidium sp.2 0.00 0.00 1.11 0.67
Trombella sp.1 0.00 0.00 0.00 0.22
Erythraeidae (larva) 0.00 0.00 0.56 0.00
Trombiculidae sp.1 (larva) 0.00 0.46 0.00 0.00
Bdellidae sp.1 0.00 2.28 0.00 0.00
Camerobia sp.1 0.13 0.00 0.00 0.00
Cunaxidae sp.1 0.00 0.46 0.00 0.00
Scutacaridae sp.1 0.00 0.00 0.00 0.22
Anystidae sp.1 0.13 0.00 0.00 0.00
Actinedide sp.1 (larva) 0.00 0.00 0.56 0.00
Actinedide sp.2 (larva) 0.13 0.00 0.00 0.00
Actinedide sp.3 (larva) 0.00 0.00 0.00 0.22
Actinedide sp.8 0.00 6.39 0.00 0.90
Actinedide sp.12 0.13 0.00 0.00 0.00
Actinedide sp.13 0.00 0.00 0.00 0.22
Gamasida
Evimirus uropodinus 0.00 1.37 0.00 1.12
Fuscuropoda sp.1 0.38 0.00 0.00 0.45
Holocelaeno sp.1 0.51 0.00 0.00 0.00
Hypoaspis sp.1 0.13 0.46 1.11 0.22
Hypoaspis sp.2 0.13 0.46 0.56 0.22
Hypoaspis sp.3 0.00 0.00 0.00 0.22
Ololaelaps sp.1 0.13 0.00 0.56 0.00
Microgynium sp.1 0.00 0.00 0.00 2.02
Microgynium sp.2 0.13 0.00 0.00 0.00
Pachylaelaps sp.1 0.13 0.00 0.00 0.22
Pachylaelaps sp.2 0.13 0.46 0.00 0.00
Rhodacaridae sp.1 0.00 2.74 0.56 0.22
Rhodacaridae sp.2 0.00 0.00 0.00 0.67
Rhodacaridae sp.3 0.13 0.00 0.00 0.22
Rhodacaridae sp.4 0.00 0.00 0.56 0.00
Rhodacaridae sp.5 0.00 0.91 0.00 0.00
Trachyuropodide sp.1 0.51 0.91 1.11 0.00
Trachyuropodide sp.2 3.28 0.00 0.00 0.67
Trachyuropodide sp.3 2.15 1.37 2.78 7.17
Trachyuropodide sp.4 0.00 0.00 0.56 0.00
Trachyuropodide sp.1 (larva) 0.00 0.00 0.56 0.00
Trichouropoda sp.1 0.00 0.46 0.56 0.45
Urodiaspis sp.1 0.51 1.37 0.00 1.57
Uropodidae sp.1 0.00 0.00 1.11 0.00
Uropodidae sp.2 2.40 4.57 0.00 0.90
Uropodidae sp.3 2.78 0.46 1.11 1.12
Uropodidae sp.4 0.25 0.00 0.00 0.00
Epicrius sp.1 0.00 0.00 0.00 0.22
Cosmolaelaps sp.1 0.00 0.00 0.00 0.22
Diplogyniidae sp.1 0.00 0.00 0.00 1.79
Eviphididae sp.1 0.00 0.00 0.00 0.22
Haplozetidae sp.1 0.00 0.00 0.56 0.00
Macrochelidae sp.1 0.00 0.00 0.00 1.35
Afrotrachytes sp.1 28.28 23.29 3.33 28.25
Afrotrachytes (larva) 1.14 0.00 0.00 0.00
Gamaside (polytriche) 0.13 0.00 0.00 0.00
Gamaside sp.1 0.00 0.46 0.00 0.00
Gamaside sp.2 0.13 0.46 0.00 0.00
Gamaside sp.3 0.13 4.11 0.00 0.00
Gamaside sp.4 0.00 0.00 0.56 0.00
Gamaside sp.5 0.13 0.00 0.00 0.00
Gamaside sp.6 0.00 0.00 1.67 0.00
Gamaside sp.7 0.00 0.00 0.00 0.22
Gamaside sp.8 0.00 0.46 0.00 0.22
Gamaside sp.9 0.00 0.00 0.00 0.22
Gamaside sp.10 0.00 0.00 0.00 0.22
Gamaside sp.11 0.25 0.00 0.00 0.90
Gamaside sp.12 0.00 0.00 0.56 0.00
Gamaside sp.13 0.00 0.46 0.56 0.00
Gamaside sp.14 0.38 0.46 1.67 3.14
Gamaside sp.15 0.00 0.00 0.56 0.00
Gamaside sp.16 0.13 0.00 0.56 0.22
Gamaside sp.17 0.25 0.00 0.00 0.00
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Gamaside sp.18 0.38 0.00 0.00 0.00
Gamaside sp.19 0.13 0.00 0.00 0.00
Gamaside sp.20 0.00 0.00 0.56 0.00
Gamaside sp.21 0.00 0.00 1.11 0.00
Gamaside sp.22 0.00 0.00 0.56 0.00
Gamaside sp.23 0.13 0.00 0.00 0.00
Gamaside sp.24 0.00 0.00 0.56 0.00
Gamaside sp.25 0.00 0.46 0.00 0.00
Gamaside sp.26 0.00 0.00 0.56 0.00
Gamaside sp.27 0.13 0.00 0.00 1.12
Gamaside sp.28 0.00 0.00 0.00 0.67
Gamaside sp.29 0.00 0.00 0.56 0.00
Gamaside sp.30 0.00 0.00 0.00 0.22
Gamaside sp.31 0.00 0.00 0.00 0.22
Oribatida
Belbidae sp.1 0.51 0.46 1.11 0.00
Belbidae sp.2 0.76 0.46 0.00 1.35
Quatrobelba sp.1 0.38 0.00 0.00 0.00
Lamellobates palustris 2.27 0.46 0.56 0.22
Paralamellobates schoutedeni 0.13 1.37 0.00 0.00
Lamellobates sp.3 0.00 0.00 0.00 0.22
Lamellobates sp.4 0.00 0.00 0.56 0.00
Lamellobates (larva) 0.13 0.00 0.00 0.00
Nothrus sp.1 0.00 0.91 0.00 0.00
Nothridae sp.1 0.13 0.00 0.00 0.00
Nothridae sp.2 0.00 0.00 0.00 0.22
Allonothrus sp.1 0.00 0.00 0.00 0.22
Malaconothrus sp.1 0.13 0.46 0.00 0.67
Malacoangelia sp.1 0.76 0.00 1.11 0.00
Malaconothrus sp.3 0.51 0.00 0.00 0.00
Lopheremaeus mirabilis 0.38 0.00 0.00 0.00
Paralopheremaeus legendrei 0.00 3.20 0.56 0.45
Mycobatidae sp.1 0.13 0.00 0.00 0.00
Mycobatidae sp.2 4.42 3.65 0.56 0.67
Mycobatidae sp.3 0.63 0.00 0.00 0.90
Oribatulidae sp.1 0.88 0.91 1.11 0.00
Oribatulidae (larva) 0.00 0.46 0.00 0.00
Oribatulidae (Protonymphae) 0.00 0.00 5.00 0.45
Sphaerochtonius sp.1 0.13 0.00 0.00 0.00
Sabahtritia sp.1 1.01 0.00 1.11 0.22
Mesoplophora sp.1 2.27 0.46 0.00 0.22
Mesoplophoridae sp.1 0.00 0.00 0.00 0.45
Dolicheremaeus sp.1 1.39 0.00 0.56 0.00
Lohmanniidae sp.2 0.25 0.00 1.67 0.00
Lohmanniidae sp.3 0.25 0.00 0.00 0.00
Epilohmannia sp.1 1.52 4.57 2.22 1.35
Phyllolohmannia sp.1 0.00 0.00 0.00 0.22
Lohmannia sp.1 0.25 0.00 0.00 0.00
Euphthiracarus sp.1 0.13 0.00 0.56 0.00
Euphthiracarus sp.2 0.76 0.46 0.56 0.22
Euphthiracaridae sp.1 0.00 0.00 0.00 0.22
Phthiracarus sp.4 0.63 0.00 1.67 0.45
Austracarus sp.1 0.13 0.00 0.00 0.00
Meristacarus sp.1 3.28 5.02 0.56 0.67
Mixacarus sp.1 1.14 0.00 1.11 0.00
Rhysotritia duplicata 0.63 3.20 0.00 2.47
Oppia sp.1 0.76 0.00 0.00 0.00
Oppia sp.2 2.65 0.91 19.44 4.48
Oppiidae sp.1 0.00 0.00 5.00 0.22
Galumna sp.4 1.77 0.00 8.89 1.57
Galumna sp.5 3.03 0.00 1.67 0.45
Galumna sp.6 1.01 0.00 0.00 0.45
Galumna sp.9 0.13 0.91 0.00 0.00
Galumna sp.10 2.78 0.00 1.11 0.00
Galumna sp.11 0.13 0.91 0.56 1.57
Galumna sp.12 0.00 0.00 0.00 0.45
Heterogalumna sp.1 0.00 0.00 0.00 0.45
Scheloribatidae sp.1 0.00 0.46 0.56 0.00
Euscheloribates sp.1 0.00 0.00 0.00 0.22
Damaeus onustus 0.38 0.00 0.00 0.00
Damaeidae sp.2 0.13 0.00 0.00 0.00
Damaeidae sp.3 0.13 0.00 0.00 1.12
Damaeidae sp.4 0.00 0.00 0.56 0.00
Cosmochthonius sp.1 0.00 0.00 0.56 0.00
Dendracarus sp.1 0.00 0.00 0.00 3.14
Neocarabodes sp.1 0.25 0.00 0.00 0.00
Carabodes sp.1 2.40 0.46 0.00 0.00
Carabodidae sp.1 1.26 0.46 0.00 0.45
Cepheus sp.1 0.25 0.46 0.00 0.00
Cepheidae sp.2 0.13 0.00 0.00 0.00
Cepheidae sp.3 0.00 0.00 0.00 0.22
Oribate (Tritonympha) 0.13 0.00 0.00 0.00
Xylobatidae sp.1 0.00 0.00 0.56 0.45
Xylobatidae sp.2 0.38 1.37 0.00 0.00
Xylobatidae sp.3 0.13 0.00 0.56 0.45
Xylobatidae sp.4 0.13 0.00 0.56 0.45
Galumnellidae sp.1 0.25 0.00 0.00 0.00
Galumnellidae sp.2 0.38 0.00 0.00 0.22
Hamobates sp.1 0.13 0.00 0.00 0.00
Afronothrus sp.1 0.25 1.83 2.78 0.45
Saxicolestes sp.1 0.00 0.00 2.78 0.00
Oribate sp.1 0.88 3.65 2.22 0.90
Oribate sp.10 0.00 0.46 0.00 0.00
Oribate sp.32 0.13 0.00 0.00 0.00
Oribate sp.43 0.13 0.00 0.00 0.00
Oribate sp.49 0.00 0.00 0.00 0.90
Oribate sp.52 0.00 0.00 0.56 0.00
Platyliodes sp.1 0.13 0.00 0.00 0.00
Endeostigmate sp.1 0.00 0.00 0.00 0.22
Endeostigmate sp.2 0.13 0.00 0.00 0.00
Acaridida
Acaridae sp.1 0.88 0.00 1.67 0.00
Acaridae sp.2 0.00 0.00 0.00 0.22
Acaridae sp.3 0.00 0.00 0.00 0.22
Acaridae sp.4 3.16 0.00 0.00 0.00
Rhysoglyphus sp.1 0.00 3.20 0.00 0.00
Rhysoglyphus sp.2 0.00 3.65 0.00 0.22
Rhysoglyphus sp.3 3.54 0.00 1.67 8.74
Number of taxonomic groups 98 52 66 85
Number of dominant groups 7 12 5 6
Ratio Oribatida / Actinedida 52.28 3.95 24.8 10.53
4.4 Variation in soil quality: A part from the bulk density, all abiotic factors data were
significantly different (P < 0.05) between sites.
Water contents mean values were higher in Taï
4633 primary forest (17.15%). Soil pH-H2O mean values were acid in Taï primary forest and basic in the others sites (Table 5). As for Corg (g/kg), Ctot (%), Ntot (%), C/N, SOM (g/kg), results showed that values were higher in the upper (0-5
cm) layer than in deep soils. In general, these values were higher in Oume (SOM-rich sites) and Taï (SOM-moderate sites) primary forest relative to Lamto savannah (SOM-poor sites) and Oume teak plantation (SOM-less sites).
Table 5: Soil characteristics, (mean ± standard error) values measured in the two extreme layers (0-5 cm and 35-40 cm) and entire profile (0-40 cm) of mineral soils in the four sites. Extreme layers (N = 10), entire profile (N = 16). P-values of one-way ANOVA tests.
Oume primary forest Taï primary forest Lamto savannah Teak plantation p values
31.70 ± 4.50 20.7 ± 2.08 10.7 ± 1.14 16.70 ± 1.13 0.0004 ***
3.17 ± 0.45 2.07 ± 0.21 1.07 ± 0.12 1.70 ± 0.14 0.0006 ***
0.32 ± 0.05 0.17 ± 0.02 0.1 ± 0.02 0.18 ± 0.02 0.0002 ***
9.81 ± 0.28 12.49 ± 0.46 10.81 ± 0.19 9.43 ± 0.17 0.0001 ***
53.89 ± 7.64 35.19 ± 3.54 18.19 ± 1.93 28.39 ± 1.93 0.0004 ***
5.74 ± 0.36 6.6 ± 0.49 5.3 ± 0 5.44 ± 0.14 0.0386 *
0.58 ± 0.04 0.66 ± 0.05 0.53 ± 0 0.54 ± 0.01 0.0386 *
0.05 ± 0.01 0.06 ± 0.01 0.03 ± 0 0.05 ± 0.01 0.0165 *
12.27 ± 1.07 11.43 ± 0.34 16.79 ± 0.54 12.63 ± 1.15 0.0007 ***
9.76 ± 0.61 11.22 ± 0.83 9.01 ± 0 9.25 ± 0.24 0.0386 *
1.13 ± 0.05 1.09 ± 0.04 0.97 ± 0.04 1.05 ± 0.05 0.5368 ns 11.16 ± 0.68 17.15 ± 1.11 11.35 ± 0.92 15.36 ± 0.89 0.0101 *
7.35 ± 0.05 5.94 ± 0.04 6.51 ± 0.05 7.33 ± 0.05 0.0001 ***
Significant at levels 0.05 (*), 0.01 (**) and 0.001 (***).
4.5 Patterns of species indicators assemblages and mesological factors across the sites: A PCA on correlation matrix was done on the data consisting of 35 variables (i.e.
mesological variables and species indicators listed in Table 3) and 4 objects (i.e. sites). The correlation circle (Fig. 1A) showed an assemblage pattern of variables within the sites with the first two axes accounting for 31% of the total inertia.
The first axis (23%) indicated moderate differences in mesological and biological factors since the variables were either positively or negatively correlated (Fig. 1A). Bulk density (BD), depth, carbon / nitrogen (C/N) were correlated positively to the first axis whereas total nitrogen (Ntot), soil organic matter (SOM), organic carbon (Corg), total carbon (Ctot), water content (WC), Galumna sp.5, Trachyuropodide sp.2, and Uropodide sp.3 were negatively correlated to
the same axis. The second axis revealed less difference in biotic and abiotic factors, nevertheless Malacoangelia sp.1, Galumna sp.10, Mesoplophora sp.1, Carabodes sp.1, Potential of Hydrogen (pH), Afrotrachytes (larva) were positively correlated to the second axis while Actinedide sp.8, Mycrogynium sp.1, Oribatulidae (Protonymphae), Trachyuropodide sp.3 and Galumna sp.4 were negatively correlated to the same axis.
The ordination of sites across the zones and localities revealed the impact of two ecological factors (Fig. 1B). First, the availability of soil organic resources from the sites influences moderately the change in species indicators richness composition. Following the axis 1, organic resources (Corg (g/kg), Ctot (%), Ntot (%), SOM (g/kg)) decrease from Oume primary forest to Lamto savannah. The second factor was related to the disturbance state of the forest since
the first axis separated less and undisturbed habitats from moderately and highly disturbed
systems.
CtotCorg Ntot
C/N SOM
Depth BD
WC
pH
Ori9
Gal4 OriP
Gam3 Af1
Me1 Gal10
Gal5 Ori26 Ori1
Tra2
Lam1 Par1
Uro3
Aca4 Dol1 Mer1
Sab1 Mal1 Afl
Tra3 Mac1
Den1
Myc1 Gam14
Act8
-1 1 -1 1
Axis 2 (8%)
A
Axis 1 (23%)
-2.2 2.2 -3 3
OTK
TPF LAS Axis 1 (23%) OPF Axis 2 (8%)
B
Figure 1: A. Correlation circle of the PCA showing the general pattern of distribution in abiotic factors and species indicators across the four sites. B. Projection of sites on the factorial planes 1–2, (Bulk density (BD), Depth, Water content (WC), total carbon (Ctot), organic carbon (Corg), Soil organic matter (SOM), total nitrogen (Ntot), Potential of Hydrogen (pH), ratio Carbon / Nitrogen (C/N), Oppia sp.2 (Ori9), Galumna sp.4 (Gal4), Oribatulidae (Protonymphae) (OriP), Gamaside sp.3 (Gam3), Afrotrachytes sp.1 (Af1), Mesoplophora sp.1 (Me1), Galumna sp.10 (Gal10), Galumna sp.5 (Gal5), Carabodes sp.1 (Ori26), Mycobatidae sp.2 (Ori1), Trachyuropodide sp.2 (Tra2), Lamellobates palustris (Lam1), Lopheremaeus mirabilis (Par1), Uropodide sp.3 (Uro3), Acaridea sp.4 (Aca4), Dolicheremaeus sp.1 (Dol1), Meristacarus sp.1 (Mer1), Sabahtritia sp.1 (Sab1), Malacoangelia sp.1 (Mal1), Afrotrachytes (larva) (Afl), Trachyuropodide sp.3 (Tra3), Macrochelidae sp.1 (Mac1), Dendracarus sp.1 (Den1), Mycrogynium sp.1 (Myc1), Gamaside sp.14 (Gam14), Actinedide sp.8 (Act8)).
5 DISCUSSION
5.1 Soil quality, disturbance and indicators species: Traditional approaches to soil quality evaluation were based on the use of physical, chemical and microbiological indicators (Parisi et al., 2005). Recently, although not new, the use of bioindicators is an innovative approach for assessing various types of environmental mismanagement (Paoletti, 1999). The ordination made revealed that all species indicators and environmental parameters varied independently of the bulk density and soil depth. The affinity between organic matters and soil Oribatida in most terrestrial ecosystems was outlined by Behan-Pelletier (1999). Indeed, in this study, most species sampled were recorded in the topsoil (organic horizons) where nutrients
resources were abundant. The Oribatida use soil organic matters as nutrients resources for their development and reproduction. All terrestrial ecosystems consist of aboveground and belowground biodiversity that interact to influence the community and the process at different levels (Wardle et al., 2004). This assertion agrees with our data (see Table 2) because indicators species characterizing the Guinean domain (undisturbed site) and represented by Taï primary forest were highly different to those observed in Sudanese domain (disturbed sites). In Taï, vegetation cover limits severely the incident light penetration (Alexandre, 1982; Koné, 2004). The Guinean domain is also characterized by a high precipitation and an
4634 absence of anthropic perturbation. In Taï, soil was acid. Vegetation and soil type associated to climate characteristics contribute strongly for clustering the mite richness and may be used as indicator of health state of the different ecosystems foresters (Gergócs and Hufnagel, 2009; Proctor et al., 2011; Sabbatini- Peverieri et al., 2011; Zhao et al., 2013). If we considered the four sites and distinguished between litter and mineral soil (see Table 3), we remarked that the major species indicators arising to Oume primary forest, where a large amount organic matter and a moderate disturbed were observed. However, a weak number of indicators species were observed in Oume teak plantation, where a high disturbance (clearing and cutting) was recorded.
This site was characterized by a monospecific timber, limiting the heterogeneity of litter type, principal source of organic matter. In fact, the mite and particularly Oribatid (phytophagous, saprophagous) have a potentiality to respond quantitatively and qualitatively to short-term environmental alteration. On the other hand, the modification of the microhabitats, and the mite community structure due to clearing, cutting or agriculture practice could eliminates some species, specifically those with a life cycle longer than one year (Behan-Pelletier, 1999). However, the loss of particular species may seem to have no direct impact on soil quality, but it may severely affect those species with more direct roles through food web interactions (Stork and Eggleton, 1992). Lamto savannah soil was characterized by a very low organic matter and nitrogen content (SOM-poor site) compared to the other three sites. This trend was confirmed by several studies in the same area (Mordelet et al., 1996; Le Roux, 2006). Indeed Lamto vegetation was composed by discontinuous layer of trees and a shrub dominated by tall palm trees (Borassus aethiopum) and Chromolaena odorata (Asteraceae) by location. Despite its protected status, and its transition for reforestation, a less disturbed was established. Species indicators from Lamto locality or site were attributed to Oribatids (Dendracarus sp.1, Galumna sp.11, Damaeidae sp.3,
Oribate sp.49) and Gamasids (Trachyuropodide sp.3, Mycrogynium sp.1, Gamaside sp.14, Evimirus uropodinus, Macrochelidae sp.1), two majors taxa with a different trophical group, respectively (phytophagous, saprophagous) and (predatious, fungivorous).
5.2 Bioindicators importance and soil mite variation: Indicators of ecological integrity may be found at many organizational levels including species, stand, landscape and ecosystem (Carignan and Villard, 2002). The methodology aiming at defining indicator species is reviewed by Carignan and Villard (2002) who conclude that each study presents arguments on the suitability of each taxon as a potential indicator.
The type of food ingested by the mite varies greatly depending on the life stage. Despite the plasticity of the trophical resource and their very low mobility by active movement (Berthet, 1964), some competition risks can be observed. Intra or interspecific relations (competition) and the resource sharing (Anderson, 1978), predation, dispersal-limited, diversity of timber type, and ecological niches, the phorésie (Athias-Binche, 1994), the habitat type and trophical resource complexity contribute optionally to control the variability of bioindicators species number (Gulvik, 2007; Gergócs and Hufnagel, 2009).
Nevertheless the number of species bioindicators of health state from the Habitat investigated increased with the species richness (see Table 3).
Changes in the dominance structure of mite communities (Oribatida to Actinedida ratio) are suggested to be an “early warning” criterion for stressed mite communities (Gulvik, 2007). Indeed the value of Oribatida-Actinedida ratio varied from 3.95 in teak plantation to 52.28 in Oume primary forest. This observation was so close to remark from Werner and Dindal (1990). These authors conclude that the value of Oribatida- Actinedida ratio ranged below 1.0 in arable fields and above 1.0 in more stable ecosystem, such agrosystem and natural forests. According to (Gulvik, 2007), increases in actinedids may reflect recent disturbance.
6 CONCLUSION
It is true that some characteristics such as the Maturity Index (MI) based on ranking Gamasid mite taxa (r/k scale) and functional groups have not been taken in consideration in this investigation. Nevertheless, this study gives a first insight on the potential use of some defined
species of soil fauna in characterizing the ecosystems of West Africa, of their climatic influence, their soil composition and the level of anthropic perturbation or restoration. It highlights the need for a deep taxonomic work for this unknown compartment of biodiversity.
7 ACKNOWLEDGEMENTS
Thanks to R. Jocqué, Y. Samyn, and D. Van Den Spiegel for advices and grants. Financial supports from CSM-BGBD project, FRS/UCL, Philippe
Lebrun Fund, GTI/IRScNB, ABIC/MRAC are gratefully acknowledged.
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