Research Article |
Corresponding author: Salvatora Nsenga Nkulu ( nsengankulu@gmail.com ) Academic editor: Nicolas Barbier
© 2022 Salvatora Nsenga Nkulu, Pierre Meerts, Edouard Ilunga wa Ilunga, Mylor Ngoy Shutcha, David Bauman.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Nsenga Nkulu S, Meerts P, Ilunga wa Ilunga E, Ngoy Shutcha M, Bauman D (2022) Medicinal Vitex species (Lamiaceae) occupy different niches in Haut-Katanga tropical dry woodlands. Plant Ecology and Evolution 155(2): 236-247. https://doi.org/10.5091/plecevo.89394
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Background and aims – Sustainable management of the medicinal plant resources provided by tropical forests is of utmost importance to human populations in developing countries. Trees and shrubs of the genus Vitex (Lamiaceae) are of great medicinal importance in Haut-Katanga (SE D.R. Congo), frequently used to treat tropical diseases. However, the security of supply is threatened, particularly by urban sprawl and mining. A conservation strategy for medicinal plants is urgently needed. In this context, we try to better understand the ecological factors (mostly soil) explaining the distribution of three medicinal species of Vitex (Lamiaceae) (V. fischeri, V. madiensis, and V. mombassae) that co-occur in the tropical dry woodlands in the region of Lubumbashi.
Material and methods – In 114 plots (10 m radius), comprising at least one species of Vitex, all woody species with a DBH ≥ 10 cm were inventoried and soil samples were collected. Multivariate Regression Trees (MRT) combined with indicator species index IndVal and Redundancy analysis (RDA) were used to characterise habitats and woody plant communities associated to each Vitex species and to explain the variability of plant community composition.
Key results – Four habitats were identified, and the three Vitex species differ significantly in ecological range. Vitex fischeri is a specialist of a most distinctive community on high Mg and low Al soil (termite mounds). Vitex mombassae is indicative of one habitat, corresponding to low altitude (< 1230 m) plots. Vitex madiensis has a broader range, being a generalist of all habitats except termite mounds.
Conclusion – These results emphasise the importance of a detailed knowledge of species ecology to design species-specific conservation strategies, even for congeneric species occurring in sympatry in the same landscape.
aluminium, conservation, indicator species, medicinal, miombo, niche, soil, termite mound, tropical dry woodlands, woody species
The provision of medicinal plants is one of the important ecosystem services or nature contribution to people supplied by tropical forests and woodlands. Indeed, 70% of the population in sub-Saharan Africa uses plant medicinal resources as the access to the ‘modern’ healthcare system is very limited due to the lack of suitable infrastructure and the low incomes (
The same situation occurs in the Haut-Katanga province (D.R. Congo) where medicinal woody plants, widely used by the urban and rural dwellers, are declining rapidly because of the reduction of woodland or their intensive exploitation (
The development of a conservation program of the three Vitex species has become a priority to ensure a sustainable supply of these vital ecosystem services and to support the healthcare system in this region. Resource management of these three sympatric medicinal species under high anthropogenic impact is therefore crucial and requires a good understanding of the species’ autecology and synecology. Indeed, the development of conservation programs for Vitex is crucial, in a context of steadily decreasing woodland area. Thus, the implementation of an adequate conservation strategy can only be achieved through a thorough understanding of the deterministic processes responsible for the variability of plant communities associated with Vitex species.
Previous studies in the Katangan miombo woodland have highlighted the importance of habitat heterogeneity at multiple spatial scales in tree community assemblages and species coexistence (
Despite their key role in traditional tropical medicine, the ecology of Vitex species, their assemblage with other species into communities, and their dependence on specific abiotic conditions (soil, topography) remain unstudied and therefore poorly understood. It is in this context that we try to better understand the ecological mechanisms explaining the distribution of three medicinal Vitex species (V. fischeri, V. madiensis, and V. mombassae) that co-occur in the dry woodlands of Katanga (SE D.R. Congo).
The genus Vitex (Lamiaceae, formerly Verbenaceae) comprises about 250 species found in tropical and subtropical regions (
Here, we address the following specific questions: (a) Do the three Vitex species occur in distinct plant communities and occupy different ecological niches? (b) What are the ecological factors discriminating the different communities?
The study was conducted on the plain of Lubumbashi (Haut-Katanga province in the D.R. Congo), covering an area of 2500 km2 (11°25’57.23”S, 27°16’3.11”E; 11°53’18.98”S, 27°15’56.31”E; 11°53’21.63”S, 27°44’25. 86”E; 11°25’37.70”S, 27°44’29.59”E), with the post office downtown used as the centroid (Supplementary file 1). The climate is CW6 (
Considered as the centre of endemism in the northern part of the Zambezian region, the plain of Lubumbashi is dominated by the humid miombo woodland (Kuper 2004;
The geological substrate of the region is dominated by dolomitic shale and siltstone of the neoproterozoic Nguba and Roan groups (
A total of 200 1-ha plots were defined along four main roads (Kasenga, Kafubu, Kipushi, and Likasi), covering the different degraded states of the landscape (miombo woodland, degraded miombo, shrub savannah, post-cultivation wasteland, and agricultural land) as described by
Soil samples were systematically collected from each 10 m radius plot (0–20 cm soil layer). The soil samples were analysed according to the standard protocol of
Plot elevation was obtained in the field with a GPS (Edge 830), and height above the nearest drainage (HAND) was obtained for all circular plots at a one arc-second (ca 30 m) resolution (100 river head threshold cells) from the digital elevation model SRTM (
Absolute abundance (number of individuals of a species in a habitat) and relative abundance (ratio of the number of individuals of a species in a habitat to the total number of individuals of the species across all habitats) were calculated per habitat following
We used multivariate statistical methods focused on both prediction and explanation to model the relationships between species and ecological variables and define species assemblages and specialist and indicator species of particular habitats. First, we used Multivariate Regression Trees (MRT;
To avoid unstable models due to collinearity issues, we calculated pairwise Pearson correlations across all explanatory variables and, for the variable pairs with r > +0.7 and r < -0.7, one of the two variables was removed from the model (
Multivariate Regression Trees (MRT) is a form of constrained clustering method (
The indicator species associated with each habitat were defined using the IndVal index. This index is calculated by considering both the fidelity and specificity of the species (
Redundancy analysis (RDA) was used as a complementary approach to the combination of MRT and IndVal indices, to explain the variability of plant community composition from the heterogeneity of ecological factors. Explanatory variables were standardised to mean zero and unit standard deviation prior to the analysis. The statistical significance of the overall association between the community matrix and the environmental variable matrix, as well as each of the constrained RDA axis, were tested using 999 permutations of the model residuals (
A Hellinger transformation was performed on the matrix of tree species abundance per plot using the R package vegan (
We used permutation ANOVAs to test for differences in each environmental variable among the habitats defined by the MRT approach in order to better characterize them. To do so, the PERMANOVAs consisted of one environmental variable (e.g. Ca content) being modelled as a function of the factor ‘habitat’ (four levels, one per habitat; see Results), where each observation consisted of the corresponding variable value in one plot. If the ANOVA for a given environmental variable indicated that the variable differed significantly among habitats (based on 999 permutations), permutation t-tests were used to compare each pair of habitats and define the pairs that differed significantly. Permutation ANOVAs and t-tests were performed using the R functions anova.1way (
All analyses were performed in the statistical environment R v.4.0 (
A total of 82 species were inventoried, belonging to 32 families and 62 genera (Supplementary file 5). We inventoried 286 individuals of Vitex across all plots. Cluster partitioning of the MRT analyses in relation to environmental variables identified four habitats with an explanatory power of 11% (Fig.
Habitats and corresponding community assemblages as defined by multivariate regression trees. The dominant species (highest absolute abundance) in each habitat are ranked in decreasing order of abundance and the indicator species are in bold with an asterisk indicating a significant p value (p < 0.05; 4999 permutations). Optimised habitat discrimination was performed using the following environmental variables: elevation (E), aluminium concentration (Al), and magnesium (Mg). Statistical values for the MRT analysis included: relative error = 0.891, cross-validation error = 1.03, standard error = 0.0249. n represents the number of plots within each habitat.
H1 was characterised by a very distinct floristic composition (Supplementary file 5), with 29 species only occurring in this habitat. Fabaceae were rare (9%) in this habitat. The species were grouped into two categories according to leaf phenology: deciduous (Cassia abbreviata, Lannea discolor, and Zanthoxylum chalybeum) and evergreen (Allophylus africanus, Boscia mossambicensis, Markhamia obtusifolia, and V. fischeri). Markhamia obtusifolia and Combretum molle were the most abundant species.
In the other three habitats, the Fabaceae was the most frequent family (48%). H2 had a low number of species (30 species) with an average tree height of 8.5 m. The average cover of the tree and shrub layer was 53% and 43%, respectively. Brachystegia boehmii and B. spiciformis were the most abundant species in H2. However, H3 and H4 were characterised by a dense shrub layer (52%) and a sparse tree layer (28%) with 66 and 54 species, respectively. The trees observed in H3 and H4 had an average height of 6.5 m. Brachystegia boehmii and Albizia adianthifolia were the abundant species in H3 and B. spiciformis and Ochna schweinfurthiana in H4.
Significant indicator species associated with each habitat were identified by permutations of the IndVal index in the habitat where the species was more abundant (Supplementary file 5). A total of 15 indicator species were detected in habitat H1, H2, and H4 (Table
A total of 45 specialist species were detected in all habitats. Vitex fischeri was a specialist in H1 and V. mombassae in H4. In contrast, B. boehmii, B. spiciformis, Julbernardia paniculata, and V. madiensis were generalists of H2, H3, and H4 (Supplementary file 5).
IndVal values of indicator species for habitats associated with Vitex. * p < 0.05; ** p < 0.01; *** p < 0.001.
Species | MRT-Habitats | IndVal |
Vitex fischeri | 1 | 0.70*** |
Haplocoelum foliolosum | 1 | 0.58*** |
Allophylus africanus | 1 | 0.50*** |
Ziziphus mucronata | 1 | 0.46*** |
Combretum molle | 1 | 0.43*** |
Markhamia obtusifolia | 1 | 0.40** |
Cassia abbreviata | 1 | 0.27** |
Ficus thonningii | 1 | 0.22* |
Zanthoxylum chalybeum | 1 | 0.20** |
Boscia angustifolia | 1 | 0.18* |
Pericopsis angolensis | 2 | 0.31* |
Uapaca pilosa | 2 | 0.24** |
Piliostigma thonningii | 2 | 0.15* |
Vitex mombassae | 4 | 0.32** |
Pterocarpus angolensis | 4 | 0.26* |
A constrained ordination (RDA) was used to further describe and quantify the relation between community composition and environmental heterogeneity. The RDA between environmental variables and species abundances indicated a significant explanation of species composition variability by the environment (p < 0.001), although the overall explanatory power was relatively limited (adjusted R2 = 0.111). The first two constrained axes explained 10.6% of the total variability. Axis 1 expressed on the constrained coordinated (7.6% of the variance) had major contributions from Mg, pH, K, Mn, and organic matter content (negative correlations), and Al and E (positive correlations) (Fig.
The projection of the 4 MRT habitats in the ordination plane showed that habitats H1 and H2 were clearly different from the other two (H3 and H4). H1 was characterised by soil with high Mg concentration on axis 1, and H2 was located on fertile soils with high P concentration on axis 2. However, H3 and H4 formed a continuum located in intermediate altitude areas on poor soils with high Al concentrations (Fig.
Ordination diagram showing the result of the redundancy analysis (RDA) in the constrained space. A. Projection of environmental variables and plots. Only significant variables (p < 0.05) are displayed; adjusted R² value = 0.098. The 4 habitats of the MRT are represented by different colours (H1: blue, H2: yellow, H3: grey, and H4: orange). B. Projection of species with goodness of fit ≥ 0.1 in the ordination plane formed by axes 1 and 2. Indicator species are coloured in the same way as their respective habitat and species in black have a goodness of fit = 0.1. The indicator species of H2 are not shown because they have goodness of fit values below 0.1. Elevation (E), shrub cover (Cs), tree cover (Ct), organic matter (OM). See Supplementary file 5 for species acronyms.
The development of a conservation strategy requires a good knowledge of the species autecology. In this paper, we characterised the autecology of three congeneric, sympatric species of the genus Vitex that co-occur in the dry woodlands of southern D.R. Congo. The three species are important conservation targets due to their medicinal properties. In this paper, we assessed if they are associated to distinct plant communities and if their distribution can be accounted for by variation in environmental factors. The three species were found to occur in four habitats. We first examine if these habitats correspond to previously described vegetation units.
Habitat 1 corresponds to termite mound vegetation. The Katangan dry tropical woodlands are characterised by the presence of Macrotermes mounds, which harbour a highly distinctive vegetation (
The other two species occur in the woodlands surrounding the termite mounds. Such woodlands are characterised by a high frequency of Fabaceae (Julbernardia paniculata, Albizia adianthifolia) and, in particular, the abundance of several species of Brachystegia. Based on the phytosociological classification of
Our work further supports previous results pointing to the importance of topography and soil heterogeneity for the assemblage and dynamics of tree communities in miombo woodlands (
Here, we used complementary multivariate constrained analyses (MRT and RDA) to model soil-plant relationships associated with the three sympatric congeneric Vitex species at a regional scale. We highlighted four distinct habitats as well as associated specialist and indicator species and provided a detailed characterisation of the physico-chemical features of these habitats.
In this study, the four habitats presented statistically different values of nine environmental variables (see Supplementary file 6) and the discriminatory environmental variables of the habitats associated with the Vitex species were Mg, Al, and elevation. It is evident that even at fine spatial scales, heterogeneity in the edaphic and topographic environment facilitates the specialisation of species to contrasting habitats (
The other two Vitex species (V. madiensis and V. mombassae) were associated to base cation-poor soils with high aluminium concentration. Vitex madiensis was mainly a generalist of H2, H3, and H4. These results corroborate the observations of
The model generated from the MRT based solely on variability in soil chemistry, elevation, HAND, and structural variables predicted 10% and explained 11% of the spatial distribution of tree communities, while the RDA explained 9.9% using the same environmental variables. The explanatory and predictive powers observed in our study are lower than the range of variation (19% to 49%) of community-habitat associations in tropical forests (e.g.
These results emphasise the importance of a detailed knowledge of species ecology to design species-specific conservation strategies, for congeneric species occurring sympatrically in the same landscape. The designation of protected areas should include the different habitats needed to conserve the three species. In particular, V. fischeri is associated to termite mounds, a habitat that is threatened by brick manufacturing. Vitex mombassae occurs mostly at lower elevations which are under pressure by shifting agricultural practices, while V. madiensis occupies a broader range of habitats, except termite mounds.
Future work on these Vitex species will be necessary to further understand their ecology as well as how it translates into potential differences in terms of secondary compounds of medical interest. Examples of future questions are whether the broad-niched V. madiensis is phenotypically more variable than the other two species, and whether populations occurring in different habitats show a different compositions of pharmacologically relevant compounds.
We thank Jonathan Muledi (UNILU) for his help in identifying species in the field, as well as Thomas Drouet (ULB), Nausicaa Noret (ULB), and Alexandre Van Baekel (ULB) for their invaluable help with the soil analyses. We are grateful to Pierre Ploton for his help with Google Earth Engine. This research was funded by the Académie de Recherche et d’Enseignement Supérieur (ARES, Fédération Wallonie‐Bruxelles, Belgium; project PHYTOKAT; project leaders Pierre Duez (UMons) and Salvius Bakari Amuri (UNILU)). DB was supported by the Wiener-Anspach Foundation, the Belgian American Educational Foundation, and the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 895799.
Geographic map showing the spatial distribution of plots in the study area.
Variation of environmental variables in the whole dataset.
Pearson correlation coefficients between environmental variables.
Abundance of woody species associated with the three Vitex species in the four habitats.
Comparison of environmental variables between the four habitats.
Distribution of the four habitats in relation to geological substrate.
Box plots of elevation as a function of geological substrate.