Journal of &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

Microarthropod use as bioindicators of the environmental state: case of soil () from Côte d’Ivoire.

Julien Kouadio N’Dri 1* , Thierry Hance 2, Henri Marc André 3, Jan Lagerlöf 4, Jérôme Ebagnérin Tondoh 1 1 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, 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: , 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.1 whereas three species, respectively Rhysoglyphus sp.1, Dendracarus sp.1 and Acaridae sp.4 were dominant and specialist. Chemical elements Corg (g/kg), C tot (%), N tot (%), 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 -Actinedida ratio ranged from 3.95 in teak plantation to 52.28 in Oume primary forest.

2 INTRODUCTION Value of biodiversity conservation has been developed to measure the biological diversity recognized worldwide (Bonn and Gaston, 2005; (Shannon, 1962; Pielou, 1969; Whittaker, 1972); Humphrey, 2005), notably because the erosion of however, they present some bias such as biodiversity elements can cause impoverished overestimating or underestimating the role of rare ecosystem functioning (Mertz et al., 2007). species. In that context, Dufrêne and Legendre However, biodiversity indicators are still needed (1997) renewed the notion of indicators by to assess changes due to ecosystems management combining the relative abundance of a species and global change. Several indices have been with its relative frequency of occurrence in 4622 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

defined groups of sites. This approach seems richness, trophic groups, functional groups), and particularly sound for monitoring of soil characteristics of the biological process ecosystem changes and biodiversity conditions (bioaccumulation, soil modification). From this because its cost-effective, indicators are easily and point of view, mites or others soil reliably identified, the indicators represent eco- microarthropods species and species assemblages functionally important species, and respond offer several advantages for assessing the quality differently to disturbance regimes (Pearce and of soil ecosystems (Behan-Pelletier, 1999; Parisi et Venier, 2006; Guéi and Tondoh, 2012). Many al., 2005; Gulvik, 2007; Gergócs & Hufnagel, definitions have been attributed to the notion of 2009; Proctor et al., 2011; Sabbatini-Peverieri et indicators (Maleque et al., 2009). Nevertheless, the al., 2011; Zhao et al., 2013). Most soil mites live in biological indicators are recognized as being the organic horizons, play an essential role in organisms or communities of organisms which organic matter decomposition but also represent reaction are observed representatively to evaluate a trophically heterogenous group with predators, the state or the health of an ecosystem (Ferris detripagous and mycopagous species. Previous and Humphrey, 1999; Walz, 2000; Burger, 2006; study in South African soils showed that Gerhardt, 2012). According to the different Oribatida dominate the forest soil while applications of biological indicators, three groups Trombidiform mites were more abundant in the can be distinguished: (1) environmental indicator, savannah (Olivier and Ryke, 1965; Loots and where species responding predictably to Ryke, 1967). In contrast to the anaerobic process environmental disturbance or change,(2) of fermentation and putrefaction causing an ecological indicator, where species are known to increase of Acaridida, a best porosity (aeration) of be sensitive to pollution and habitat the soil promotes the development and fragmentation,(3) biodiversity indicator, where emergence of Oribatida (Ducarme et al., 2004). species richness of an indicator taxon is used as The identification of characteristic or indicator indicator for species richness of a community species is a current practice in ecology and (Gerhardt, 2012). Direct measurement of soil biogeography. Field studies describing sites or biodiversity is expensive, and therefore a habitats usually mention one or several species substitution of measurement by indication is that characterize each habitat. However, there is a desirable (Ekschmitt et al., 2003). The different clear lack of data concerning the African soil properties of soil , which can be mesofauna. Our aim was to provide a first insight potentially used as indicators of soils quality was into this field by extraction of potential indicator listed by Linden et al. (1994). These include single species of a completely new set of data sampled organism level characteristics (behaviour, in well-contrasted ecosystems. development), community characteristics (species

3 MATERIAL AND METHODS 3.1 Study sites and sampling design: Four 30-35 cm, 35-40 cm), with a steel corer ( ∅ 3.5 sites located in Ivory Coast were studied: Lamto cm). A total of 270 soil cores were taken at each savannah (Coordinates: 6°13' N, 5°02' W; site and along the entire soil profile for altitude: 125 m asl) and Oumé primary forest and extracting. Another set of 240 soil cores were Teak plantation (Coordinates: 6°31’ N, 5°30’ W; taken for physico-chemical analysis. More details altitude: 200 m asl) situated in Sudanese domain concerning the sampling are given by N’Dri and and the Tai primary forest (Coordinates: 5°45’ N, André (2011), and other descriptions relative to 7°07 W; altitude: 150-200 m asl) based in the site such as climate regime, temperature, Guinean domain. Each site was sampled twice rainfall pattern, vegetation and soil type are during 2008 at different depth (Litter, 0-5 cm, 5- presented in Table 1. 10 cm, 10-15 cm, 15-20 cm, 20-25 cm, 25-30 cm,

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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 26°C 25.35°C (1993-2002) 34.58°C 26°C (1998-2007) Temperature of the study years 25.9°C ----- 36.99°C 25.9°C (2008) Precipitation of the last 10 years 1447.9 mm 1853.2 mm (1993-2002) 1270.02 mm 1447.9 mm (1998-2007) Precipitation of the study years 1592 mm ----- 1211.4 mm 1592 mm (2008) Vegetation characteristics Semi-deciduous forest Humid forest Discontinuous layer of trees and 14-year-old teak shrubs dominated by tall palm (mesophile type) 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)

Moderately disturbed site Levels of the disturbance Undisturbed site Less disturbed site Highly disturbed site and and limited to clearing and limited to some tracks cutting ----- No available

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3.2 Mite extraction and identification: where Nsites ij is the number of sites in -group j The mesofauna was extracted during 1-week where species i is present, and Nsites j is the total using a Berlese-Tullgren system. The extracted number of sites in that group. The percentage microarthropods were poured into a Petri-dish indicator value for species i in-group of sites j is: from where the mites were sorted from the rest of the microarthropods in 70% ethanol and IndValij = A ij × B ij × 100 counted under a binocular microscope. The indicator value for species i is: Temporary mounts of specimens were made and IndVali = max [ IndValij ] examined thoroughly for fine taxonomic details under the compound microscope. In the absence Hierarchical classification of samples (clusters) of African keys, identification of mites was done based mostly on sites characteristic was used for at species level or as morphospecies (i.e., data analysis whereas groups represent the individuals that differed from morphological different partitioning level (climatic zones, features), using keys and illustrations provided in localities, sites and litter vs. mineral soil). Balogh and Balogh (1992), Krantz (1978), Dindal Contrary to Dufrêne and Legendre (1997), where (1990) and Krantz and Walter (2009). Respective only IndVal index significant at P ≤ 0.01 and photographs were treated with AUTO -MONTAGE superior to 25% have been taken in and classified in a database. Reference collection consideration, all species that have an index value and database were deposited in the African significant at P < 0.05 are presented in the Museum of Tervuren, Belgium. different tables. Two IndVal analyses were done. 3.3 Mesological factors analysis: The pH- According to the initial analysis, the first level of

H2O (Baize, 1988) was measured with a pH the classification separated climatic zones meter (HANNA) in 960 mineral soil cores. Bulk (Guinean vs. Sudanese) following the density (g.cm -3) and soil water content (WC) from precipitation level and soil pH type. The second 960 mineral soil samples were measured after 48 level separated localities (Oumé vs. Lamto vs. h drying at 105°C (Baize, 1988). Other chemical Taï) according to vegetation type and Ctot (%), analyses such as organic carbon (C org ), total Ntot (%) content and distinguished high SOM- carbon (C tot ), total nitrogen (N tot ), ratio carbon / content sites (SOM-rich sites) from low C tot (%), nitrogen (C/N), soil organic matters (SOM) from Ntot (%) content ones (SOM-poor sites). The extreme layers (0-5 cm and 35-40 cm) were level 3 segregated sites depending on the level of realized on 80 samples by the “Centre Provincial disturbance: undisturbed sites (Taï primary de l’Agriculture et de la Ruralité” in La Hulpe forest), less disturbed sites (Lamto savannah), (Belgium). Soil analyses were realized on the moderately disturbed sites (Oume primary forest) upper and bottom layers (0–5 cm and 35–40 cm) and highly disturbed sites (Oume teak in order to assess correlation between soil plantation). A second analysis opposes litter characteristics and species indicators. dwelling to mineral soil dwelling mites 3.4 Data analysis: The indicator value (microhabitat). As like to Badejo and Ola-adams (IndVal ) was calculated for each morphospecies, (2000), Kaczmarek and Marquardt (2010), the as described by Dufrêne and Legendre (1997): Berger-Parker Dominance Index for each Specificity (A ij ), Aij = Nindividuals ij / taxonomic group was done. This index is a Nindividuals i measure of the percentage contribution of a where Nindividuals ij is the mean number of taxonomic group to the total number of mites in species i across sites of group j, and each site. Generic level taxa that provided 3% or Nindividuals i is the sum of the mean number of more of the total density of mites in a site are individuals of species i over all groups. regarded as dominant. The mites were not named Fidelity (B ij ), Bij = Nsites ij /Nsites j according to the Code of Zoological Nomenclature because the lack of taxonomic

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information for African soil mites.Soil component analysis (PCA) was done to analyze mesological factors means were compared using a the effects of land-use type (sites) on both species one-way ANOVA test. These tests were indicators (listed in Table 3) and mesological conducted using the software Statistica 7.0 factors. These analyses used the module ‘PCA’ of (StatSoft Inc., 1984–2004). At last, a principal the software ADE-4 (Thioulouse et al., 1997).

4 RESULTS 4.1 Species indicator of the different basic soil, despite a richness estimated at 149 sites: In all, 177 soil mites species were species. Nine species, four oribatids and five identified (Lamto savannah: 85, Oume primary gamasids, are indicators of Lamto locality (SOM- forest: 98, Oume teak plantation: 52 and Taï poor site), whereas a single oribatid, Meristacarus primary forest: 66 species). On 66 species from sp.1, is indicator of the locality of Oumé (SOM- the Guinean zone (Taï primary forest), only four rich sites). If sites are considered, two species, a species, three oribatids and one uropodid, can be gamasid, Gamaside sp.3 and an acaridid, considered as indicators of that zone where the Rhysoglyphus sp.1, are indicators of the Teak precipitation level was high with an acid soil. In plantation (highly disturbed site). 15 mites (Table contrast, three species are indicators of the 2) are also indicator species of Oume primary Sudanese zone with a low precipitation and a 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

Gal umna 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

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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

Do licheremaeus 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 primary forest, while only a single gamasid is second partition in 2 microhabitats, litter vs. indicator of litter in Oume teak plantation. In mineral soil, was made in all sites (data from all mineral soil, a single Actinedida, Actinedide sp.8 is site was pooled). A single oribatid is an indicator indicator of Oume teak plantation. The number species of litter, Oppiidae sp.1. In contrast, of indicator species rises to five in Lamto Rhysotritia duplicata and two savannah and to 16 in Oume primary forest. Afrotrachytes sp.1 and Uropodidae sp.2 are There is no indicator species of litter in Oume indicator species of mineral soil. If sites are primary forest and Lamto savannah, neither of considered, i.e. if all samples are partitioned into mineral soil in Taï primary forest. Whatever the 8 groups (litter and mineral soil from the four partitioning and the type of habitats investigated, sites), the list of species indicator of the indicators species represents 21% of the total microhabitats is much longer (Table 3). Three species richness. oribatids are species indicator of litter in Taï

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 s p.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

Afrot rachytes (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 Meristacarus sp.1 (3.28-5.02%), Rhysotritia duplicata Berger-Parker Dominance Index for each (3.20%), Galumna sp.4 (8.89%), Galumna sp.5 taxonomic group is presented in Table 4. The (3.03%), Dendracarus sp.1 (3.14%), Oribate sp.1 value of this number varied between five (Taï (3.65%), Oppiidae sp.1 (5.00%), Oppia sp.2 (4.48- primary forest) and 12 (Oume teak plantation). 19.44%), Acaridae sp.4 (3.16%), Rhysoglyphus sp.1 At the scale of the four sampling sites, 23 species (3.20%), Rhysoglyphus sp.2 (3.65%), Rhysoglyphus were dominants: Actinedide sp.8 (6.39%), sp.3 (3.54-8.74%) . In addition, only one species Trachyuropodide sp.2 (3.28%), Trachyuropodide sp.3 was dominant and ubiquitous, particularly (7.17%), Uropodide sp.2 (4.57%), Afrotrachytes sp.1 Afrotrachytes sp.1 whereas three species, (3.33-28.28%), Gamaside sp.3 (4.11%), Gamaside respectively Rhysoglyphus sp.1, Dendracarus sp.1 and sp.14 (3.14%), Paralopheremaeus legendrei (3.20%), Acaridae sp.4 were dominant and specialist. The Mycobatidae sp.2 (3.65-4.42%), Oribatulidae dominant groups represent 13% of the total (Protonymphae) (5.00%), Epilohmannia sp.1 (4.57%), 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 4628 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

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 4629 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

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 4630 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

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 significantly different (P < 0.05) between sites. the bulk density, all abiotic factors data were Water contents mean values were higher in Taï 4631 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

primary forest (17.15%). Soil pH-H2O mean cm) layer than in deep soils. In general, these values were acid in Taï primary forest and basic values were higher in Oume (SOM-rich sites) and in the others sites (Table 5). As for C org (g/kg), Taï (SOM-moderate sites) primary forest relative Ctot (%), N tot (%), C/N, SOM (g/kg), results to Lamto savannah (SOM-poor sites) and Oume showed that values were higher in the upper (0-5 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 the same axis. The second axis revealed less assemblages and mesological factors across difference in biotic and abiotic factors, the sites: A PCA on correlation matrix was done nevertheless Malacoangelia sp.1, Galumna sp.10, on the data consisting of 35 variables (i.e. Mesoplophora sp.1, Carabodes sp.1, Potential of mesological variables and species indicators listed Hydrogen (pH), Afrotrachytes (larva) were in Table 3) and 4 objects (i.e. sites). The positively correlated to the second axis while correlation circle (Fig. 1A) showed an assemblage Actinedide sp.8, Mycrogynium sp.1, Oribatulidae pattern of variables within the sites with the first (Protonymphae), Trachyuropodide sp.3 and Galumna two axes accounting for 31% of the total inertia. sp.4 were negatively correlated to the same axis. The first axis (23%) indicated moderate The ordination of sites across the zones and differences in mesological and biological factors localities revealed the impact of two ecological since the variables were either positively or factors (Fig. 1B). First, the availability of soil negatively correlated (Fig. 1A). Bulk density organic resources from the sites influences (BD), depth, carbon / nitrogen (C/N) were moderately the change in species indicators correlated positively to the first axis whereas total richness composition. Following the axis 1, nitrogen (N tot ), soil organic matter (SOM), organic resources (C org (g/kg), C tot (%), N tot (%), organic carbon (Corg), total carbon (C tot ), water SOM (g/kg)) decrease from Oume primary forest content (WC), Galumna sp.5, Trachyuropodide sp.2, to Lamto savannah. The second factor was and Uropodide sp.3 were negatively correlated to related to the disturbance state of the forest since 4633 Journal of Animal &Plant Sciences, 2016. Vol.29, Issue 2: 4622-4637 Publication date 1/07/2016, http://www.m.elewa.org/JAPS ; ISSN 2071-7024

the first axis separated less and undisturbed systems. habitats from moderately and highly disturbed

1 2.2 A -1 1 B -3 3 -1 -2.2

Me1 Gal10Mal1

Afl Ori26 pH Ori1 OPF Axis2 (8%) Af1 Axis2 (8%) Sab1 Gam3 Depth Mer1 Ori9 BD OTK Lam1 Ntot Par1Aca4Dol1 Axis 1 (23%) SOM Den1 Axis 1 (23%) Corg Ctot Mac1 Gal5 Gam14 C/N WC Tra2 Uro3 OriP Act8 Myc1 LAS Tra3 TPF

Gal4

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 (C tot ), organic carbon (Corg), Soil organic matter (SOM), total nitrogen (N tot ), 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 resources were abundant. The Oribatida use soil indicators species: Traditional approaches to organic matters as nutrients resources for their soil quality evaluation were based on the use of development and reproduction. All terrestrial physical, chemical and microbiological indicators ecosystems consist of aboveground and (Parisi et al., 2005). Recently, although not new, belowground biodiversity that interact to the use of bioindicators is an innovative approach influence the community and the process at for assessing various types of environmental different levels (Wardle et al., 2004). This mismanagement (Paoletti, 1999). The ordination assertion agrees with our data (see Table 2) made revealed that all species indicators and because indicators species characterizing the environmental parameters varied independently Guinean domain (undisturbed site) and of the bulk density and soil depth. The affinity represented by Taï primary forest were highly between organic matters and soil Oribatida in different to those observed in Sudanese domain most terrestrial ecosystems was outlined by (disturbed sites). In Taï, vegetation cover limits Behan-Pelletier (1999). Indeed, in this study, severely the incident light penetration (Alexandre, most species sampled were recorded in the 1982; Koné, 2004). The Guinean domain is also topsoil (organic horizons) where nutrients characterized by a high precipitation and an

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absence of anthropic perturbation. In Taï, soil Oribate sp.49) and Gamasids ( Trachyuropodide sp.3, was acid. Vegetation and soil type associated to Mycrogynium sp.1, Gamaside sp.14, Evimirus climate characteristics contribute strongly for uropodinus , Macrochelidae sp.1), two majors taxa clustering the mite richness and may be used as with a different trophical group, respectively indicator of health state of the different (phytophagous, saprophagous) and (predatious, ecosystems foresters (Gergócs and Hufnagel, fungivorous). 2009; Proctor et al., 2011; Sabbatini- Peverieri et 5.2 Bioindicators importance and soil al., 2011; Zhao et al., 2013). If we considered the mite variation: Indicators of ecological integrity four sites and distinguished between litter and may be found at many organizational levels mineral soil (see Table 3), we remarked that the including species, stand, landscape and ecosystem major species indicators arising to Oume primary (Carignan and Villard, 2002). The methodology forest, where a large amount organic matter and a aiming at defining indicator species is reviewed moderate disturbed were observed. However, a by Carignan and Villard (2002) who conclude weak number of indicators species were observed that each study presents arguments on the in Oume teak plantation, where a high suitability of each taxon as a potential indicator. disturbance (clearing and cutting) was recorded. The type of food ingested by the mite varies This site was characterized by a monospecific greatly depending on the life stage. Despite the timber, limiting the heterogeneity of litter type, plasticity of the trophical resource and their very principal source of organic matter. In fact, the low mobility by active movement (Berthet, 1964), mite and particularly Oribatid (phytophagous, some competition risks can be observed. Intra or saprophagous) have a potentiality to respond interspecific relations (competition) and the quantitatively and qualitatively to short-term resource sharing (Anderson, 1978), predation, environmental alteration. On the other hand, the dispersal-limited, diversity of timber type, and modification of the microhabitats, and the mite ecological niches, the phorésie (Athias-Binche, community structure due to clearing, cutting or 1994), the habitat type and trophical resource agriculture practice could eliminates some complexity contribute optionally to control the species, specifically those with a life cycle longer variability of bioindicators species number than one year (Behan-Pelletier, 1999). However, (Gulvik, 2007; Gergócs and Hufnagel, 2009). the loss of particular species may seem to have Nevertheless the number of species bioindicators no direct impact on soil quality, but it may of health state from the Habitat investigated severely affect those species with more direct increased with the species richness (see Table 3). roles through food web interactions (Stork and Changes in the dominance structure of mite Eggleton, 1992). Lamto savannah soil was communities (Oribatida to Actinedida ratio) are characterized by a very low organic matter and suggested to be an “early warning” criterion for nitrogen content (SOM-poor site) compared to stressed mite communities (Gulvik, 2007). Indeed the other three sites. This trend was confirmed by the value of Oribatida-Actinedida ratio varied several studies in the same area (Mordelet et al., from 3.95 in teak plantation to 52.28 in Oume 1996; Le Roux, 2006). Indeed Lamto vegetation primary forest. This observation was so close to was composed by discontinuous layer of trees remark from Werner and Dindal (1990). These and a shrub dominated by tall palm trees ( Borassus authors conclude that the value of Oribatida- aethiopum ) and Chromolaena odorata (Asteraceae) by Actinedida ratio ranged below 1.0 in arable fields location. Despite its protected status, and its and above 1.0 in more stable ecosystem, such transition for reforestation, a less disturbed was agrosystem and natural forests. According to established. Species indicators from Lamto (Gulvik, 2007), increases in actinedids may reflect locality or site were attributed to Oribatids recent disturbance. (Dendracarus sp.1, Galumna sp.11, Damaeidae sp.3,

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6 CONCLUSION It is true that some characteristics such as the species of soil fauna in characterizing the Maturity Ind ex (MI) based on ranking Gamasid ecosystems of West Africa, of their climatic mite taxa ( r/k scale) and functional groups have influence, their soil composition and the level of not been taken in consideration in this anthropic perturbation or restoration. It investigation. Nevertheless, this study gives a first highlights the need for a deep taxonomic work insight on the potential use of some defined for this unknown compartment of biodiversity.

7 ACKNOWLEDGEMENTS Thanks to R. Jocqué, Y. Samyn, and D. Van Den Lebrun Fund, GTI/IRScNB, ABIC/MRAC are Spiegel for advices and grants. Financial supports gratefully acknowledged. from CSM-BGBD project, FRS/UCL, Philippe

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