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Individual shrubs, large scale grass cover and seasonal rainfall explain invertebrate-derived macropore density in a semi-arid Namibian savanna
Journal of Arid Environments 176 (2020) 104101
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Individual shrubs, large scale grass cover and seasonal rainfall explain invertebrate-derived macropore density in a semi-arid Namibian savanna
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Arnim Marquart∗, Katja Geissler, Jessica Heblach, Christoph Lobas, Elise Münch, Niels Blaum Department of Plant Ecology and Nature Conservation, Institute of Biochemistry and Biology, University of Potsdam, Am Mühlenberg 3, 14476, Potsdam, Germany
A R T I C LE I N FO
A B S T R A C T
Keywords: Macropores Ecosystem engineers Shrub-encroachment Ecosystem functioning Soil fauna Land degradation
Macropores created by invertebrates improve ecosystem functions such as soil properties and hydrological processes. In semi-arid savannas, where water is the main limiting resource and precipitation is scarce macropores might increase infiltration, and thereby improve water availability for plants. Macropores may therefore represent a buffering mechanism counteracting degradation in the form of shrub-encroachment. We investigated the interacting effects of vegetation structures at small scales and vegetation cover at landscape scales, and seasonality on invertebrate macropores. First, macropore density and size distribution was measured at open soil, in direct proximity to perennial grass tussocks and shrubs, at grass dominated, intermediate and shrub dominated sites. Secondly, we recorded macropores on randomly chosen plots along a shrub cover gradient at three points in time within the rainy season. Individual shrubs and the amount of large scale grass cover increased macropore densities. Interestingly, macropore numbers were highest at the beginning of the rainy season. We argue that macropore densities reflect the activity and influence of soil macrofauna on ecosystem functioning, which is greatest at highly heterogeneous vegetation. Rangeland management should aim for high grass cover with scattered shrubs for sustainable soil health, by applying appropriate stocking rates, selectively removing shrubs or reseeding perennial grasses.
1. Introduction In drylands the risk of degradation is predicted to be greatest in semi-arid climate where both sensitivity to degradation and human population pressure are of intermediate value (Safriel et al., 2006). Degradation in semi-arid savannas is often caused by heavy livestock grazing which, in combination with other factors as precipitation and drought frequency, can lead to shrub encroachment (Jeltsch et al., 2000; Lohmann et al., 2012; Roques et al., 2001). The increase of shrub density, in combination with a decrease of perennial palatable grasses, often leads to a decrease in carrying capacity, impaired soil water budgets and nutrient cycling, landscape fragmentation, and habitat loss for local animal and plant species (e.g. Archer, 2009; Eldridge et al., 2011). There is a solid body of literature on the effects of shrub encroachment on vegetation structure (e.g. Lett and Knapp, 2005) and related abundance and diversity of various animal groups, as mammals (Blaum et al., 2007b, 2007a), birds (Sirami et al., 2009), and insects (Blaum et al., 2009; Hering et al., 2019; Wiezik et al., 2013). However, only few have focused on functional groups as macropore-building arthropods. Especially in the light of shrub encroachment, macropore-building
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invertebrates might play a vital role in maintaining ecosystem services and counteracting degradation (Byers et al., 2006; Jouquet et al., 2006; Lavelle et al., 2006). Semi-arid savanna ecosystems, which are often affected by shrub thickening, are mostly nutrient limited and driven by low seasonal water availability (D'Odorico and Porporato, 2006; Sankaran et al., 2005). Thereby, it is crucial for plant survival that a relatively large fraction of the scarce rain water infiltrates into the soil and becomes available to plants and is not lost by surface run-off and evaporation (Popp et al., 2009). Furthermore, it is expected that in future precipitation events will become less frequent but more intense, due to climate change, leading to an increased risk of drought (Diffenbaugh and Field, 2013; Van der Esch et al., 2017). Therefore, we presume that the effect of macropore-building invertebrates on water infiltration dynamics and nutrient pools in soils will be of increasing relevance under future climatic conditions. The activity of macroporebuilding invertebrates is considered a potential buffer for climate change in savannas (Bonachela et al., 2015), and as these climate zones are most prone to degradation and extreme climate events, these organisms may play a crucial role in restoration management (Byers et al., 2006; Colloff et al., 2010; Kaiser et al., 2017). Due to their far reaching impacts on ecosystems, macropore-creating invertebrates can
Corresponding author. E-mail address: [email protected] (A. Marquart).
https://doi.org/10.1016/j.jaridenv.2020.104101 Received 10 May 2019; Received in revised form 10 October 2019; Accepted 9 January 2020 0140-1963/ © 2020 Elsevier Ltd. All rights reserved.
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Fig. 1. (A) Map of Namibia with annual rainfall (shades of grey indicate isoclines at 50-mm intervals). The study location is indicated by the square. (B) Sentinel-2 satellite image of the study location (Feb. 2017, only Band 8: Near Infrared Reflectance: darker colour indicates higher vegetation density; derived with QGIS 2.18.26). The small squares indicate the seven 50 m × 50 m study sites along the shrub gradient; the larger white squares indicate the study sites where macropores were surveyed next to vegetation structures (not to scale). (C) Schematic representation of one study site with 40 macropore survey plots (small squares) along four transects, and 10 vegetation survey plots (large squares) along two transects. (D) Exemplary photograph of one 50 cm × 50 cm plot with four differently sized macropores (indicated by white circles).
surrounding ecosystem. Soil-burrowing dung beetles improve soil-hydrological properties, by increasing water infiltration and soil porosity, and reducing surface water runoff (Brown et al., 2010). However, most studies only analyzed the ecosystem function of a specific taxon of soil engineering invertebrates. In contrast, Colloff et al. (2010) demonstrated an increase in infiltration induced by the total number of invertebrate macropores. In a previous study, we also found a higher number of macropores under shrub canopies compared to open soil, increasing the sub-canopy soil's infiltration capacity (Marquart et al. in revision). Therefore, we argue that the number and sizes of macropores might give a good indication of the strength and effectivity exerted by macropore-building species on ecosystem functioning. However, it remains unclear to which extent the activity of these mostly herbivore macropore-building invertebrates is influenced by the proximate presence of single plants or rather by broad scale vegetation cover. We would expect a higher number of invertebrate created macropores next to vegetation structures, especially under shrub canopies, compared to open soil. In particular, shrubs are known to provide favorable habitats for macro-arthropods (i.e. increased soil litter biomass and soil moisture, improved soil texture, and soil fertility) (Zhao and Liu, 2013). On the broader landscape scale, we hypothesize that macropores would be most abundant in areas with intermediate shrub cover levels, as arthropod richness is highest at medium encroached states, and arthropod abundance was found to be positively correlated with shrub cover (Blaum et al., 2009; Hering et al., 2019). Furthermore, vegetation cover in a grassland ecosystem was found to be correlated with the mound size of subterranean ant species (Blomqvist et al., 2000). Previous studies have found a higher soil macro-arthropod density during the rainy season compared to the dry season (Vikram Reddy and Venkataiah, 1990). Termites, as macropore-building species, display mixed results, but for semi-arid to arid environments their
be regarded as ecosystem engineers. Ecosystem engineers are defined as organisms that modulate the availability of resources for other species by causing physical state changes in biotic or abiotic materials (Jones et al., 1996, 1997). In soil, the relative importance of regulation imposed by ecosystem engineering is likely to be greater than trophic relationships (Lavelle, 2002). However, until today most research on macropore-creating organisms focused on earthworms in temperate ecosystems (Jouquet et al., 2006). In tropical and subtropical climate zones, including a large fraction of global drylands, the functional invertebrate species engineering soils are primarily termite and ant species (Jouquet et al., 2006). In drylands, macropore-creating invertebrates can influence ecosystems on multiple scales inducing far reaching effects and feedbacks (Colloff et al., 2010; Jouquet et al., 2006; Lavelle et al., 2006). Termites, for example, have the capacity to build galleries and modify soil aggregates on different scales. On the scale of soil structure, termite activity impacts soil's clay content and nutrient cycling, thereby affecting inter alia the water holding capacity. On the soil profile scale, large amounts of soil are translocated and increased soil porosity is leading to higher water infiltration rates and preferential flow. On the landscape level, these combined effects increase heterogeneity by generating islands of fertility and are counteracting water runoff and erosion (Bottinelli et al., 2015; Jouquet et al., 2016). Thereby termite mounds shape the spatial structure of vegetation on large scales (e.g. Bonachela et al., 2015). Even though termites are the most prominent representatives of tropical soil ecosystem engineers, several subterranean ant and beetle species are also considered to impact ecosystems in a likewise manner. For example, Nkem et al. (2000) showed that ants influence soil structure, nutrient distribution, porosity, and infiltration beyond the parameter of the mound and into the 2
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2.2. Vegetation surveys on a shrub cover gradient We established a shrub cover gradient with seven study sites of 0.25 ha (50 m × 50 m). The gradient was located within the same interdune from grassland regions to highly shrub encroached areas with an average distance of 740 m, but a minimum of 500 m between study sites (Fig. 1B). Shrub cover was calculated as the sum of the canopy areas (except for V. erioloba, which is a typical grassland tree) divided by the total site area, resulting in shrub cover values ranging from 0 to 22%. Grass canopy cover and species composition on each study site was recorded in ten regular spaced subplots (5 m × 5 m) along two transects with five subplots each. Transects were set 15 m apart from the site edges with an inter-subplot spacing of 5 m (Fig. 1C). Fig. 2. Cumulative precipitation throughout the rainy season, measured on the study area. Periods of macropore surveys are indicated by shaded areas.
2.3. Macropore surveys First, we surveyed macropores on randomly chosen subplots on seven 50m × 50m plots along a shrub cover gradient (0–22% shrub canopy cover) at the beginning, in the peak and at the end of the rainy season to test for a landscape and seasonal effect (Fig. 2). On each study site, 10 subplots (50 cm × 50 cm) were established along four transects, respectively, and all invertebrate derived surface macropores were counted and divided into three size classes (small: < 5 mm; medium: 5–10 mm, large: > 10 mm) (Fig. 1C&D). We used this approach to keep subplot selection identical among study sites and independent of single shrubs and grass tussocks. Apart from macropore numbers and size, the surveys included small scale parameters, as distance of the subplot to next shrub and grass cover on the subplot. Second, we surveyed macropores specifically neighboring shrubs, grass tussocks and open soil on a grass dominated, intermediate and shrub encroached plot, respectively, to test for small scale effects of vegetation structures and their interaction with broad scale shrub encroachment (Fig. 1B). On one grass dominated, one intermediate and one shrub dominated study site, 10 S. mellifera shrubs, 10 large perennial grass tussocks and 10 interspace plots on open soil, respectively, were randomly chosen. At each vegetation structure and interspace plot three subplots (50 cm × 50 cm) were established in direct proximity and macropores were surveyed as described above.
activity mostly peaked within the rainy season (e.g. Davies et al., 2015; Dawes-Gromadzki and Spain, 2003). Temporal dynamics of macroporebuilding arthropod activity within the rainy season have not been reported yet. Here, we research if macropore dynamics are primarily controlled by vegetation structure on a small scale or by landscape wide vegetation cover in a semi-arid Namibian savanna rangeland. The largest fraction of Namibian land surface is used for extensive livestock farming as main agricultural activity, making shrub encroachment through degradation to one of the major social concerns (Namibia Ministry of Environment and Tourism, 2011). However, shrub encroachment in semi-arid savannas is a global phenomenon (Eldridge et al., 2011; Naito and Cairns, 2011) and therefore, its impact on soil faunal activity of general interest. In this study, we used two approaches at different scales of grass and shrub cover to test how vegetation affects invertebrate macropore numbers and size, as a proxy for soil-burrowing invertebrates’ activity. 2. Methods 2.1. Study site description
2.4. Analysis
The study was conducted on the commercial livestock farm Ebenhazer in the western Kalahari, Omaheke region with a mean elevation of 1340 m above seas level (23°13′14.6″S 18°26′49.5″E; Fig. 1A). Livestock comprised mostly cattle and sheep with 0.04–0.08 livestock units (LSU)/ha. One LSU is the grazing equivalent of one adult dairy cow. Mean annual precipitation in this area is 267 mm, but precipitation is highly variable (annual precipitation coefficient of variance = 95 mm). Mean annual temperature is 19.6 °C with an average minimum temperature of 6.2 °C in winter (May–November) and an average maximum temperature of 30.8 °C in summer (December–April) (1970–2010; Fick and Hijmans, 2017). The landscape is defined by NW-SE orientated, parallel running longitudinal dunes, rising 15 m above the plain located north-east of the farm (Fig. 1B). The inter-dunes are characterized by sporadically occurring, scattered calcareous outcrops. The soils are ferralic arenosol and are acidic (pH 5.8 ± 0.4) with a low organic matter content (0.89 ± 0.33%; mean and standard deviation of 10 topsoil samples), and with little horizon development. The sandy soil is nutrient-poor and primarily consists of fine, aeolian deposited sand grains with a ferric coating (Dougill and Thomas, 2004), and a mean sum of silt and clay of 5.2 ± 1.6% (mean and standard deviation of 10 soil samples at 10 cm depth). The most common woody species are Vachellia erioloba, Senegalia mellifera and Vachelia hebeclada. The grass layer mainly consists of the perennial species Stipagrostis uniplumis, Aristida stipitata, A. meridionalis, and the annual species Schmidtia kalahariensis, Eragrostis cylindriflora, E. biflora, and Pogonarthria fleckii.
A two-stage approach was used to analyze the effect of measured variables on both, the surface macropores at different vegetation cover, as well as surface macropores at microsites. At the microsite level we first used a generalized linear mixed model with a Poisson error distribution to analyze the effects of microsite (grass, shrub, bare soil), broad scale vegetation (grass dominated, intermediate, shrub dominated), and their interaction on the number of macropores. We included a random block variable to account for the three pseudo-replicates at each microsite. In a second step, a linear mixed model was fitted to test the influence of microsite and broad-scale vegetation on the averaged total macropore area, using a dataset where measurements without macropore counts were eliminated. We used generalized linear models with a quasi-Poisson error distribution to analyze the effect of large scale vegetation cover (shrub and grass canopy cover of the 50 m × 50 m plots) and time in season (early, mid, late) on macropore densities. In a second step, a linear mixed model was fitted to test the influence of time in season and large scale vegetation cover on the averaged total macropore area, using a dataset where measurements without macropore counts were eliminated. Prior to analysis, all values of macropore area were square-rooted and log10 transformed to meet the assumption of normality. Standardized residuals were used to visually test the assumptions. Minimal adequate models were chosen by AIC comparison. Analysis was conducted in R Version 3.5.1 (R Core Team, 2018). The significance level of all test 3
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Fig. 3. Effect of small scale vegetation structures on macropore numbers. Bars show the averaged sums of counted macropores under shrub canopies, neighboring large grass tussocks and on open soil plots. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
Fig. 4. Effect of landscape wide vegetation structure on macropore numbers. Bars show the averaged sums of counted macropores on grass dominated, intermediate and shrub dominated plots. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
statistics was p = 0.05.
3. Results No significant negative correlation between shrub cover and cover of perennial grasses was not found (r = −0.43, p = 0.3). However, the highest perennial grass canopy cover of nearly 20% was found on the plot without shrubs. At the highest shrub cover, we found a rather high perennial grass cover of 16%. The canopy cover of annual grasses was over all low and did not exceed 2%. Both, individual plants on a small scale and vegetation cover on landscape scale, as well as the recording time during the rainy season affected the number and area of invertebrate surface macropores. The number of surface macropores was on average four times higher under shrub canopies than on open soil and next to grass tussocks (χ22 = 74.3, p < 0.001) (Fig. 3). The higher macropore numbers were accompanied by the corresponding total area of macropores (shrub: 3.66 ± 0.39 mm2; open soil: 0.68 ± 0.13 mm2; grass: 1.00 ± 0.13 mm2) (χ22 = 49.76, p < 0.001). On the landscape scale, the number and area of macropores were approximately twice as high on the grass dominated plot compared to the shrub dominated plot (number of macropores: χ22 = 10.61, p < 0.01; area of macropores: χ22 = 5.99, p < 0.05) (Fig. 4). An interaction effect between vegetation on the small scale and landscape scale tends to explain the lower macropore numbers in the shrub dominated plot mainly by a decreased effect of single shrubs on macropores, but not of microsites neighboring grasses or open soil (χ24 = 8.73, p = 0.068) (Fig. 5). Time in season strongly impacted the number of visible macropores along the shrub gradient, with twice the amount of macropores in the beginning of the rainy season, after only a few rain events, compared to the middle and end of the rainy season (F1,836 = 26.97, p < 0.001) (Fig. 6). Landscape-wide areal grass cover had a positive but rather weak effect on macropore density (F1,836 = 19.31, p < 0.001) with the highest average macropore density at the plot with the highest grass cover of 19% (Fig. 7). Large scale shrub cover had no effect on the averaged macropore number and area. The largest fraction of macropores surveyed were constructed by Isoptera and Formicidea and to a lesser proportion by Scarabidea and Carabidea. Since we only rarely could observe the specific species associated to a particular macropore type and because many macropores
Fig. 5. Interaction plot between landscape scale effect and small scale vegetation structures on the linear prediction of macropore numbers derived from the linear regression model. The different vegetation structures are indicated by different symbols and line types. Note that the interaction effect was slightly non-significant (p = 0.068), but the AIC of the interaction model was lower in model comparison.
were hardly identifiable, we did not determine a precise taxon, but for the clearly identifiable types (i.e. ants, termites, beetles) we did not observe a pattern between treatments. 4. Discussion In this study, we examined the interacting effects of small scale vegetation structures and vegetation cover at landscape scale on the amount and size of invertebrate derived surface macropores, as a proxy for soil-burrowing invertebrate activity, at three different times during a rainy season in a semi-arid Namibian rangeland. Our results indicated a positive effect of single shrubs on the small scale and grass canopy cover on the landscape scale on soil-burrowing invertebrate activity. Furthermore, the highest numbers of macropores were surveyed at the beginning of the rainy season. Together our results indicate that the retention of shrubs in savanna environments and potential reseeding of perennial grasses could increase soil invertebrate abundance and activity, and thereby improve multiple ecosystem functions such as water 4
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invertebrate assemblage (Doblas-Miranda et al., 2009; Liu et al., 2013) in different dryland ecosystems. On the local scale we found the largest fraction of macropores associated with shrubs most likely because subcanopy soils are favorable habitats for soil invertebrates in terms of temperature, shelter, and sustenance (Zhao and Liu, 2013). Furthermore, shrubs are focal points of soil moisture, independently of macropores, due to less evaporation caused by shading, hydraulic lift, and lower soil bulk density (e.g. because sub-canopy soil is less prone to trampling by large herbivores). These factors moreover improve shrubs as nesting sites for soil macro-fauna (Zhao and Liu, 2013). The increased amount of macropores created by soil invertebrates under shrub canopies, on the other hand, feeds back on the soil's infiltration capacity (Marquart et al., 2019, in revision) and may increase the shrubs accessibility of water. In addition, many soil arthropods, as termite and ant species, increase decomposition of plant organic matter, thereby enhancing nutrient availability for the shrubs and ground vegetation in the shrubs zone of influence (Cammeraat and Risch, 2008; Riutta et al., 2012; Zhang et al., 2015). Even though little is known regarding direct effects of macropores on plant physiology, there is indeed an indication that perennial grasses which grow in proximity to macropores have a higher drought tolerance (Geissler et al., unpublished data). Thus, the direct effect of shrubs in combination with soil-macrofauna-mediated effects can improve soil health and support vegetation surrounding the shrubs in relatively densely shrub covered savanna systems.
Fig. 6. Temporal effect during the rainy season on macropore numbers. Bars show the averaged sums of counted macropores at the three macropore surveys at the beginning, middle and end of the rainy season. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
4.2. Effect of broad scale vegetation cover On the large scale the highest numbers of macropores were measured in grass dominated sites, both on sampling plots along transects as well as plots specifically placed next to shrubs, grass tussocks, and open soil. Although this positive effect of grass cover at landscape scale might at first seem contradictory to the local effect of shrubs, it becomes very plausible given that a high grass canopy cover in combination with scattered shrubs results in a highly heterogeneous and diverse vegetation. Harvester ants (Messor sp.), which are very common macroporecreating arthropods in the Kalahari region, depend on grass seeds as nutrition. A patchy mosaic of shrubs, grasses and forbs represents a structural complex habitat which has been found to increase arthropod diversity compared to degraded and shrub-encroached states (Gardner et al., 1995). Thus, a more complex diverse vegetation might indirectly lead to a bottom-up effect increasing abundance of carnivorous macropore-creating arthropods as Cicindelinae larvae, Chilopoda species or scorpions (Haddad et al., 2009). This increase in ecosystem complexity might explain the interaction effect of large and local scale vegetation, where the positive effect of local shrubs on macropores is dampened in a larger scale shrub dominated ecosystem.
Fig. 7. Effect of landscape wide areal grass cover on macropore numbers. Error bars represent standard errors of the mean. The regression line is derived from the generalized linear model.
4.3. Temporal effect on macropores
infiltration and litter decomposition. The majority of macropores in our study were constructed by Isoptera, Formicidea, and to a lesser proportion by Scarabidea and Carabidea – all groups which are known to affect ecosystem functioning (Brown et al., 2010; Cammeraat and Risch, 2008; Jouquet et al., 2016). We think that our focus on the diverse spectrum of visible surface macropores very well reflects the spatial-temporal ecosystem engineering outcome. Hence, the combined burrowing activity of different soil-burrowing invertebrates can affect the ecosystem on multiple levels.
We found significantly higher numbers of macropores at the beginning of the rainy season after just a few rain events, compared with later measurements, which suggests that the initial increase in soil moisture might have triggered soil invertebrate activity after the long dry period. With high activity of soil arthropods and the construction of a large number of macropores after the first rain events the positive effects on the ecosystem, i.e. increased water infiltration and an enhanced litter decomposition, immediately gain in importance in the beginning of the vegetation period.
4.1. Effect of neighboring vegetation
5. Conclusions
Our results are in accordance with a number of publications regarding the relationship between vegetation and soil fauna. Individual shrubs have been shown to increase the densities of termites (Christ, 1998), seed-harvester ants (Rissing, 1988), and the total soil macro-
It is well documented that macropore-building invertebrates exert wide reaching effects on soil properties and are therefore considered as soil engineers which influence the availability of resources for other organisms, including microorganisms and plants (Jones et al., 1996, 5
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1997). In this study we showed that the burrowing activity of invertebrates (as amount of actual found macropores) and therefore their beneficial impact on the ecosystem were controlled by vegetation on both the local and broad scale. Shrub presence thereby plays an important role at the small scale, while overall grass cover enhances the positive effect of shrubs. In the light of shrub encroachment, we suggest a paradigm shift. Shrubs should not be regarded as the main problem per se, but rather degradation in form of decreasing grass cover and vegetation complexity. Semi-arid savannas are often prone to heavy livestock grazing, which gives shrubs a competitive advantage over perennial grasses and amplifies degradation. An adjusted management system and stocking rate might counteract degradation, by increasing grass cover on the broad scale and therefore soil invertebrate activity. On the other hand, when shrub clearing or thinning are chosen as management option to fight shrub encroachment, an appropriate shrub density should be retained in the system to maintain a healthy vegetation heterogeneity. However, we think that in the future a stronger focus should be directed on the relationship between macropore dynamics and soil ecosystem functioning. Macropores and their spatial and temporal distribution might function as a good indicator for soil health, and could easily and expeditiously be surveyed for rangeland assessments.
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Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments We would like to acknowledge the financial support of the German Federal Ministry of Education and Research (BMBF) in the framework of the SPACES project OPTIMASS (FKZ: 01LL1302A). This research was carried out under research permit no. 2226/2016 of the Namibian Ministry of Environment and Tourism. We would like to thank Pieter Hugo for the possibility and infrastructure to conduct our research on the Ebenhazer farm. References Archer, S.R., 2009. Rangeland conservation and shrub encroachment: new perspectives on an old problem. In: Wild Rangelands. John Wiley & Sons, Ltd, pp. 53–97. https:// doi.org/10.1002/9781444317091.ch4. Blaum, N., Rossmanith, E., Jeltsch, F., 2007a. Land use affects rodent communities in Kalahari savannah rangelands. Afr. J. Ecol. 45, 189–195. https://doi.org/10.1111/j. 1365-2028.2006.00696.x. Blaum, N., Rossmanith, E., Popp, A., Jeltsch, F., 2007b. Shrub encroachment affects mammalian carnivore abundance and species richness in semiarid rangelands. Acta Oecol. 31, 86–92. https://doi.org/10.1016/j.actao.2006.10.004. Blaum, N., Seymour, C., Rossmanith, E., Schwager, M., Jeltsch, F., 2009. Changes in arthropod diversity along a land use driven gradient of shrub cover in savanna rangelands: identification of suitable indicators. Biodivers. Conserv. 18, 1187–1199. https://doi.org/10.1007/s10531-008-9498-x. Blomqvist, M.M., Olff, H., Blaauw, M.B., Bongers, T., Putten, W.H.V.D., 2000. Interactions between above- and belowground biota: importance for small-scale vegetation mosaics in a grassland ecosystem. Oikos 90, 582–598. https://doi.org/10.1034/j.16000706.2000.900316.x. Bonachela, J.A., Pringle, R.M., Sheffer, E., Coverdale, T.C., Guyton, J.A., Caylor, K.K., Levin, S.A., Tarnita, C.E., 2015. Termite mounds can increase the robustness of dryland ecosystems to climatic change. Science 347, 651–655. https://doi.org/10. 1126/science.1261487. Bottinelli, N., Jouquet, P., Capowiez, Y., Podwojewski, P., Grimaldi, M., Peng, X., 2015. Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil and Tillage Research. Soil Structure and its Functions in Ecosystems: Phase matter & Scale matter 146, 118–124. https://doi.org/10.1016/j.still.2014.01. 007. Brown, J., Scholtz, C.H., Janeau, J.-L., Grellier, S., Podwojewski, P., 2010. Dung beetles (Coleoptera: scarabaeidae) can improve soil hydrological properties. Appl. Soil Ecol. 46, 9–16. https://doi.org/10.1016/j.apsoil.2010.05.010. Byers, J.E., Cuddington, K., Jones, C.G., Talley, T.S., Hastings, A., Lambrinos, J.G., Crooks, J.A., Wilson, W.G., 2006. Using ecosystem engineers to restore ecological systems. Trends Ecol. Evol. 21, 493–500. https://doi.org/10.1016/j.tree.2006.06.
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February, E.C., Frost, P.G.H., Hiernaux, P., Hrabar, H., Metzger, K.L., Prins, H.H.T., Ringrose, S., Sea, W., Tews, J., Worden, J., Zambatis, N., 2005. Determinants of woody cover in African savannas. Nature 438, 846–849. https://doi.org/10.1038/ nature04070. Sirami, C., Seymour, C., Midgley, G., Barnard, P., 2009. The impact of shrub encroachment on savanna bird diversity from local to regional scale. Divers. Distrib. 15, 948–957. https://doi.org/10.1111/j.1472-4642.2009.00612.x. Van der Esch, S., ten Brink, B., Stehfest, E., Bakkenes, M., Sewell, A., Bouwman, A., Meijer, J., Westhoek, H., van den Berg, M., 2017. Exploring Future Changes in Land Use and Land Condition and the Impacts on Food, Water, Climate Change and Biodiversity: Scenarios for the Global Land Outlook. PBL Netherlands Environmental Assessment Agency, The Hague. Vikram Reddy, M., Venkataiah, B., 1990. Seasonal abundance of soil-surface arthropods in relation to some meteorological and edaphic variables of the grassland and treeplanted areas in a tropical semi-arid savanna. Int. J. Biometeorol. 34, 49–59. https:// doi.org/10.1007/BF01045820. Wiezik, M., Svitok, M., Wieziková, A., Dovčiak, M., 2013. Shrub encroachment alters composition and diversity of ant communities in abandoned grasslands of western Carpathians. Biodivers. Conserv. 22, 2305–2320. https://doi.org/10.1007/s10531013-0446-z. Zhang, W., Yuan, S., Hu, N., Lou, Y., Wang, S., 2015. Predicting soil fauna effect on plant litter decomposition by using boosted regression trees. Soil Biol. Biochem. 82, 81–86. https://doi.org/10.1016/j.soilbio.2014.12.016. Zhao, H.-L., Liu, R.-T., 2013. The “bug island” effect of shrubs and its formation mechanism in Horqin Sand Land, Inner Mongolia. Catena 105, 69–74. https://doi.org/ 10.1016/j.catena.2013.01.009.
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Individual shrubs, large scale grass cover and seasonal rainfall explain invertebrate-derived macropore density in a semi-arid Namibian savanna
T
Arnim Marquart∗, Katja Geissler, Jessica Heblach, Christoph Lobas, Elise Münch, Niels Blaum Department of Plant Ecology and Nature Conservation, Institute of Biochemistry and Biology, University of Potsdam, Am Mühlenberg 3, 14476, Potsdam, Germany
A R T I C LE I N FO
A B S T R A C T
Keywords: Macropores Ecosystem engineers Shrub-encroachment Ecosystem functioning Soil fauna Land degradation
Macropores created by invertebrates improve ecosystem functions such as soil properties and hydrological processes. In semi-arid savannas, where water is the main limiting resource and precipitation is scarce macropores might increase infiltration, and thereby improve water availability for plants. Macropores may therefore represent a buffering mechanism counteracting degradation in the form of shrub-encroachment. We investigated the interacting effects of vegetation structures at small scales and vegetation cover at landscape scales, and seasonality on invertebrate macropores. First, macropore density and size distribution was measured at open soil, in direct proximity to perennial grass tussocks and shrubs, at grass dominated, intermediate and shrub dominated sites. Secondly, we recorded macropores on randomly chosen plots along a shrub cover gradient at three points in time within the rainy season. Individual shrubs and the amount of large scale grass cover increased macropore densities. Interestingly, macropore numbers were highest at the beginning of the rainy season. We argue that macropore densities reflect the activity and influence of soil macrofauna on ecosystem functioning, which is greatest at highly heterogeneous vegetation. Rangeland management should aim for high grass cover with scattered shrubs for sustainable soil health, by applying appropriate stocking rates, selectively removing shrubs or reseeding perennial grasses.
1. Introduction In drylands the risk of degradation is predicted to be greatest in semi-arid climate where both sensitivity to degradation and human population pressure are of intermediate value (Safriel et al., 2006). Degradation in semi-arid savannas is often caused by heavy livestock grazing which, in combination with other factors as precipitation and drought frequency, can lead to shrub encroachment (Jeltsch et al., 2000; Lohmann et al., 2012; Roques et al., 2001). The increase of shrub density, in combination with a decrease of perennial palatable grasses, often leads to a decrease in carrying capacity, impaired soil water budgets and nutrient cycling, landscape fragmentation, and habitat loss for local animal and plant species (e.g. Archer, 2009; Eldridge et al., 2011). There is a solid body of literature on the effects of shrub encroachment on vegetation structure (e.g. Lett and Knapp, 2005) and related abundance and diversity of various animal groups, as mammals (Blaum et al., 2007b, 2007a), birds (Sirami et al., 2009), and insects (Blaum et al., 2009; Hering et al., 2019; Wiezik et al., 2013). However, only few have focused on functional groups as macropore-building arthropods. Especially in the light of shrub encroachment, macropore-building
∗
invertebrates might play a vital role in maintaining ecosystem services and counteracting degradation (Byers et al., 2006; Jouquet et al., 2006; Lavelle et al., 2006). Semi-arid savanna ecosystems, which are often affected by shrub thickening, are mostly nutrient limited and driven by low seasonal water availability (D'Odorico and Porporato, 2006; Sankaran et al., 2005). Thereby, it is crucial for plant survival that a relatively large fraction of the scarce rain water infiltrates into the soil and becomes available to plants and is not lost by surface run-off and evaporation (Popp et al., 2009). Furthermore, it is expected that in future precipitation events will become less frequent but more intense, due to climate change, leading to an increased risk of drought (Diffenbaugh and Field, 2013; Van der Esch et al., 2017). Therefore, we presume that the effect of macropore-building invertebrates on water infiltration dynamics and nutrient pools in soils will be of increasing relevance under future climatic conditions. The activity of macroporebuilding invertebrates is considered a potential buffer for climate change in savannas (Bonachela et al., 2015), and as these climate zones are most prone to degradation and extreme climate events, these organisms may play a crucial role in restoration management (Byers et al., 2006; Colloff et al., 2010; Kaiser et al., 2017). Due to their far reaching impacts on ecosystems, macropore-creating invertebrates can
Corresponding author. E-mail address: [email protected] (A. Marquart).
https://doi.org/10.1016/j.jaridenv.2020.104101 Received 10 May 2019; Received in revised form 10 October 2019; Accepted 9 January 2020 0140-1963/ © 2020 Elsevier Ltd. All rights reserved.
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Fig. 1. (A) Map of Namibia with annual rainfall (shades of grey indicate isoclines at 50-mm intervals). The study location is indicated by the square. (B) Sentinel-2 satellite image of the study location (Feb. 2017, only Band 8: Near Infrared Reflectance: darker colour indicates higher vegetation density; derived with QGIS 2.18.26). The small squares indicate the seven 50 m × 50 m study sites along the shrub gradient; the larger white squares indicate the study sites where macropores were surveyed next to vegetation structures (not to scale). (C) Schematic representation of one study site with 40 macropore survey plots (small squares) along four transects, and 10 vegetation survey plots (large squares) along two transects. (D) Exemplary photograph of one 50 cm × 50 cm plot with four differently sized macropores (indicated by white circles).
surrounding ecosystem. Soil-burrowing dung beetles improve soil-hydrological properties, by increasing water infiltration and soil porosity, and reducing surface water runoff (Brown et al., 2010). However, most studies only analyzed the ecosystem function of a specific taxon of soil engineering invertebrates. In contrast, Colloff et al. (2010) demonstrated an increase in infiltration induced by the total number of invertebrate macropores. In a previous study, we also found a higher number of macropores under shrub canopies compared to open soil, increasing the sub-canopy soil's infiltration capacity (Marquart et al. in revision). Therefore, we argue that the number and sizes of macropores might give a good indication of the strength and effectivity exerted by macropore-building species on ecosystem functioning. However, it remains unclear to which extent the activity of these mostly herbivore macropore-building invertebrates is influenced by the proximate presence of single plants or rather by broad scale vegetation cover. We would expect a higher number of invertebrate created macropores next to vegetation structures, especially under shrub canopies, compared to open soil. In particular, shrubs are known to provide favorable habitats for macro-arthropods (i.e. increased soil litter biomass and soil moisture, improved soil texture, and soil fertility) (Zhao and Liu, 2013). On the broader landscape scale, we hypothesize that macropores would be most abundant in areas with intermediate shrub cover levels, as arthropod richness is highest at medium encroached states, and arthropod abundance was found to be positively correlated with shrub cover (Blaum et al., 2009; Hering et al., 2019). Furthermore, vegetation cover in a grassland ecosystem was found to be correlated with the mound size of subterranean ant species (Blomqvist et al., 2000). Previous studies have found a higher soil macro-arthropod density during the rainy season compared to the dry season (Vikram Reddy and Venkataiah, 1990). Termites, as macropore-building species, display mixed results, but for semi-arid to arid environments their
be regarded as ecosystem engineers. Ecosystem engineers are defined as organisms that modulate the availability of resources for other species by causing physical state changes in biotic or abiotic materials (Jones et al., 1996, 1997). In soil, the relative importance of regulation imposed by ecosystem engineering is likely to be greater than trophic relationships (Lavelle, 2002). However, until today most research on macropore-creating organisms focused on earthworms in temperate ecosystems (Jouquet et al., 2006). In tropical and subtropical climate zones, including a large fraction of global drylands, the functional invertebrate species engineering soils are primarily termite and ant species (Jouquet et al., 2006). In drylands, macropore-creating invertebrates can influence ecosystems on multiple scales inducing far reaching effects and feedbacks (Colloff et al., 2010; Jouquet et al., 2006; Lavelle et al., 2006). Termites, for example, have the capacity to build galleries and modify soil aggregates on different scales. On the scale of soil structure, termite activity impacts soil's clay content and nutrient cycling, thereby affecting inter alia the water holding capacity. On the soil profile scale, large amounts of soil are translocated and increased soil porosity is leading to higher water infiltration rates and preferential flow. On the landscape level, these combined effects increase heterogeneity by generating islands of fertility and are counteracting water runoff and erosion (Bottinelli et al., 2015; Jouquet et al., 2016). Thereby termite mounds shape the spatial structure of vegetation on large scales (e.g. Bonachela et al., 2015). Even though termites are the most prominent representatives of tropical soil ecosystem engineers, several subterranean ant and beetle species are also considered to impact ecosystems in a likewise manner. For example, Nkem et al. (2000) showed that ants influence soil structure, nutrient distribution, porosity, and infiltration beyond the parameter of the mound and into the 2
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2.2. Vegetation surveys on a shrub cover gradient We established a shrub cover gradient with seven study sites of 0.25 ha (50 m × 50 m). The gradient was located within the same interdune from grassland regions to highly shrub encroached areas with an average distance of 740 m, but a minimum of 500 m between study sites (Fig. 1B). Shrub cover was calculated as the sum of the canopy areas (except for V. erioloba, which is a typical grassland tree) divided by the total site area, resulting in shrub cover values ranging from 0 to 22%. Grass canopy cover and species composition on each study site was recorded in ten regular spaced subplots (5 m × 5 m) along two transects with five subplots each. Transects were set 15 m apart from the site edges with an inter-subplot spacing of 5 m (Fig. 1C). Fig. 2. Cumulative precipitation throughout the rainy season, measured on the study area. Periods of macropore surveys are indicated by shaded areas.
2.3. Macropore surveys First, we surveyed macropores on randomly chosen subplots on seven 50m × 50m plots along a shrub cover gradient (0–22% shrub canopy cover) at the beginning, in the peak and at the end of the rainy season to test for a landscape and seasonal effect (Fig. 2). On each study site, 10 subplots (50 cm × 50 cm) were established along four transects, respectively, and all invertebrate derived surface macropores were counted and divided into three size classes (small: < 5 mm; medium: 5–10 mm, large: > 10 mm) (Fig. 1C&D). We used this approach to keep subplot selection identical among study sites and independent of single shrubs and grass tussocks. Apart from macropore numbers and size, the surveys included small scale parameters, as distance of the subplot to next shrub and grass cover on the subplot. Second, we surveyed macropores specifically neighboring shrubs, grass tussocks and open soil on a grass dominated, intermediate and shrub encroached plot, respectively, to test for small scale effects of vegetation structures and their interaction with broad scale shrub encroachment (Fig. 1B). On one grass dominated, one intermediate and one shrub dominated study site, 10 S. mellifera shrubs, 10 large perennial grass tussocks and 10 interspace plots on open soil, respectively, were randomly chosen. At each vegetation structure and interspace plot three subplots (50 cm × 50 cm) were established in direct proximity and macropores were surveyed as described above.
activity mostly peaked within the rainy season (e.g. Davies et al., 2015; Dawes-Gromadzki and Spain, 2003). Temporal dynamics of macroporebuilding arthropod activity within the rainy season have not been reported yet. Here, we research if macropore dynamics are primarily controlled by vegetation structure on a small scale or by landscape wide vegetation cover in a semi-arid Namibian savanna rangeland. The largest fraction of Namibian land surface is used for extensive livestock farming as main agricultural activity, making shrub encroachment through degradation to one of the major social concerns (Namibia Ministry of Environment and Tourism, 2011). However, shrub encroachment in semi-arid savannas is a global phenomenon (Eldridge et al., 2011; Naito and Cairns, 2011) and therefore, its impact on soil faunal activity of general interest. In this study, we used two approaches at different scales of grass and shrub cover to test how vegetation affects invertebrate macropore numbers and size, as a proxy for soil-burrowing invertebrates’ activity. 2. Methods 2.1. Study site description
2.4. Analysis
The study was conducted on the commercial livestock farm Ebenhazer in the western Kalahari, Omaheke region with a mean elevation of 1340 m above seas level (23°13′14.6″S 18°26′49.5″E; Fig. 1A). Livestock comprised mostly cattle and sheep with 0.04–0.08 livestock units (LSU)/ha. One LSU is the grazing equivalent of one adult dairy cow. Mean annual precipitation in this area is 267 mm, but precipitation is highly variable (annual precipitation coefficient of variance = 95 mm). Mean annual temperature is 19.6 °C with an average minimum temperature of 6.2 °C in winter (May–November) and an average maximum temperature of 30.8 °C in summer (December–April) (1970–2010; Fick and Hijmans, 2017). The landscape is defined by NW-SE orientated, parallel running longitudinal dunes, rising 15 m above the plain located north-east of the farm (Fig. 1B). The inter-dunes are characterized by sporadically occurring, scattered calcareous outcrops. The soils are ferralic arenosol and are acidic (pH 5.8 ± 0.4) with a low organic matter content (0.89 ± 0.33%; mean and standard deviation of 10 topsoil samples), and with little horizon development. The sandy soil is nutrient-poor and primarily consists of fine, aeolian deposited sand grains with a ferric coating (Dougill and Thomas, 2004), and a mean sum of silt and clay of 5.2 ± 1.6% (mean and standard deviation of 10 soil samples at 10 cm depth). The most common woody species are Vachellia erioloba, Senegalia mellifera and Vachelia hebeclada. The grass layer mainly consists of the perennial species Stipagrostis uniplumis, Aristida stipitata, A. meridionalis, and the annual species Schmidtia kalahariensis, Eragrostis cylindriflora, E. biflora, and Pogonarthria fleckii.
A two-stage approach was used to analyze the effect of measured variables on both, the surface macropores at different vegetation cover, as well as surface macropores at microsites. At the microsite level we first used a generalized linear mixed model with a Poisson error distribution to analyze the effects of microsite (grass, shrub, bare soil), broad scale vegetation (grass dominated, intermediate, shrub dominated), and their interaction on the number of macropores. We included a random block variable to account for the three pseudo-replicates at each microsite. In a second step, a linear mixed model was fitted to test the influence of microsite and broad-scale vegetation on the averaged total macropore area, using a dataset where measurements without macropore counts were eliminated. We used generalized linear models with a quasi-Poisson error distribution to analyze the effect of large scale vegetation cover (shrub and grass canopy cover of the 50 m × 50 m plots) and time in season (early, mid, late) on macropore densities. In a second step, a linear mixed model was fitted to test the influence of time in season and large scale vegetation cover on the averaged total macropore area, using a dataset where measurements without macropore counts were eliminated. Prior to analysis, all values of macropore area were square-rooted and log10 transformed to meet the assumption of normality. Standardized residuals were used to visually test the assumptions. Minimal adequate models were chosen by AIC comparison. Analysis was conducted in R Version 3.5.1 (R Core Team, 2018). The significance level of all test 3
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Fig. 3. Effect of small scale vegetation structures on macropore numbers. Bars show the averaged sums of counted macropores under shrub canopies, neighboring large grass tussocks and on open soil plots. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
Fig. 4. Effect of landscape wide vegetation structure on macropore numbers. Bars show the averaged sums of counted macropores on grass dominated, intermediate and shrub dominated plots. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
statistics was p = 0.05.
3. Results No significant negative correlation between shrub cover and cover of perennial grasses was not found (r = −0.43, p = 0.3). However, the highest perennial grass canopy cover of nearly 20% was found on the plot without shrubs. At the highest shrub cover, we found a rather high perennial grass cover of 16%. The canopy cover of annual grasses was over all low and did not exceed 2%. Both, individual plants on a small scale and vegetation cover on landscape scale, as well as the recording time during the rainy season affected the number and area of invertebrate surface macropores. The number of surface macropores was on average four times higher under shrub canopies than on open soil and next to grass tussocks (χ22 = 74.3, p < 0.001) (Fig. 3). The higher macropore numbers were accompanied by the corresponding total area of macropores (shrub: 3.66 ± 0.39 mm2; open soil: 0.68 ± 0.13 mm2; grass: 1.00 ± 0.13 mm2) (χ22 = 49.76, p < 0.001). On the landscape scale, the number and area of macropores were approximately twice as high on the grass dominated plot compared to the shrub dominated plot (number of macropores: χ22 = 10.61, p < 0.01; area of macropores: χ22 = 5.99, p < 0.05) (Fig. 4). An interaction effect between vegetation on the small scale and landscape scale tends to explain the lower macropore numbers in the shrub dominated plot mainly by a decreased effect of single shrubs on macropores, but not of microsites neighboring grasses or open soil (χ24 = 8.73, p = 0.068) (Fig. 5). Time in season strongly impacted the number of visible macropores along the shrub gradient, with twice the amount of macropores in the beginning of the rainy season, after only a few rain events, compared to the middle and end of the rainy season (F1,836 = 26.97, p < 0.001) (Fig. 6). Landscape-wide areal grass cover had a positive but rather weak effect on macropore density (F1,836 = 19.31, p < 0.001) with the highest average macropore density at the plot with the highest grass cover of 19% (Fig. 7). Large scale shrub cover had no effect on the averaged macropore number and area. The largest fraction of macropores surveyed were constructed by Isoptera and Formicidea and to a lesser proportion by Scarabidea and Carabidea. Since we only rarely could observe the specific species associated to a particular macropore type and because many macropores
Fig. 5. Interaction plot between landscape scale effect and small scale vegetation structures on the linear prediction of macropore numbers derived from the linear regression model. The different vegetation structures are indicated by different symbols and line types. Note that the interaction effect was slightly non-significant (p = 0.068), but the AIC of the interaction model was lower in model comparison.
were hardly identifiable, we did not determine a precise taxon, but for the clearly identifiable types (i.e. ants, termites, beetles) we did not observe a pattern between treatments. 4. Discussion In this study, we examined the interacting effects of small scale vegetation structures and vegetation cover at landscape scale on the amount and size of invertebrate derived surface macropores, as a proxy for soil-burrowing invertebrate activity, at three different times during a rainy season in a semi-arid Namibian rangeland. Our results indicated a positive effect of single shrubs on the small scale and grass canopy cover on the landscape scale on soil-burrowing invertebrate activity. Furthermore, the highest numbers of macropores were surveyed at the beginning of the rainy season. Together our results indicate that the retention of shrubs in savanna environments and potential reseeding of perennial grasses could increase soil invertebrate abundance and activity, and thereby improve multiple ecosystem functions such as water 4
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invertebrate assemblage (Doblas-Miranda et al., 2009; Liu et al., 2013) in different dryland ecosystems. On the local scale we found the largest fraction of macropores associated with shrubs most likely because subcanopy soils are favorable habitats for soil invertebrates in terms of temperature, shelter, and sustenance (Zhao and Liu, 2013). Furthermore, shrubs are focal points of soil moisture, independently of macropores, due to less evaporation caused by shading, hydraulic lift, and lower soil bulk density (e.g. because sub-canopy soil is less prone to trampling by large herbivores). These factors moreover improve shrubs as nesting sites for soil macro-fauna (Zhao and Liu, 2013). The increased amount of macropores created by soil invertebrates under shrub canopies, on the other hand, feeds back on the soil's infiltration capacity (Marquart et al., 2019, in revision) and may increase the shrubs accessibility of water. In addition, many soil arthropods, as termite and ant species, increase decomposition of plant organic matter, thereby enhancing nutrient availability for the shrubs and ground vegetation in the shrubs zone of influence (Cammeraat and Risch, 2008; Riutta et al., 2012; Zhang et al., 2015). Even though little is known regarding direct effects of macropores on plant physiology, there is indeed an indication that perennial grasses which grow in proximity to macropores have a higher drought tolerance (Geissler et al., unpublished data). Thus, the direct effect of shrubs in combination with soil-macrofauna-mediated effects can improve soil health and support vegetation surrounding the shrubs in relatively densely shrub covered savanna systems.
Fig. 6. Temporal effect during the rainy season on macropore numbers. Bars show the averaged sums of counted macropores at the three macropore surveys at the beginning, middle and end of the rainy season. The grey-scale fractions of the bars represent the three macropore size classes. Error bars represent standard errors of the mean.
4.2. Effect of broad scale vegetation cover On the large scale the highest numbers of macropores were measured in grass dominated sites, both on sampling plots along transects as well as plots specifically placed next to shrubs, grass tussocks, and open soil. Although this positive effect of grass cover at landscape scale might at first seem contradictory to the local effect of shrubs, it becomes very plausible given that a high grass canopy cover in combination with scattered shrubs results in a highly heterogeneous and diverse vegetation. Harvester ants (Messor sp.), which are very common macroporecreating arthropods in the Kalahari region, depend on grass seeds as nutrition. A patchy mosaic of shrubs, grasses and forbs represents a structural complex habitat which has been found to increase arthropod diversity compared to degraded and shrub-encroached states (Gardner et al., 1995). Thus, a more complex diverse vegetation might indirectly lead to a bottom-up effect increasing abundance of carnivorous macropore-creating arthropods as Cicindelinae larvae, Chilopoda species or scorpions (Haddad et al., 2009). This increase in ecosystem complexity might explain the interaction effect of large and local scale vegetation, where the positive effect of local shrubs on macropores is dampened in a larger scale shrub dominated ecosystem.
Fig. 7. Effect of landscape wide areal grass cover on macropore numbers. Error bars represent standard errors of the mean. The regression line is derived from the generalized linear model.
4.3. Temporal effect on macropores
infiltration and litter decomposition. The majority of macropores in our study were constructed by Isoptera, Formicidea, and to a lesser proportion by Scarabidea and Carabidea – all groups which are known to affect ecosystem functioning (Brown et al., 2010; Cammeraat and Risch, 2008; Jouquet et al., 2016). We think that our focus on the diverse spectrum of visible surface macropores very well reflects the spatial-temporal ecosystem engineering outcome. Hence, the combined burrowing activity of different soil-burrowing invertebrates can affect the ecosystem on multiple levels.
We found significantly higher numbers of macropores at the beginning of the rainy season after just a few rain events, compared with later measurements, which suggests that the initial increase in soil moisture might have triggered soil invertebrate activity after the long dry period. With high activity of soil arthropods and the construction of a large number of macropores after the first rain events the positive effects on the ecosystem, i.e. increased water infiltration and an enhanced litter decomposition, immediately gain in importance in the beginning of the vegetation period.
4.1. Effect of neighboring vegetation
5. Conclusions
Our results are in accordance with a number of publications regarding the relationship between vegetation and soil fauna. Individual shrubs have been shown to increase the densities of termites (Christ, 1998), seed-harvester ants (Rissing, 1988), and the total soil macro-
It is well documented that macropore-building invertebrates exert wide reaching effects on soil properties and are therefore considered as soil engineers which influence the availability of resources for other organisms, including microorganisms and plants (Jones et al., 1996, 5
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1997). In this study we showed that the burrowing activity of invertebrates (as amount of actual found macropores) and therefore their beneficial impact on the ecosystem were controlled by vegetation on both the local and broad scale. Shrub presence thereby plays an important role at the small scale, while overall grass cover enhances the positive effect of shrubs. In the light of shrub encroachment, we suggest a paradigm shift. Shrubs should not be regarded as the main problem per se, but rather degradation in form of decreasing grass cover and vegetation complexity. Semi-arid savannas are often prone to heavy livestock grazing, which gives shrubs a competitive advantage over perennial grasses and amplifies degradation. An adjusted management system and stocking rate might counteract degradation, by increasing grass cover on the broad scale and therefore soil invertebrate activity. On the other hand, when shrub clearing or thinning are chosen as management option to fight shrub encroachment, an appropriate shrub density should be retained in the system to maintain a healthy vegetation heterogeneity. However, we think that in the future a stronger focus should be directed on the relationship between macropore dynamics and soil ecosystem functioning. Macropores and their spatial and temporal distribution might function as a good indicator for soil health, and could easily and expeditiously be surveyed for rangeland assessments.
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