Impact of Macrotermes termitaria as a source of heterogeneity on tree diversity and structure in a Sudanian savannah under controlled grazing and annual prescribed fire (Burkina Faso)

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Forest Ecology and Management 255 (2008) 2337–2346 www.elsevier.com/locate/foreco

Impact of Macrotermes termitaria as a source of heterogeneity on tree diversity and structure in a Sudanian savannah under controlled grazing and annual prescribed fire (Burkina Faso) Saran Traore´ a,c, Robert Nyga˚rd b, Sita Guinko a, Michel Lepage c,* a

Laboratoire de Biologie et Ecologie Ve´ge´tales, UFR/SVT, Universite´ de Ouagadougou, Burkina Faso b Sida/SAREC, SE-105 25, Stockholm, Sweden c Institut de Recherche pour le De´veloppement, IRD, 01 BP 182, Ouagadougou 01, Burkina Faso Received 3 May 2006; received in revised form 6 December 2007; accepted 31 December 2007

Abstract Macrotermes termitaria are conspicuous features of savannah ecosystems in the Sudanian and Sahelian zones of West Africa. The mounds, alive or abandoned, are a major source of heterogeneity in the landscape. The purpose of the present study was to assess the impact of termitaria on tree community in a state forest of the Sudanian regional centre (Tiogo forest, Burkina Faso), under controlled burning and grazing experiments. A comparative inventory was carried out in a split-plot experiment (16 subplots of 2500 m2): 8 subplots where fire regime and grazing were controlled and 8 subplots exposed to grazing and with annual prescribed fire since 1992. All tree individuals (1.5 m) were recorded, both on termitaria and outside and their basal area at stump level was measured. A total of 61 observed (or 65.7  2.4 estimated) tree species were recorded on 28 Macrotermes subhyalinus mounds (54 observed species or 60.8  3.3 estimated), the immediate surroundings (44 observed and 59.0  0.0 estimated species) and the rest of subplots (56 observed and 63.6  0.0 estimated). Specific density was higher on mounds in comparison with the surroundings (P < 0.05). Results showed that termitaria played a key role in maintaining higher species diversity as compared to their surroundings (P < 0.05). Differences in species diversity between termitaria and immediate surroundings appeared more pronounced in disturbed plots (submitted to both fire and grazing). Some species, such as Tamarindus indica, Boscia senegalensis, Cadaba farinosa, Capparis sepiaria and Maerua angolensis are found solely on termitaria. Besides, the density of trees was significantly higher on termitaria compared to the surrounding (P < 0.05), as well as total basal area per unit of 100 m2 area (P < 0.05). We concluded that Macrotermes termitaria play an important role as a source of heterogeneity in this Sudanian savannah woodland ecosystem. This role is particularly important in ecosystems under stresses. Termitaria acted as refuge for tree vegetation. The density and dynamics of M. subhyalinus termitaria should, therefore, be taken into account in the global strategy of the forest resources management and conservation. # 2008 Published by Elsevier B.V. Keywords: Macrotermes termitaria; Heterogeneity; Savannah woodland; Tree diversity; Tree structure; Biodiversity conservation

1. Introduction The diversity of the tree component of savannah ecosystems is degrading in West Africa, especially in Sudanian and Sahelian areas (Grouzis, 1988; Larwanou, 1998; Lykke, 2000; Mahamane and Mahamane, 2005). This degradation traces back to the drought years 1973–1984 and is characterized by a loss of woody and herbaceous perennial species (Mahamane

* Corresponding author. Tel.: +226 50 30 67 37; fax: +226 50 31 03 85. E-mail address: [email protected] (M. Lepage). 0378-1127/$ – see front matter # 2008 Published by Elsevier B.V. doi:10.1016/j.foreco.2007.12.045

and Mahamane, 2005). The main factors for this trend are related to the scarcity and abnormal seasonal distribution of rains, to the increasing demographic pressure and to an overexploitation of natural resources (overgrazing, fuel requirement, and extensive cultivation). Facing this degradation and counteracting this negative trend, several recent studies emphasized the fundamental importance of the environmental heterogeneity in controlling and improving ecological factors as biodiversity, nutrient cycling, hydrologic conditions and productivity (Asbjornsen et al., 2004). Islands of soil fertility are a common feature of arid and semi-arid ecosystems (Schlesinger et al., 1996;

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Thompson et al., 2005). Anthropogenic disturbances such as fires and livestock pressure are interfering with the landscape heterogeneity and patchiness in affecting the regeneration and establishment of the tree vegetation, as well as its spatial distribution (Bachelet et al., 2000; Sawadogo et al., 2005). As a source of heterogeneity, termitaria are a typical feature in tropical and subtropical areas (Harris, 1966; Lee and Wood, 1971). In Africa they are found in savannah ecosystems as well as in agricultural lands with agro-forestry fallow systems. Some termitaria are occupied by termites and others are abandoned but their structure remains for long time, even decades. They present various shapes and sizes, according to the termitaria builder species, to the type of soil where they are built and to the degree of erosion. In the course of their activities of nesting and foraging, termites considerably modify the structure of the soil surface horizon. They enrich it in clay, increase its infiltration capacities and thus promote microbial metabolism and nutrient availability to woody plants (Abbadie and Lepage, 1989; Oue´draogo, 1997). Consequently, as ecosystem engineers (Dangerfield et al., 1998), they create localized topographic features that are safe and fertile biotopes (Arshad, 1982; Timberlake and Childes, 2004) for a better tree vegetation growth. Most of the domed or cathedral shaped termitaria are epigeal structures resulting from the above ground activities of termites belonging to the Macrotermes genus (subfamily Macrotermitinae) (Lee and Wood, 1971; Hauser, 1976; Maduakor et al., 1995; Oue´draogo, 1997). Associations in bush-thickets, in groves or in islets (Harris, 1966; Hauser, 1976; Belsky, 1983) are conspicuous features in landscapes where Macrotermes termitaria grow. The specific plant composition of these structures and their physiognomy vary between phytogeographical regions (Glovers et al., 1964; Fanshawe, 1968; Oue´draogo, 1997; Fleming and Loveridge, 2003). Epigeal termitaria affect the tree flora of several ecosystems. Work led by Wild (1952) in Zimbabwe showed a predominance of Capparidaceae and Celastraceae families on larger termitaria, where 72 observed species were recorded, corresponding to about half of the woody plants in the community. Glovers et al. (1964) reported that 10 out of the 59 species observed on the plain of Loita in Kenya were situated on Macrotermes termitaria. Boscia, Cadaba, Capparis and Maerua were the most prevailing genera on large termitaria in Zambia where Fanshawe (1968) noted a floristic composition different from the surrounding vegetation. In Burkina Faso, Guinko (1984a) noted a specific disparity of plants on termitaria based on the presence/ absence of observed species. The objective of this study was to evaluate the effect of Macrotermes termitaria on tree species diversity, composition and structure as compared with their surrounding in Sudanian woodland, where controlled experiments have been conducted since 1992, on the effects of grazing and prescribed annual early fire. Our hypothesis is that termites, as ecosystem engineers (Jones et al., 1994) play a major role in tree diversity in this ecosystem.

2. Materials and methods 2.1. Study area The study area was located in the Tiogo State Forest (128130 N; 28420 W) at an altitude of 300 m a.s.l., in Burkina Faso, West Africa. This forest belongs to the Sudanian regional centre of endemism (White, 1983), in between the North and South Sudanian Zones (Guinko, 1984b). The rainy season is unimodal and lasts from May to October. The mean annual rainfall (1994–2003) was 843.4 mm (S.E. = 212.8 mm). Mean daily minimum and maximum temperatures varied between 16 and 32 8C in January to 26 and 40 8C in April. The area is characterized by deep Lixisols (LX) (>75 cm deep) (FAO soil classification system (Driessen et al., 2001). Main soil characteristics are as follows: clay 24.8%, fine silt 15.0%, coarse silt 25.4%, fine sand 21.7%, coarse sand 13.1%, total organic matter 1.8%, total nitrogen 0.1%, C/N ratio 11.4%, available phosphorus 1.4 ppm and pH (H2O) 6.2 (Sawadogo et al., 2005). In total 74 woody and 177 herbaceous species have been recorded at the experimental site (Nouvellet and Sawadogo, 1995). The vegetation is a tree and bush savannah with a grass layer dominated by the annual grasses Andropogon pseudapricus and Loudetia togoensis as well as the perennial grasses Andropogon gayanus. The main forbs species are Cochlospermum planchonii, Borreria spp and Wissadula amplissima. In terms of basal area, the main species are Entada africana, Lannea acida, Anogeissus leicarpus, Vitellaria paradoxa, Detarium microcarpum, Combretum micrantum and Acacia macrostachya. An average stand density of 542 woody individual ha1 was recorded (Sawadogo et al., 2005), representing a basal area (at stump level) of 10.9 m2 ha1. 2.2. Experimental design The Tiogo experimental site (18 ha) was established in the dry season 1992. It consists of a split-plot design, divided into two contiguous main plots of which one was fenced off as to exclude livestock and the other plot was exposed to livestock grazing (Fig. 1). Each main plot was divided into four blocks (2.25 ha) that contain each nine subplots of 0.25 ha (50 m  50 m); subplots are separated from each other by 20–30 m fire breaks. Different treatments are randomly applied in the subplots. Treatments were assigned to tree management: (i) no cutting, (ii) selective cutting of 50% of the basal area and (iii) selective cutting followed by direct sowing of tree species. Each of these treatments experienced three fire regimes: (i) fire protection, (ii) 2 years fire protection followed by early annual fire, and (iii) early annual fire since the beginning of the experiment (Sawadogo et al., 2005). In the present study we sampled only the subplots – protected or unprotected from grazing – submitted (8 subplots) or not (8 subplots) to permanent annual early fire, without cutting (Fig. 1). Three treatments were compared (N = 4 subplots): grazing vs. no grazing; fire vs. no fire; mound vs. surrounding. The prescribed fire was annually applied at the

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on all mounds and their surroundings on the 16 subplots (0.25 ha). All individuals are plotted on a scaled map and the diameter at stump level and height were measured. According to Couteron et al. (2000), woody individuals of 1.5 m in height can be considered as adults because they are capable of producing seeds. The individuals were plotted on a map and their basal area at stump level was measured. Identification of species and families of plants were made and updated according to Nikolov (1996), Arbonnier (2000) and Bosch et al. (2002). 2.4. Termitaria sampling

Fig. 1. The experimental plots in the Tiogo forest (From Nouvellet and Sawadogo, 1995).

end of rainy season in October to November when the grass layer humidity was about 40%. The opened subplots were mainly browsed by livestock and also by wild animal. The livestock carrying capacity in Tiogo forest was 1.4 tropical livestock unit ha1 (T.L.U. ha1) (Sawadogo, 1996) and the grazing pressure was about 50% of this capacity (Sawadogo et al., 2005). 2.3. Vegetation sampling All woody plants ( 1.5 m) encountered were recorded during the midst of the rainy season from July to August 2003,

Three types of epigeal termitaria of different sizes and shapes exist in the experimental site. They resulted from the building activities of three termite genera: Cubitermes spp., (soil feeders), Trinervitermes spp. (grass feeders) and Macrotermes spp. (litter feeders). Table 1 summarizes the data obtained from mound density (381–1239 mounds ha1 according to the different treatments) and basal area above ground (218.9–985.0 m2 ha1). The large mound builders were determined as Macrotermes subhyalinus (Rambur) and Macrotermes bellicosus (Smeathman). This last species is close to the actual northern limit of its distribution. Only 3 mounds belonging to this species were found in our sampling and not included in our analysis. Thus our study focused only on M. subhyalinus mounds because of their large effect on soil rehandling, soil surface and tree pattern in this ecosystem. The mounds of this termite species represented 91.9% of the whole basal area occupied by termite mounds in the 16 subplots. M. subhyalinus mounds are roughly dome-shaped. A mature mound appeared as a central dome surrounded by a coneshaped erosion skirt. The limit between the mound area and its surrounding was determined by the raised concave relief of the mound skirt.

Table 1 Number of termite mounds per ha and their basal area (m2 ha1) per species according to the treatments (N = 4  4 subplots of 0.25 ha) (mean  standard error) Treatment No grazing

Fire

No fire

Grazing

Fire

No fire

Mound-builder species

Density (N ha1)

Basal area (m2 ha1)

Cubitermes spp. Macrotermes subhyalinus Trinervitermes spp. Total all species Cubitermes spp. Macrotermes subhyalinus Trinervitermes spp. Total all species

13.0  6.6 4.0  0.0 364.0  150.0 381 12.0  8.5 9.0  1.9 1218.0  326.0 1239

1.8  0.8 206.1  80.3 11.0  4.6 218.9 4.3  3.3 288.9  117.5 39.8  7.54 332.9

Cubitermes spp. Macrotermes subhyalinus Macrotermes bellicosus Trinervitermes spp. Total all species Cubitermes spp. Macrotermes subhyalinus Macrotermes bellicosus Trinervitermes spp. Total all species

1.0  1.0 8.0  0.0 1.0  1.0 380.0  120.7 390 6.0  3.8 7.0  1.9 2.0  1.2 768.0  177.00 783

0.1  0.16 673.9  324.6 5.22  5.2 11.2  3.3 706 0.8  0.6 878.8  486.2 83.2  74.8 22.3  4.2 985

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To characterize the spatial heterogeneity created by Macrotermes mounds, we defined an area, as the 5 m wide ring around the mound (immediate surrounding) and the remainder area of the subplot (area located out of the 5 m wide ring). According to the situation of their basis, plants were considered to belong to the termitaria, to their immediate surrounding or to the remaining subplot. A total of 28 M. subhyalinus termitaria were found in the 16 subplots or 4 ha (average density: 7.0 mounds ha1). The total surface sampled was 2047.8 m2 for the mound area, 5718.6 m2 for their immediate surroundings and 32233.6 m2 for the rest of the subplots. 2.5. Data analysis Genera, family and species names of woody plants and their occurrences on termitaria and surroundings were noted. The floristic composition on all the mounds as well as on the surrounding areas was examined according to the observed tree species (presence/absence) during the sampling period in 2003. The species richness (total number of tree species) was based on the observed and estimated species number for mounds and their surroundings. The estimate of species richness was analyzed graphically using the rarefaction curve (observed species richness as a function of the cumulative number of individuals sampled) (Magurran, 2004). The nonparametric estimator, Jackknife (Chazdon et al., 1998; Chiarucci et al., 2003) was also used to estimate total tree species richness: Jackknife 1 based on species incidence (presence/absence) and Jackknife 2 based on species abundance in tree community. According to Chazdon et al. (1998), the Jackknife estimators performed better species diversity in tree community while the observed number of tree species underestimates the true number of species present. The rarefaction curve and the Jackknife richness estimators were provided by EstimateS 8.00 software package (Colwell, 2006) and the following formulas (the recommended default) were used to compute the Jackknife estimators: Jackknife 1 (incidence-based estimator of species richness):   m1 SJack 1 ¼ Sobs: þ Q1 m Jackknife 2 (abundance-based estimator of species diversity):      2m  3 ðm  2Þ2 SJack 2 ¼ Sobs: þ Q1  Q2 m mðm  1Þ where Sest is the estimated species richness and ‘est’ is replaced in the formula by the estimator name; Sobs is total number of species observed in all the sampling area pooled; m, total number of mounds and surroundings; Qj = number of species that occur in exactly j areas (Q1 is the frequency of uniques, Q2 the frequency of duplicates). To compare the species diversity between the different areas, the specific density was calculated as species richness at

the unit of 100 m2 of area for the mounds and their surroundings. To describe stand structure characteristics for mound and surrounding areas, average tree density and average tree basal area were compared between the 3 areas. The analysis of variance (Zar, 1999) were used to assess the influence of mound state (alive or deserted) and the effects of all the treatments on the specific density, on the tree density and basal area for mean values of blocks in the 16 subplots. Prior to the analysis of variance, the specific density data were logtransformed as x + 1 because of zero-density values. The impact of disturbances on the pattern of the Macrotermes mounds was also assessed. The three factors analysis of variance was performed with the following general linear model (GLM): Y ijkl ¼ m þ bi þ G j þ F k þ M l þ GF jk þ GM jl þ FM kl þ GFM jkl þ eijkl where Yijkl is the response variable, m is the overall mean, bi the block effect (replication), Gj is the effect of livestock j, F k is the effect of fire k and Ml the effect of Mound location l. The parameters Gj, F k, Ml and their interactions were examined as fixed factors and bi as random. Multiple comparisons were made with Tukey’s test to detect differences between treatments (Zar, 1999). All the statistical analyses were performed using SPSS 11.01 for Windows at 5% level of significance. 3. Results 3.1. Mound distribution and density We noticed that fire has a strong negative influence on mound density, particularly for the genus Trinervitermes (grass feeder): 1218 mounds ha1 in subplots with livestock and fire exclusions, 380 mounds ha1 in subplots exposed to both stresses (P = 0.005) (Table 1). For the species M. subhyalinus, within the area submitted to grazing, 8 mounds were found on burnt subplots and 7 on unburnt subplots. In the plots protected from grazing, 4 mounds were recorded on burnt and 9 on unburnt subplots (Table 1). The mean basal area occupied by one mound of M. subhyalinus varied from 32 m2 in the fenced subplots with early fire to 126 m2 in the subplots exposed to livestock but protected from early fire. Total area covered in each subplot varied from 206 m2 ha1 in the subplots protected from livestock but submitted to early fire to 879 m2 ha1 in those exposed to livestock grazing with fire exclusion (Table 1) (2.1–8.8% of the total area). During the sampling period, we noticed 14 inhabited mounds belonging to M. subhyalinus and 14 abandoned mounds by its original builder inside the 16 subplots. There were no statistically significant influences of treatment on mound state (alive or abandoned), on mound mean basal area and no significant influences of mound state on tree community in this study (ANOVA, P > 0.05). Therefore,

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we further considered the Macrotermes mound community as a whole (without distinguished between alive or dead nests).

Table 2 Observed and estimated tree species richness for 2003 in the 16 subplots in the Tiogo forest (mean  standard deviation)

3.2. Species richness

Area

A total of 61 species from 7631 trees individuals were encountered on the 28 mounds with 3572 individuals and their surroundings (immediate = 559 individuals and rest of subplot = 3500 individuals) (Table 2). Fifty-four were recorded on termitaria (which covered only 5% of the area) vs. 44 species for the immediate surrounding and 56 for the rest of sampling subplots. Out of the 61 tree species, 40 species (or 66%) were common between mounds and their immediate surroundings. Fourteen (or 23%) species were solely observed on mounds comparing to their immediate surroundings and 4 species (7%) only on these immediate surroundings. Forty-nine species (or 80%) were observed both on mounds and the rest of the subplots while 5 species were solely observed on mounds area. (Floristic complete list can be found with authors). Fig. 2 showed species rarefaction curves for the sampling areas plotted in relation to the number of tree individuals sampled. Rarefaction curves for the mound and rest of subplot samples reached a plateau except that of the immediate surrounding. When the mounds and the rest of subplots samples were rarefied to the value of N = 559 individuals observed on the immediate surroundings, their species richness were lower. The species richness of the rest of subplots also exceeded that recorded on the mounds (Fig. 2). For the same number of individuals sampled, termite mounds showed the lowest observed species richness. But the observed species corresponded to an average specific density of 85  23/100 m2 (S.E.) on the mounds, 5  1/100 m2 (S.E.) on the immediate surroundings and 1  0/100 m2 (S.E.) on the rest of subplots. This average specific density was 17 times higher on mounds than the immediate surrounding and 85 times that observed on the rest of subplots. There was a decreasing in the specific density from termite mounds to out off mounds. The Jackknife 1 estimator showed the highest estimate of the total species richness in all the 16 subplots (65  2.4 S.D.) and

Total observed species

Estimates of total tree species richness Jackknife 1

Jackknife 2

Mound Immediate surrounding Rest of subplot

54 44 56

60.8  3.3 52.6  2.6 61.6  2.3

60.1  0.0 59.0  0.0 63.6  0.0

Total

61

65.7  2.4

65.5  0.0

on Macrotermes mounds (60.8  3.3 S.D.) while the Jackknife 2 estimator generated the greatest estimate of the total richness in the immediate surrounding (59.0  0 S.D.) and the rest of subplot (63.6  0 S.D.) (Table 2). The estimate of the total species richness tended to be closed to the number of observed species. 3.3. Floristic composition A total of 22 families and 46 genera were identified in the study subplots. Out of these families, Mimosaceae, Combretaceae and Cesalpiniaceae, with, respectively, 9, 9 and 6 species were the most represented families. Apocynaceae, Capparaceae, Ebenaceae, Opiliaceae and Sapindaceae families were only observed on mounds and none in the immediate surroundings. Relative frequencies of family revealed that the family Combretaceae dominated with a relative frequency of 39% on termitaria (immediate surrounding = 33% and rest of subplots = 38%), followed by Rubiaceae 16% (vs. 6% and 6%) and Tiliaceae 13% on mounds (vs. 3% and 3%). The family Mimosaceae showed a relative frequency 9% on mounds and 23 and 21% on mound surroundings. The genera Allophyllus, Baissea, Boscia, Cadaba, Capparis, Diospyros, Maerua, Opilia, Saba and Tamarindus were totally absent from the immediate surroundings and the genera Boscia, Flueggea were not observed in the rest of subplots. Out of the 46 genera only 3 genera (Annona, Lonchocarpus and Xeroderris) were found only on the mound surroundings (immediate and out of immediate). The species Allophyllus africanus P. Beauv., Boscia senegalensis (Pers.) Lam. ex Poir., Cadaba farinosa Forssk., Capparis sepiaria L., Grewia bicolor Juss., G. lasiodiscus K. Schum, Gardenia sokotensis Hutch., Maerua angolensis DC., Opilia celtidifolia (Guill. & Perr.) Endl.ex Walp and Tamarindus indica L. appeared to be confined to mound soil. 3.4. Effects of livestock grazing

Fig. 2. Expected species accumulation curve in the 16 subplots in the Tiogo forest.

The livestock grazing statistically had no effect on the mean specific density (P > 0.05) (Table 3). The mean density and mean basal area of tree community also showed no significant difference caused by the livestock activities in our study subplots (P > 0.05).

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Table 3 Impact of livestock grazing and prescribed annual fire on the mean tree specific density, the mean tree density and basal area in Tiogo forest subplots Parameters

Treatments

2

Specific density (S/100 m ) Tree density (N/100 m2) Tree basal area (m2/100 m2) * **

Grazing

No grazing

P

Fire

No fire

P

33.3 81 0.7

27.4 156.6 1.1

0.232 0.056 0.175

21.2 172.6** 1.2 *

39.5 65 0.6

0.15 0.008 0.045

P < 0.05. P < 0.01.

Table 4 Impact of Macrotermes mounds on the mean specific density, the mean tree density and basal area during the study period in Tiogo forest Parameters

Microhabitat

Specific density (S/100 m2) Tree density (N/100 m2) Tree basal area (m2/100 m2)

Mound

Immediate surrounding

Rest of subplot

84.8 a 323.2 a 2.4 a

4.9 b 21.8 b 0.1 b

1.4 c 11.5 b 0.2 b

Mean with different letter (a–c) along the same row are significantly different (P < 0.05) according to Tukey HSD test.

3.5. Effects of prescribed annual fire The effects of prescribed annual fire were not statistically significant for the mean specific density (P > 0.05) (Table 3). The mean tree density and the mean tree basal area were significantly increased for the burnt subplots in fire vs. no fire treatment (P < 0.01 and <0.05, respectively). 3.6. Effects of Macrotermes mounds The presence of M. subhyalinus mounds in the 16 subplots significantly influenced the mean specific density (P < 0.05) during the sampling period (Table 4). Pairwise comparisons revealed that the mean tree specific density was higher on the mounds than on the immediate surrounding (P < 0.0001) and than on the rest of the subplot (P < 0.0001). This mean specific density was also higher for the immediate surrounding comparing to the rest of the subplots (P < 0.001) (Table 4). The effects of M. subhyalinus mounds increased significantly the mean tree density and mean basal area of tree community in the study subplots (P < 0.001 and Table 5 Impact of the annual fire and mound location interaction on the mean tree density and mean basal area in the study subplots Treatment

Parameters

Mound

Immediate surrounding

Rest of subplot

Fire

Tree density (N/100 m2) Tree basal (area m2/100 m2)

494.8 3.4

12.2 0.1

10.9 0.2

No fire

Tree density (N/100 m2) Tree basal area (m2/100 m2)

151.7 1.5

31.4 0.1

12 0.2

<0.001, respectively). Regarding the mean values, we noticed that Macrotermes mounds carried the highest tree density and basal area in comparison with their immediate surrounding (P < 0.001) and the rest of the subplots (P < 0.001). 3.7. Interaction effects Annual early fire and livestock did not interact significantly on the specific density (P < 0.05). The effects of fire and livestock interaction induced no statistical influence on the mean tree density and mean basal area (P < 0.05). A prescribed fire  Macrotermes mounds impact was observed for the mean tree density and mean basal area (P < 0.001 and <0.018, respectively) solely (Table 5). The analysis of the mean values showed that the early fire considerably decreased tree density and basal area in the areas located outside mounds. The mean tree density was sharply increased on Macrotermes mounds (495/100 m2) in the subplots submitted to early fire as compared to the immediate surrounding and to the rest of subplots during the sampling periods (12/100 m2 and 11/100 m2, respectively). We noticed an increase in the mean tree basal area mainly for mounds located in subplots under early fire (3 m2/100 m2) (Table 5). The interaction effects due to the livestock  mound location were only noticed for the mean tree density (P < 0.05) (Table 6). The mean tree density was greater on mound than in surrounding areas in subplots exposed or not to grazing in the regard of the mean values. In contrast, the livestock  fire  mound interaction was had no significant effect on the tree community in our study subplots during the sampling period (P > 0.05).

Table 6 Impact of the livestock and mound location interaction on the mean tree density in subplots Treatment

Grazing No grazing

Tree density (N/100 m2) Mound

Immediate surrounding

Rest of subplot

211.3 435.1

19.1 24.4

12.7 10.2

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4. Discussion 4.1. Termitaria Mound densities found in this study ranked in the highest densities recorded in West-African savannah ecosystems for Macrotermes (0.15–10.73 ha1: Buxton, 1979; Pomeroy, 1977) and Trinervitermes (2.8–1300: Lepage, 1972; Ohiagu, 1979; Roose, 1976). Total mound basal areas are comparable to the data found in other biotopes: 1.5–9.8% (Lepage, 1972; Tano, 1993). The interaction between fire and termite mound density has been examined in few studies (Trapnell et al., 1976; Spain et al., 1986). The effect of fire, through grass incineration, could induce an intensification of the competition for foraging space and food resources, especially for grass-feeding termites Trinervitermes. Therefore, a decreasing in the mound density of such species (Lepage and Darlington, 2000) was remarkable, as evidenced in this study. On the other hand, fire could induce spatial heterogeneity and moisture stress, which could favor Macrotermitinae, Macrotermes, in drier habitats and increased their success and colony establishment (Davies, 1997). 4.2. Floristic composition Our sampling, done within 4 ha, revealed 61 observed species (84.7% of the total figure given in Nouvellet and Sawadogo (1995), indicating 65.7  2.4 tree species that would be found both on Macrotermes mounds and in their surroundings. The estimated species richness defined an evolution of the number of observed species with the number of tree individuals towards those obtained by Nouvellet and Sawadogo (1995). We sampled 73% of the total species found by previous authors in the Tiogo forest on 2047.8 m2 of Macrotermes mound soil. Approximately 89% of all species encountered and inventoried in this study were observed on mounds. In this Sudanian woodland ecosystem, tree vegetation associated with Macrotermes termitaria contains savannah species as well as forest species. Species encountered on the termitaria were either trees able to attain a considerable height: T. indica L. (Cesalpiniaceae), D. mespiliformis (Ebenaceae), or species confined to this particular environment, as B. senegalensis, C. farinosa, C. sepiaria and M. Angolensis (Capparaceae). Some other species from the genera Balanites, Combretum, Feretia, and Grewia, as well as A. leiocarpus species, exhibited higher relative frequencies on mounds compared to the surrounding. Such species preferences of the natural vegetation to grow on large mounds built by Macrotermitinae in Africa and Asia have been reported in other areas (Wood, 1996). The majority of the studies confirmed that the termitaria supported vegetation with trees and shrubs quite distinct from the surrounding landscape (Holt and Lepage, 2000). Logan (1992) questioned if termite mounds had a positive or a negative role on vegetation. Species G. bicolor often had been met on termite mounds in Sahelian area of Senegal (Poupon, 1980). Oue´draogo and Lepage (1997)

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reported that the densities of Boscia and Pterocarpus were, respectively, 10 and 3.5 times higher on Macrotermes mounds in a sub-Sahelian ecosystem, whereas Acacia was only found on mounds. The same authors noticed that the species Guiera senegalensis was never recorded on mounds. In Lamto savannah, stem densities of Borassus aethiopum and Piliostigma thonningii were, respectively, 7 and 2 times higher on mounds (Konate´ et al., 1999). These associations between Macrotermes mounds and tree species raised a discussion on the way of the relationship between the termite builder and the plant species: which one came first? Oue´draogo (1997) analyzed the spatial interactions between some tree species and mounds, using Diggle’s G and Ripley’s K, functions that are able to distinguish whether the association exist and the way of this association (whether the distribution of the tree species is oriented towards the termite mound, or the opposite). Results revealed that Boscia was clearly associated with Macrotermes mounds. Whatever the primer, complex interactions took place between the large and long-lived Macrotermes mound and the tree population. Many factors could be considered to explain the presence of distinctive vegetation on termite mounds like protection from fire, improved drainage, greater soil depth, higher soil moisture (Konate´ et al., 1999) or improved fertility status (Salick et al., 1983; Tano, 1993; Wood, 1996). The ability of some tree species to form mycorrhizal associations in soil enriched with Macrotermes mound soil (Duponnois et al., 2005) also could be in favor of a better growth of a distinctive vegetation. These authors have demonstrated that M. subhyalinus mound materials were natural microbial inoculants that promoted plant growth. The presence of species, such as T. indica, B. senegalensis, C. farinosa, C. sepiaria and M. angolensis, Combretum sp, F. apodanthera, and Grewia sp, could result from their deep affinity for termitaria and their adaptabilities to some environmental conditions that characterized termitaria or other ecologically similar sites. Consequently, as microsites, termitaria exhibited their own regional woody flora everywhere they appeared. Under specified climatic conditions, termitaria appeared as a special and additive factor of the specific diversity, the floristic composition, and the abundance of the woody vegetation within natural ecosystems in tropical zone. 4.3. Effects of livestock grazing The effect of livestock was not statistically significant for the species richness, tree density and tree basal area in grazing vs. no grazing treatments during our sampling period at Tiogo forest. This suggested that the observed difference in the tree species and the distribution of their abundance in this site did not depend upon livestock grazing. The opened subplots even if fire events took place at the Tiogo forest were regularly visited by animals to graze mainly the herbaceous species. Since the grazing pressure was 50% of livestock carrying capacity in the study subplots, some tree species could survive moderate grazing intensity that allows succession to proceed. This fact

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can also limit competitive species to dominate tree community. Belsky (1987) reported evidence showing that low to moderate herbivory sometimes has no measurable effect. 4.4. Effects of prescribed annual fire The prescribed annual fire did not significantly influence the specific density but significantly affected the mean tree density and the mean tree basal area in this study. But the observed specific density in burnt subplots can be explained by the disappearance of fire sensitive species. The continuous fire event may hinder the regeneration of these tree species or induce their mortality. In contrast, we noticed that tree density and basal area in burnt subplots were, respectively, 3 and 2 times higher than tree density and basal area in unburnt subplots. As fire response strategy in this case, tree species increased the size of their populations mainly by sprouting propagation as Sawadogo et al. (2002) pointed out. Similar fire response of tree species was observed by Otterstrom and Schwartz (2006) in a dry tropical forest. One might argue that the early fire is non-lethal to adult trees. The increase of tree basal resulted from the great density. 4.5. Effects of Macrotermes mounds The effect of termite mounds was significant on tree species richness, tree density and tree basal area in our work. According to the results, the Macrotermes mounds, immediate surrounding and the rest of subplot appeared as 3 different areas for tree species richness but still having the same site conditions like parent soil and climatic factors. According to Menaut et al. (1995) termitaria increased tree species richness by more than 40% in savanna woodlands. Furthermore, the effect of Macrotermes mounds induced a greater tree density and basal area. This fact was due to the abundance of some species that were solely found on mound and for which mound soil constituted a natural habitat. On the other hand, the presence of mound could promote vegetative as well as sexual propagation of tree vegetation and then could increase tree density by less than 20% in savanna woodlands (Menaut et al., 1995). As a consequence in savannah ecosystem, the comparative smaller basal area of Macrotermes mounds soil carried large concentration of tree vegetation. 4.6. Interaction effects The prescribed annual early fire and livestock acted independently or in combination with other factors on the tree population as evidenced by the absence of significant interaction on the specific density, tree density and tree basal area. The effect of interaction due to livestock grazing  Macrotermes mounds was significant for the tree density whereas the prescribed fire  Macrotermes mounds interaction significantly induced an increase in tree density and basal area during the sampling period. Tree densities were much higher on mounds as compared to the surroundings in

subplots submitted to annual fire and subplots protected from fire. The higher difference in tree density occurred in subplots exposed both to fire and to grazing. These differences could be due to the sensitiveness of some species to fire and livestock grazing. By consuming and trampling livestock reduces the above ground grass biomass and also removes the fine fuels (grass) that helped to carry the light intensity fires (Sawadogo et al., 2002, 2005). Our results could not be valuably compared to the data previously obtained in the Tiogo forest (Nouvellet and Sawadogo, 1995), as these authors considered only tree individuals 10 cm GBH. The rarity of grass cover on termitaria prevented fire stretching and also made this area less attractive for livestock. On the other hand, termitaria vegetation appeared impenetrable thickets to livestock. The presence of thorny species (species of Capparidaceae) also prevented the livestock to keep close to termitaria as well as other areas. In that case, termitaria play the key role of refuge for fire and livestock-sensitive tree species as pointed out by Fanshawe (1968). 5. Conclusion Our analysis suggested that Macrotermes termitaria significantly affected the woody community in terms of species diversity, tree density and community distribution. Tree density and basal area were increased on mounds as compared to the surrounding soils while the difference in tree species richness generated three different areas under the same site conditions. The role of termitaria as microsites of increased biodiversity is particularly important when the ecosystem is submitted to disturbances (early fire and grazing by livestock). Under such situations, termitaria could act as refuges for the woody vegetation. The vegetation of the large termitaria sheltered a particular flora, which constituted local community reservoirs. These reservoirs could then be considered as a way of biodiversity conservation and thereby, should be taken into account in the long-term global strategy of forest resources management and conservation. Acknowledgements The authors are grateful to Swedish International Development Cooperation Agency/SAREC project. A grant from this agency was obtained under the research program ‘‘Ecosystem regeneration’’. Special thanks are due to Dr. Louis Sawadogo for valuable field assistance during this work, to Pr. Jeanne Millogo for valuable suggestions for improving the paper and to two anonymous reviewers for their valuables comments and suggestions. References Abbadie, L., Lepage, M., 1989. The role of subterranean fungus-comb chambers (Isoptera, Macrotermitinae) in soil nitrogen cycling in a preforest savanna (Coˆte d’Ivoire). Soil Biol. Biochem. 21 (8), 1067–1071.

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