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Influence of soil type on the properties of termite mound nests in Southern India
Applied Soil Ecology 96 (2015) 282–287
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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Influence of soil type on the properties of termite mound nests in Southern India Pascal Jouqueta,b,* , Nabila Guilleuxa,b , Rashmi Ramesh Shanbhagc, Sankaran Subramanianb a b c
Institute of Ecology and Environmental Sciences (UMR 242 iEES Paris), Institute of Research for Development (IRD), 32 av. H. Varagnat, 93143 Bondy, France Indo-French Cell for Water Science (IFCWS), Indian Institute of Science, 560 012 Bangalore, Karnataka, India Institute of Wood Science and Technology, Malleswaram, 560 003 Bangalore, Karnataka, India
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2015 Received in revised form 11 August 2015 Accepted 13 August 2015 Available online 9 September 2015
Termite mounds are conspicuous features in many tropical ecosystems. Their shape and soil physicochemical properties have been suggested to result from the termites ecological need to control the temperature and humidity within their nests and protect themselves from predators. This study aimed to determine the influence of the parent soil properties on the shape and soil physical and chemical properties of termite mounds. Termite mounds built by the fungus-growing termite species Odontotermes obesus were compared in two forests with different soil properties (Ferralsol or Luvisol) in Southern India. Our findings confirm that soil properties influence the physicochemical characteristics of mound material and may affect the shape, but these impacts are mostly independent of the size of the mounds (i.e., the age of the colonies). Mound walls were more enriched in clay and impoverished in C and N in the Luvisol than the Ferralsol. However, their shape was more complex in the Ferralsol than the Luvisol, suggesting a possible link between the clay content in soil and the shape of termite mounds. The results also suggest that clay becomes enriched in O. obesus mound walls through a more passive process rather than solely by particle selection, and that termite mound shape results from the soil properties rather than the ecological needs of termites. In conclusion, although ecologists have mainly focused upon the influence of termite ecological needs on their nest properties, this study highlights the need for a better understanding about the role of the soil pedological properties and, as a consequence, how these properties drive the establishment and survival of termites in tropical ecosystems. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Clay Ferralsol Luvisol Termite mound architecture
1. Introduction Fungus-growing termites (Termitidae, Macrotermitinae) construct belowground chambers or aboveground mounds to protect their colonies and their exo-symbiotic fungi. Depending on the challenge of their immediate environment, termites are assumed to modify the properties of their nests in two ways: first, by selecting and modifying the soil material they use and/or by modifying the shape of their mounds. For construction, fungus-growers transport clay-enriched soil from deep soil horizons to the soil surface (e.g., Jouquet et al., 2004; Abe et al., 2009, 2012; Edosomwan et al., 2012; Mujinya et al., 2013). This enrichment in clay particles improves the resistance of termite mounds to predators and rain and it is usually more
* Corresponding author. E-mail address: [email protected] (P. Jouquet). http://dx.doi.org/10.1016/j.apsoil.2015.08.010 0929-1393/ ã 2015 Elsevier B.V. All rights reserved.
significant in long-lasting structures than in short-lived soil constructions (Jouquet et al., 2002, 2005, 2007, 2015a). Termites also influence soil chemical properties, such as soil C and N contents within their nest materials. However, the influence of termites on the C and N content is highly variable. For example, the soil organic matter (SOM) content in Macroterminae-built structures was reported to be similar (Eschenbrenner, 1986), higher (Black and Okwakol, 1997; Jouquet et al., 2003), or lower (Arshad et al., 1988; Garnier-Sillam and Harry, 1995; Contour-Ansel et al., 2000; Sall et al., 2002; Jouquet et al., 2005; Jouquet et al., 2015b) than the surrounding putative control soil. This large variability could be due to impacts specific to each termite species (the “behavior” force, sensu Harris, 1956) and the interaction between termite behavior and their environment (the “material” and “climate” forces). Although unstudied, it is also likely that the influence of termites on soil properties and their needs to control their environment vary according to the age of the termite colonies. Soil collection from deep layers requires more investment
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for young termite colonies, which are, therefore, likely to preferentially use the soil from the surface layer that is more easily available. In contrast, in the large network of galleries built over time by old colonies, termites may go deeper in the soil profile and use soil particles with a higher clay but lower C and N contents than soil in the surface layer. Nevertheless, to date the respective influences of the soil properties and colony age remain unknown. Termites are also held able to modify the shape of their mounds to control the humidity and temperature within their nests (Noirot and Darlington, 2000; Korb and Linsenmair, 1998a,b; 2001; Turner, 2004). However, this conclusion was only made from studies carried out in Africa or with African species, despite the fact that termite mounds are also conspicuous features of Asian landscapes (Jouquet et al., 2015c). In addition, the influence of the environment (usually the vegetation cover) on termite mound shapes has only been highlighted with cathedral and dome shaped Macrotermes sp. mound nests (i.e., Korb and Linsenmair, 1998a,b; 2001), while other genera also produce complex above-ground nest structures (i.e., species of the genus Odontotermes). More research is therefore needed to determine whether the ability of fungus-growing termites to adapt the properties and shape of their mounds is a generality rather than an exception. The species Odontotermes obesus (Macrotermitinae subfamily) produces some of the most impressive larger mounds that can be encountered in Southern India. These constructions are usually up to 2 m high with many circumvolutions (Roonwal, 1970, 1978) and resemble those produced by the African species Macrotermes bellicosus, whose archetypal mounds are commonly illustrated in books and reviews. Thus, the mounds of O. obesus can be used to test the concepts modeled from Macrotermes sp. concerning the factors determining termite mound composition and shape in general. The main aim of this study was therefore to determine whether the shape and properties of O. obesus mound constructions are constant or vary depending on the surrounding environment. A second objective was also to investigate whether the impact of termites on soil properties and termite mound shapes are constant for a given environment or if they vary according to the age of termite colonies. 2. Materials and methods 2.1. Study sites Termite mound properties and shapes were analysed in the Bandipur Tiger reserve forest (Mule Hole experimental watershed, Karnataka state, 11440 N and 76 260 E) and in the forest of the Jubilee Garden in the Indian Institute of Science (IISc, Bangalore city, Karnataka state, 13 010 N and 77 330 E). Soils are Ferralsols and Luvisols (World Reference Base for Soil Resources, 2014) or Oxisols and Alfisols (Soil Survey Staff, 1999), in Bandipur and IISc forests respectively (Barbiéro et al., 2007; Braun et al., 2009; Jouquet et al., 2015a,b). As a result of the short-term variability of the South–West Monsoon, the annual rainfall ranges from 900 to 1100 mm yr1 in both forests. In Bandipur forest, the vegetation is a dry deciduous woodland, dominated by the “ATT” facies (i.e., Anogeissus latifolia,Tectona grandis and Terminalia crenulata, Barbiero et al., 2007). In IISc, the vegetation is also a dry deciduous forest but it is dominated by Acacia trees, mainly Acacia auriculiformis, and to a lesser extent by Leucena leucocephala, Parkia biglandulosa, Gliricidia sepium and Delonix regia (Jouquet et al., 2015a). In these environments, Odontotermes obesus builds mounds that are very similar in shape to those produced by Macrotermes bellicosus in Africa with numerous ridges and complex structures (Roonwal, 1970,1978) (Fig. 1). Seventeen active termite mounds
Fig. 1. Examples of Odontotermes obesus termite mounds produced at IISc in the Luvisol (a) and at Bandipur in the Ferralsol (b) environments in Southern India (Karnataka). Photos P. Jouquet, April 2014.
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were randomly selected in Bandipur forest and all the termite mounds encountered in IISc were sampled (n = 13). 2.2. Soil physical and chemical properties Soil samples were collected from termite mound walls and in the surrounding soil surface environment (control, 0–5 cm deep, distance to termite mound: 5 m). The C and N concentrations in SOM were assessed with a CHN analyzer using a Flash 2000HT elemental analyzer. The clay content was measured after destruction of organic matter and dispersion with sodium hexametaphosphate (AFNOR, NFX 31 107) and using a laser particle size analyzer. Enrichment or loss in clay and C and N contents were calculated as the ratio of their concentrations in the termite mound wall to their concentrations in the surrounding soil environment (in%). 2.3. Termite mound architecture Termite mound dimensions were recorded in the field. Volumes and surfaces were assessed as if each nest was a perfect cone with the following equations: Volume = (p R2 h)/3 and Sestimated = p p R (R2 + h2), where R is the average radius and h the average height of the termite mound. The mound surface was also measured following the method described in Korb and Linsenmair (1998a) by placing toilet paper on termite mound wall and spraying it with water. The whole mounds were wrapped with negligible overlap between sheets. The surface (Smeasured) was measured by multiplying the number of sheets used to fully cover the mounds with the surface of the toilet paper sheet. Surface complexity (rsf) was calculated as the ratio Smeasured:Sestimated (Korb and Linsenmair, 1998a). 2.4. Statistical analyses
Fig. 2. Clay content in the termite mound wall (%) constructed by Odontotermes obesus (Macrotermitinae) compared to the content in control soil (%) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line (y = x). Table 1 C and N content (%) in control and termite mound soil. Values in parenthesis are standard errors (n = 13 in IISc (Luvisol) and n = 17 in Bandipur (Ferralsol)). Means listed in a column accompanied by the same capital letter are not significantly different at P < 0.05. C (%)
N (%)
Luvisol Control soil Termite soil
2.97 B (0.25) 1.14 D (0.10)
0.21 0.07
Ferralsol Control soil Termite soil
3.70 2.04
A C
(0.22) (0.12)
A C
(0.02) (0.01)
0.21 A (0.02) 0.12 B (0.01)
Higher C and N concentrations were always measured in the control soil than in the termite mound soil (Table 1). However, no relationship was found between the C and N contents in control soil and their concentrations in termite mound soils (Fig. 3a,b)
Differences between treatments were assessed using linear regressions and analyses of covariance (ANCOVA). Normality was tested with the Shapiro–Wilk test and the values were logtransformed if necessary. Analysis of variance (ANOVA) was used to analyse differences in C content and enrichment in C and N with treatments as independent variables. Differences between means were assessed with LSD tests. ANOVA assumptions were not met, even after data transformation, for the soil N content. Thus, pairwise comparisons were made with Kruskal-Wallis tests with a false discovery rate correction for measuring differences in N contents between treatments. All statistical calculations were carried out using R (R Development Core Team, 2008). Differences among treatments were declared significant at the <0.05 probability level. 3. Results 3.1. Clay, C and N contents in termite mounds As shown in Fig. 2 there was a positive linear relationship between the clay content in the termite mound wall and the clay content in the control soil surface (y = 0.89x + 13.41, R2 = 0.39, P = 0.029 and y = 0.97x + 3.50, R2 = 0.51, P = 0.001, for the Luvisol and Ferralsol, respectively). The regression slopes were not significantly different (P = 0.841). The enrichment in clay was significant ( P < 0.001 and P = 0.022, respectively for the Luvisol and Ferralsol compared with the bisecting line) and higher in the Luvisol than in the Ferralsol (i.e., significant difference in intercepts, P < 0.001) with values reaching 155.2% (Standard Error, SE: 8.0) and 118.0% (SE: 5.9), respectively ( F 1,27 = 14.8, P < 0.001).
Fig. 3. C (a) and N (b) concentrations in the termite mound wall (%) constructed by Odontotermes obesus (Macrotermitinae) compared to the control soil (%) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line (y = x).
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Fig. 4. The estimated versus the measured surface of termite mounds (m2) constructed by Odontotermes obesus (Macrotermitinae) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line y = x.
(R2 = 0.01, P = 0.838 and R2 = 0.10, P = 0.226 for the C contents in the Luvisol and Ferralsol respectively, and R2 = 0.01, P = 0.723 and R2 = 0.14, P = 0.157 for the N contents in the Luvisol and Ferralsol, respectively). On average, the C content in termite mounds reached 56.9 % (SE: 4.8) and 44.6% (SE: 4.5) of the C content in the control Ferralsol and Luvisol, respectively ( F1,27 = 5.90, P = 0.022). A similar trend was measured for the termite mound N content which reached 54.0% (SE: 4.2) and 41.3% (SE: 6.0) of that in the control soil in Ferralsol and Luvisol, respectively ( F1,27 = 4.22, P = 0.049). 3.2. Termite mound shape The relationship between measured and observed surfaces is shown in Fig. 4. Positive relationships were measured between Sestimated and Smeasured for both soil types and regression lines were above the bisecting line, suggesting that the rsf ratio >1. However, Smeasured increased more in the Ferralsol than the Luvisol (y = 2.58x, R2 = 0.87, P = 0.001, and y = 1.95x, R2 = 0.81, for Ferralsol and Luvisol, respectively, difference between slopes: P < 0.001). 3.3. Influence of termite mound size The rsf ratio increased with termite mound size in the Ferralsol (y = 2.50 + 1.67, R2 = 0.26, P = 0.0153) (Fig. 5). However, this linear relationship was not significant in the Luvisol ( P = 0.211) where rsf = 1.83 (SE: 0.13). Fig. 6a–c shows the influence of termite mound size on the C, N and clay enrichment in the termite mound wall compared to the control soil. No significant linear correlation was observed for the enrichments in C and N (R2 = 0.06, P = 0.450 and
Fig. 5. Termite mound complexity (rsf = Smeasured: Sestimated) related to termite mound volume (m3) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka).
Fig. 6. Enrichment in C (a), N (b) and clay (c) in the termite mound wall as a function of the termite mound volume (m3) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka).
R2 = 0.05, P = 0.377, for the enrichment in C content in the Luvisol and Ferralsol, respectively; R2 = 0.05, P = 0.510 and R2 = 0.07, P = 0.306 for the enrichment in N content in the Luvisol and the Ferralsol, respectively). Clay enrichment was also not linearly related to the volume of termite mounds in either the Luvisol or the Ferralsol (P = 0.515 and 0.319, respectively). 4. Discussion 4.1. Influence of the soil pedological properties As soil engineers, termites influence the physical, chemical and biological properties of tropical soils (Dangerfield et al., 1998; Jouquet et al., 2011, 2014; Bottinelli et al., 2015; Pennisi, 2015). The influence of termites on these soil properties has been shown in a large number of situations and this study confirmed the general assumption that termite mound walls have higher clay content and lower C and N contents than the surrounding surface soils (Abe and Wakatsuki, 2010; Abe et al., 2012; Millogo et al., 2011; Jouquet et al., 2015b). This study also showed that the physical and chemical properties of termite mound walls are variable and influenced by the soil type. For example, nests in the Luvisol showed higher enrichment in clay particles and impoverishment in C and N compared to the surrounding soil than those in the Ferralsol. Although we could not pinpoint the exact processes explaining these differences, they most likely result from differences in properties of deeper soil layers, which termites appear to use for their constructions (Holt and Lepage, 2000; Jouquet et al., 2011). In general, the lower C and N contents in termite mounds is due to the construction strategy of fungus-growing termites, which collect soil from deep soil layers impoverished in SOM
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content and only add salivary secretions (in contrast to soil feeding termites that add feces to their nests, Contour-Ansel et al., 2000). On the other hand, the enrichment in clay particles in termite mounds is usually explained by the need of termites to strengthen the cohesive forces between particles to ensure improved resistance against the erosive action of the rain and also probably against predators such as bears and pangolins (Jouquet et al., 2004, 2015b; Irshad et al., 2015). However, while the C and N contents in termite mound walls were constant and independent of the concentration in C and N in the soil surface layer, positive linear regressions were measured between the clay content in the termite mound wall and that in the control soil. These results highlight the close relationship between the abundance of clay in the environment and the properties of termite mound walls. They also suggest a more passive enrichment in clay in O. obesus mound walls rather than enrichment based on particle selection in response to termite ecological needs. Depending on their local environments, it is usually considered that termite nest structures can take a variety of shapes to control their internal temperature and humidity (Korb and Linsenmair, 1998a,b, 2001; Turner, 2004). However, this conclusion was made from studies comparing Macrotermes sp. mound architecture in West-African savanna versus gallery forests. In this study, termite mound shape complexity was higher in the Ferralsol than in the Luvisol, suggesting a possible link between the impact of termites on soil properties and mound shape complexity. We analysed mound shapes in two forests with very similar climates but different soil properties. Thus, we hypothesize that the increased termite mound complexity in the Ferralsol forest results from (i) differential dynamics of humidity and temperature even though similar decadal average rainfall and temperature values were measured in both ecosystems, and/or (ii) differences in soil properties. Recently, Jouquet et al. (2015b) showed that the resistance of termite mound soil to water erosion varies according to the soil properties, with lower soil aggregate stability in Vertisols than in Ferralsols. From this study, it is therefore likely that differences in soil properties between the Ferralsol and Luvisol influenced the resistance of the termite mounds to rain, and perhaps predators, and thus had an impact on the complexity of termite mound shape (e.g. the number of ridges and verticality of termite mounds). 4.2. Influence of termite mound size Although termites are considered as heterogeneity drivers (sensu Jouquet et al., 2015c) and termite mounds as hot-spots or patches with specific physical, chemical and biological properties at the ecosystem scale (e.g., Konaté et al., 1999; Choosai et al., 2009; Muvengwi et al., 2013; Seymour et al., 2014; Bonachela et al., 2015), very limited data are available on the heterogeneity in soil properties within termite mounds (Erens et al., 2015). Further, to our knowledge, no information is available on the evolution of termite mound properties over time. In this study, we used the termite mound volume as a proxy to estimate the age of the colonies (Collins, 1981; Tano and Lepage, 1990). However, no relationship was found between the volume of termite mounds and their C, N and clay contents at either study site. Therefore, the results suggest that (i) O. obesus uses soil from the same layer to construct their mound nests and (ii) this strategy is independent of colony age and the soil properties. Contrasting results were obtained concerning the evolution of termite mound shapes in the Luvisol and Ferralsol. The need to control the temperature and humidity within termite mounds is likely to increase with the increasing termite biomass and their associated fungus-comb. However, this study only showed a positive linear correlation between the termite mound volume and the rsf ratio in the
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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Influence of soil type on the properties of termite mound nests in Southern India Pascal Jouqueta,b,* , Nabila Guilleuxa,b , Rashmi Ramesh Shanbhagc, Sankaran Subramanianb a b c
Institute of Ecology and Environmental Sciences (UMR 242 iEES Paris), Institute of Research for Development (IRD), 32 av. H. Varagnat, 93143 Bondy, France Indo-French Cell for Water Science (IFCWS), Indian Institute of Science, 560 012 Bangalore, Karnataka, India Institute of Wood Science and Technology, Malleswaram, 560 003 Bangalore, Karnataka, India
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2015 Received in revised form 11 August 2015 Accepted 13 August 2015 Available online 9 September 2015
Termite mounds are conspicuous features in many tropical ecosystems. Their shape and soil physicochemical properties have been suggested to result from the termites ecological need to control the temperature and humidity within their nests and protect themselves from predators. This study aimed to determine the influence of the parent soil properties on the shape and soil physical and chemical properties of termite mounds. Termite mounds built by the fungus-growing termite species Odontotermes obesus were compared in two forests with different soil properties (Ferralsol or Luvisol) in Southern India. Our findings confirm that soil properties influence the physicochemical characteristics of mound material and may affect the shape, but these impacts are mostly independent of the size of the mounds (i.e., the age of the colonies). Mound walls were more enriched in clay and impoverished in C and N in the Luvisol than the Ferralsol. However, their shape was more complex in the Ferralsol than the Luvisol, suggesting a possible link between the clay content in soil and the shape of termite mounds. The results also suggest that clay becomes enriched in O. obesus mound walls through a more passive process rather than solely by particle selection, and that termite mound shape results from the soil properties rather than the ecological needs of termites. In conclusion, although ecologists have mainly focused upon the influence of termite ecological needs on their nest properties, this study highlights the need for a better understanding about the role of the soil pedological properties and, as a consequence, how these properties drive the establishment and survival of termites in tropical ecosystems. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Clay Ferralsol Luvisol Termite mound architecture
1. Introduction Fungus-growing termites (Termitidae, Macrotermitinae) construct belowground chambers or aboveground mounds to protect their colonies and their exo-symbiotic fungi. Depending on the challenge of their immediate environment, termites are assumed to modify the properties of their nests in two ways: first, by selecting and modifying the soil material they use and/or by modifying the shape of their mounds. For construction, fungus-growers transport clay-enriched soil from deep soil horizons to the soil surface (e.g., Jouquet et al., 2004; Abe et al., 2009, 2012; Edosomwan et al., 2012; Mujinya et al., 2013). This enrichment in clay particles improves the resistance of termite mounds to predators and rain and it is usually more
* Corresponding author. E-mail address: [email protected] (P. Jouquet). http://dx.doi.org/10.1016/j.apsoil.2015.08.010 0929-1393/ ã 2015 Elsevier B.V. All rights reserved.
significant in long-lasting structures than in short-lived soil constructions (Jouquet et al., 2002, 2005, 2007, 2015a). Termites also influence soil chemical properties, such as soil C and N contents within their nest materials. However, the influence of termites on the C and N content is highly variable. For example, the soil organic matter (SOM) content in Macroterminae-built structures was reported to be similar (Eschenbrenner, 1986), higher (Black and Okwakol, 1997; Jouquet et al., 2003), or lower (Arshad et al., 1988; Garnier-Sillam and Harry, 1995; Contour-Ansel et al., 2000; Sall et al., 2002; Jouquet et al., 2005; Jouquet et al., 2015b) than the surrounding putative control soil. This large variability could be due to impacts specific to each termite species (the “behavior” force, sensu Harris, 1956) and the interaction between termite behavior and their environment (the “material” and “climate” forces). Although unstudied, it is also likely that the influence of termites on soil properties and their needs to control their environment vary according to the age of the termite colonies. Soil collection from deep layers requires more investment
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for young termite colonies, which are, therefore, likely to preferentially use the soil from the surface layer that is more easily available. In contrast, in the large network of galleries built over time by old colonies, termites may go deeper in the soil profile and use soil particles with a higher clay but lower C and N contents than soil in the surface layer. Nevertheless, to date the respective influences of the soil properties and colony age remain unknown. Termites are also held able to modify the shape of their mounds to control the humidity and temperature within their nests (Noirot and Darlington, 2000; Korb and Linsenmair, 1998a,b; 2001; Turner, 2004). However, this conclusion was only made from studies carried out in Africa or with African species, despite the fact that termite mounds are also conspicuous features of Asian landscapes (Jouquet et al., 2015c). In addition, the influence of the environment (usually the vegetation cover) on termite mound shapes has only been highlighted with cathedral and dome shaped Macrotermes sp. mound nests (i.e., Korb and Linsenmair, 1998a,b; 2001), while other genera also produce complex above-ground nest structures (i.e., species of the genus Odontotermes). More research is therefore needed to determine whether the ability of fungus-growing termites to adapt the properties and shape of their mounds is a generality rather than an exception. The species Odontotermes obesus (Macrotermitinae subfamily) produces some of the most impressive larger mounds that can be encountered in Southern India. These constructions are usually up to 2 m high with many circumvolutions (Roonwal, 1970, 1978) and resemble those produced by the African species Macrotermes bellicosus, whose archetypal mounds are commonly illustrated in books and reviews. Thus, the mounds of O. obesus can be used to test the concepts modeled from Macrotermes sp. concerning the factors determining termite mound composition and shape in general. The main aim of this study was therefore to determine whether the shape and properties of O. obesus mound constructions are constant or vary depending on the surrounding environment. A second objective was also to investigate whether the impact of termites on soil properties and termite mound shapes are constant for a given environment or if they vary according to the age of termite colonies. 2. Materials and methods 2.1. Study sites Termite mound properties and shapes were analysed in the Bandipur Tiger reserve forest (Mule Hole experimental watershed, Karnataka state, 11440 N and 76 260 E) and in the forest of the Jubilee Garden in the Indian Institute of Science (IISc, Bangalore city, Karnataka state, 13 010 N and 77 330 E). Soils are Ferralsols and Luvisols (World Reference Base for Soil Resources, 2014) or Oxisols and Alfisols (Soil Survey Staff, 1999), in Bandipur and IISc forests respectively (Barbiéro et al., 2007; Braun et al., 2009; Jouquet et al., 2015a,b). As a result of the short-term variability of the South–West Monsoon, the annual rainfall ranges from 900 to 1100 mm yr1 in both forests. In Bandipur forest, the vegetation is a dry deciduous woodland, dominated by the “ATT” facies (i.e., Anogeissus latifolia,Tectona grandis and Terminalia crenulata, Barbiero et al., 2007). In IISc, the vegetation is also a dry deciduous forest but it is dominated by Acacia trees, mainly Acacia auriculiformis, and to a lesser extent by Leucena leucocephala, Parkia biglandulosa, Gliricidia sepium and Delonix regia (Jouquet et al., 2015a). In these environments, Odontotermes obesus builds mounds that are very similar in shape to those produced by Macrotermes bellicosus in Africa with numerous ridges and complex structures (Roonwal, 1970,1978) (Fig. 1). Seventeen active termite mounds
Fig. 1. Examples of Odontotermes obesus termite mounds produced at IISc in the Luvisol (a) and at Bandipur in the Ferralsol (b) environments in Southern India (Karnataka). Photos P. Jouquet, April 2014.
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were randomly selected in Bandipur forest and all the termite mounds encountered in IISc were sampled (n = 13). 2.2. Soil physical and chemical properties Soil samples were collected from termite mound walls and in the surrounding soil surface environment (control, 0–5 cm deep, distance to termite mound: 5 m). The C and N concentrations in SOM were assessed with a CHN analyzer using a Flash 2000HT elemental analyzer. The clay content was measured after destruction of organic matter and dispersion with sodium hexametaphosphate (AFNOR, NFX 31 107) and using a laser particle size analyzer. Enrichment or loss in clay and C and N contents were calculated as the ratio of their concentrations in the termite mound wall to their concentrations in the surrounding soil environment (in%). 2.3. Termite mound architecture Termite mound dimensions were recorded in the field. Volumes and surfaces were assessed as if each nest was a perfect cone with the following equations: Volume = (p R2 h)/3 and Sestimated = p p R (R2 + h2), where R is the average radius and h the average height of the termite mound. The mound surface was also measured following the method described in Korb and Linsenmair (1998a) by placing toilet paper on termite mound wall and spraying it with water. The whole mounds were wrapped with negligible overlap between sheets. The surface (Smeasured) was measured by multiplying the number of sheets used to fully cover the mounds with the surface of the toilet paper sheet. Surface complexity (rsf) was calculated as the ratio Smeasured:Sestimated (Korb and Linsenmair, 1998a). 2.4. Statistical analyses
Fig. 2. Clay content in the termite mound wall (%) constructed by Odontotermes obesus (Macrotermitinae) compared to the content in control soil (%) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line (y = x). Table 1 C and N content (%) in control and termite mound soil. Values in parenthesis are standard errors (n = 13 in IISc (Luvisol) and n = 17 in Bandipur (Ferralsol)). Means listed in a column accompanied by the same capital letter are not significantly different at P < 0.05. C (%)
N (%)
Luvisol Control soil Termite soil
2.97 B (0.25) 1.14 D (0.10)
0.21 0.07
Ferralsol Control soil Termite soil
3.70 2.04
A C
(0.22) (0.12)
A C
(0.02) (0.01)
0.21 A (0.02) 0.12 B (0.01)
Higher C and N concentrations were always measured in the control soil than in the termite mound soil (Table 1). However, no relationship was found between the C and N contents in control soil and their concentrations in termite mound soils (Fig. 3a,b)
Differences between treatments were assessed using linear regressions and analyses of covariance (ANCOVA). Normality was tested with the Shapiro–Wilk test and the values were logtransformed if necessary. Analysis of variance (ANOVA) was used to analyse differences in C content and enrichment in C and N with treatments as independent variables. Differences between means were assessed with LSD tests. ANOVA assumptions were not met, even after data transformation, for the soil N content. Thus, pairwise comparisons were made with Kruskal-Wallis tests with a false discovery rate correction for measuring differences in N contents between treatments. All statistical calculations were carried out using R (R Development Core Team, 2008). Differences among treatments were declared significant at the <0.05 probability level. 3. Results 3.1. Clay, C and N contents in termite mounds As shown in Fig. 2 there was a positive linear relationship between the clay content in the termite mound wall and the clay content in the control soil surface (y = 0.89x + 13.41, R2 = 0.39, P = 0.029 and y = 0.97x + 3.50, R2 = 0.51, P = 0.001, for the Luvisol and Ferralsol, respectively). The regression slopes were not significantly different (P = 0.841). The enrichment in clay was significant ( P < 0.001 and P = 0.022, respectively for the Luvisol and Ferralsol compared with the bisecting line) and higher in the Luvisol than in the Ferralsol (i.e., significant difference in intercepts, P < 0.001) with values reaching 155.2% (Standard Error, SE: 8.0) and 118.0% (SE: 5.9), respectively ( F 1,27 = 14.8, P < 0.001).
Fig. 3. C (a) and N (b) concentrations in the termite mound wall (%) constructed by Odontotermes obesus (Macrotermitinae) compared to the control soil (%) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line (y = x).
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Fig. 4. The estimated versus the measured surface of termite mounds (m2) constructed by Odontotermes obesus (Macrotermitinae) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka). The dashed line corresponds to the bisecting line y = x.
(R2 = 0.01, P = 0.838 and R2 = 0.10, P = 0.226 for the C contents in the Luvisol and Ferralsol respectively, and R2 = 0.01, P = 0.723 and R2 = 0.14, P = 0.157 for the N contents in the Luvisol and Ferralsol, respectively). On average, the C content in termite mounds reached 56.9 % (SE: 4.8) and 44.6% (SE: 4.5) of the C content in the control Ferralsol and Luvisol, respectively ( F1,27 = 5.90, P = 0.022). A similar trend was measured for the termite mound N content which reached 54.0% (SE: 4.2) and 41.3% (SE: 6.0) of that in the control soil in Ferralsol and Luvisol, respectively ( F1,27 = 4.22, P = 0.049). 3.2. Termite mound shape The relationship between measured and observed surfaces is shown in Fig. 4. Positive relationships were measured between Sestimated and Smeasured for both soil types and regression lines were above the bisecting line, suggesting that the rsf ratio >1. However, Smeasured increased more in the Ferralsol than the Luvisol (y = 2.58x, R2 = 0.87, P = 0.001, and y = 1.95x, R2 = 0.81, for Ferralsol and Luvisol, respectively, difference between slopes: P < 0.001). 3.3. Influence of termite mound size The rsf ratio increased with termite mound size in the Ferralsol (y = 2.50 + 1.67, R2 = 0.26, P = 0.0153) (Fig. 5). However, this linear relationship was not significant in the Luvisol ( P = 0.211) where rsf = 1.83 (SE: 0.13). Fig. 6a–c shows the influence of termite mound size on the C, N and clay enrichment in the termite mound wall compared to the control soil. No significant linear correlation was observed for the enrichments in C and N (R2 = 0.06, P = 0.450 and
Fig. 5. Termite mound complexity (rsf = Smeasured: Sestimated) related to termite mound volume (m3) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka).
Fig. 6. Enrichment in C (a), N (b) and clay (c) in the termite mound wall as a function of the termite mound volume (m3) for samples collected in the Luvisol (circle in white) and Ferralsol (in grey) in Southern India (Karnataka).
R2 = 0.05, P = 0.377, for the enrichment in C content in the Luvisol and Ferralsol, respectively; R2 = 0.05, P = 0.510 and R2 = 0.07, P = 0.306 for the enrichment in N content in the Luvisol and the Ferralsol, respectively). Clay enrichment was also not linearly related to the volume of termite mounds in either the Luvisol or the Ferralsol (P = 0.515 and 0.319, respectively). 4. Discussion 4.1. Influence of the soil pedological properties As soil engineers, termites influence the physical, chemical and biological properties of tropical soils (Dangerfield et al., 1998; Jouquet et al., 2011, 2014; Bottinelli et al., 2015; Pennisi, 2015). The influence of termites on these soil properties has been shown in a large number of situations and this study confirmed the general assumption that termite mound walls have higher clay content and lower C and N contents than the surrounding surface soils (Abe and Wakatsuki, 2010; Abe et al., 2012; Millogo et al., 2011; Jouquet et al., 2015b). This study also showed that the physical and chemical properties of termite mound walls are variable and influenced by the soil type. For example, nests in the Luvisol showed higher enrichment in clay particles and impoverishment in C and N compared to the surrounding soil than those in the Ferralsol. Although we could not pinpoint the exact processes explaining these differences, they most likely result from differences in properties of deeper soil layers, which termites appear to use for their constructions (Holt and Lepage, 2000; Jouquet et al., 2011). In general, the lower C and N contents in termite mounds is due to the construction strategy of fungus-growing termites, which collect soil from deep soil layers impoverished in SOM
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content and only add salivary secretions (in contrast to soil feeding termites that add feces to their nests, Contour-Ansel et al., 2000). On the other hand, the enrichment in clay particles in termite mounds is usually explained by the need of termites to strengthen the cohesive forces between particles to ensure improved resistance against the erosive action of the rain and also probably against predators such as bears and pangolins (Jouquet et al., 2004, 2015b; Irshad et al., 2015). However, while the C and N contents in termite mound walls were constant and independent of the concentration in C and N in the soil surface layer, positive linear regressions were measured between the clay content in the termite mound wall and that in the control soil. These results highlight the close relationship between the abundance of clay in the environment and the properties of termite mound walls. They also suggest a more passive enrichment in clay in O. obesus mound walls rather than enrichment based on particle selection in response to termite ecological needs. Depending on their local environments, it is usually considered that termite nest structures can take a variety of shapes to control their internal temperature and humidity (Korb and Linsenmair, 1998a,b, 2001; Turner, 2004). However, this conclusion was made from studies comparing Macrotermes sp. mound architecture in West-African savanna versus gallery forests. In this study, termite mound shape complexity was higher in the Ferralsol than in the Luvisol, suggesting a possible link between the impact of termites on soil properties and mound shape complexity. We analysed mound shapes in two forests with very similar climates but different soil properties. Thus, we hypothesize that the increased termite mound complexity in the Ferralsol forest results from (i) differential dynamics of humidity and temperature even though similar decadal average rainfall and temperature values were measured in both ecosystems, and/or (ii) differences in soil properties. Recently, Jouquet et al. (2015b) showed that the resistance of termite mound soil to water erosion varies according to the soil properties, with lower soil aggregate stability in Vertisols than in Ferralsols. From this study, it is therefore likely that differences in soil properties between the Ferralsol and Luvisol influenced the resistance of the termite mounds to rain, and perhaps predators, and thus had an impact on the complexity of termite mound shape (e.g. the number of ridges and verticality of termite mounds). 4.2. Influence of termite mound size Although termites are considered as heterogeneity drivers (sensu Jouquet et al., 2015c) and termite mounds as hot-spots or patches with specific physical, chemical and biological properties at the ecosystem scale (e.g., Konaté et al., 1999; Choosai et al., 2009; Muvengwi et al., 2013; Seymour et al., 2014; Bonachela et al., 2015), very limited data are available on the heterogeneity in soil properties within termite mounds (Erens et al., 2015). Further, to our knowledge, no information is available on the evolution of termite mound properties over time. In this study, we used the termite mound volume as a proxy to estimate the age of the colonies (Collins, 1981; Tano and Lepage, 1990). However, no relationship was found between the volume of termite mounds and their C, N and clay contents at either study site. Therefore, the results suggest that (i) O. obesus uses soil from the same layer to construct their mound nests and (ii) this strategy is independent of colony age and the soil properties. Contrasting results were obtained concerning the evolution of termite mound shapes in the Luvisol and Ferralsol. The need to control the temperature and humidity within termite mounds is likely to increase with the increasing termite biomass and their associated fungus-comb. However, this study only showed a positive linear correlation between the termite mound volume and the rsf ratio in the
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