Termite mounds reduce soil microbial diversity by filtering rare microbial taxa

Termites are ubiquitous insects in tropical and subtropical habitats, and some of them construct massive nests (‘mounds’), which substantially promote substrate heterogeneity by altering soil properties. Yet, the role of termite nesting process in regulating the distribution and diversity of soil microbial communities remains poorly understood, which introduces uncertainty in predictions of ecosystem functions of termite mounds in a changing environment. Here, by using amplicon sequencing, we conducted a survey of 134 termite mounds across >1500 km in northern Australia and found that termite mounds significantly differed from bulk soils in the microbial diversity and community compositions. Compared with bulk soils, termite nesting process decreased the microbial diversity and the relative abundance of rare taxa. Rare taxa had a narrower habitat niche breadth than dominant taxa and might be easier to be filtered by the potential intensive microbial competition during the nesting processes. We further demonstrated that the shift in pH induced by termite nesting process was a major driver shaping the microbial community profiles in termite mounds. Together, our work provides novel evidence that termite nesting is an important process in regulating soil microbial diversity, which advances our understanding of the functioning of termite mounds.     

Macrotermes mounds as sites for tree regeneration in a Sudanian woodland (Burkina Faso)

The importance of mounds created by Macrotermes subhyalinus as safe site for tree regeneration was analysed in a savannah woodland of Burkina Faso. Plantlets (height <1.5 m) were sampled and followed over an year in 72 × 4 m² quadrats located on M. subhyalinus mounds and adjacent areas. The mechanisms of regeneration and plantlet mortality were also determined. We identified three regeneration mechanisms: seedlings regenerated by seed (abundant on mounds), sprouts (abundant on adjacent areas) and root suckers (a rare case on both sites). A total of 37 species representing 17 families and 30 genera were found on all quadrats, of which 29 species were found on termite mounds and 22 species on adjacent areas. Species richness and density of plantlets at the 4 m² scale were higher on mounds than in the adjacent area (P < 0.05). Among plantlet categories, seedling density was significantly different among microhabitats (P < 0.001) and across sampling periods (P < 0.01) and, the majority of plantlet individuals appeared within the 0–25 cm height class. The mortality of plantlets and particularly seedling mortality differed significantly between microhabitats (P < 0.01) and between periods (P < 0.01), whereas more than half the variation in the death of Acacia erythrocalyx seedlings (the most abundant species) were related to the density of the live seedlings of the same species (P < 0.001). The observed mortality rate was way below 50%; plantlet density remained higher on mound during sampling periods as compared to the adjacent area. It can thus be concluded that Macrotermes termite mounds are favourable sites for the recruitments of woody plants in savannah woodlands.     

Contribution of the Western Australian wheatbelt termite,Drepanotermes tamminensis (Hill), to the soil nutrient budget

The role of soil modification by the mound-building termite,Drepanotermes tamminensis (Hill), was studied during 1991 in the Durokoppin Nature Reserve, Western Australia. Soil chemical parameters were quantified for ‘soils’ in nests and for surrounding soil in both a Wandoo (Eucalyptus capillosa) woodland and a Casuarina (Allocasuarina campestris) shrubland plot. All ‘soils’ in nests were more acidic than the surrounding soil within each study plot. Generally, nutrient levels in the nested soils were higher than the un-nested soil within each study plot and were also higher in the woodland than in the shrubland plot. Depending on the nuttient concerned, the nested soil contained between 0.3 and 21.9% of the total nutrient load per hectare within each study plot. The quantities of nutrients per hectare in termite mounds were higher in the woodland than in the shrubland plot. It is concluded that mounds of this species of termite form a significant bank of nutrients, although time for release of such nutrients depends on the degree of erosion and on the longevity of mounds.     

Geophagic termite mounds as one of the resources for African elephants in Ugalla Game Reserve,Western Tanzania

Knowledge of the distribution and nutrient values of key resources supporting the survival of wildlife species is integral for an effective conservation planning and management of the species. In the Miombo ecosystem of the Ugalla Game Reserve, African elephants (Loxodonta africana Blumenbach 1797), eat soil, that is geophagy, from certain termite mounds. We mapped that all the geophagic termite mounds are exclusively situated in the flood plain. To understand why soils from some termite mounds are eaten, we collected and analysed soil samples from 10 geophagic termite mounds, seven nongeophagic termite mounds and 13 samples from the surrounding flood plain. Percentage of clay content did not differ significantly among the soil samples. Soils from geophagic termite mounds were richer in mineral elements compared with other soil samples. The results demonstrate that the driver for geophagic behaviour is related to rich mineral element contents found in geophagic termite mounds made of the mineral‐enriching termites (Macrotermes). Thus, geophagic termite mounds play a role in elephant's dietary needs and possibly influence their movement patterns in Ugalla, as the elephants cannot obtain enough minerals from their feeds. Geophagic termite mounds should be protected from potential destructive land uses, such as airstrip construction.     

Termite mound density and distribution patterns across three land-use types in the Vhembe District of the Limpopo Province,South Africa

This study investigated the effect of land-use on density and distribution patterns of termite mounds. A total area of 12 ha was investigated using four 1 ha plots from each of three land-use types (mango orchards, maize fields and communal rangelands). A total of 297 mounds from four termite species were recorded. Plotted GIS coordinates for each mound in ArcMap showed a random distribution pattern in all land-use types. The mean number of mounds per hectare was significantly higher (p < 0.001) in communal rangelands (52.5 ± 1.21), than in maize fields (14.75 ± 3.15) and mango orchards (7.5 ± 0.87), and dominated by small-sized mounds of Trinervitermes sp. Few mounds of Odontotermes sp. were found. Mounds of the edible termites, Macrotermes natalensis and M. falciger, were found in all land-use types, with the highest density for both species being in maize fields. Although the mound height for both species was similar, mound circumference for M. falciger was significantly larger (p < 0.001) which may limit land available for agricultural use. Density of mounds was influenced by land-use which may lead to changes in termite ecosystem functioning and availability of termites as a free source of protein.     

Effects of Erosion from Mounds of Different Termite Genera on Distinct Functional Grassland Types in an African Savannah

A key aspect of savannah vegetation heterogeneity is mosaics formed by two functional grassland types, bunch grasslands, and grazing lawns. We investigated the role of termites, important ecosystem engineers, in creating high-nutrient patches in the form of grazing lawns. Some of the ways termites can contribute to grazing lawn development is through erosion of soil from aboveground mounds to the surrounding soil surface. This may alter the nutrient status of the surrounding soils. We hypothesize that the importance of this erosion varies with termite genera, depending on feeding strategy and mound type. To test this, we simulated erosion by applying mound soil from three termite genera (Macrotermes, Odontotermes, and Trinervitermes) in both a field experiment and a greenhouse experiment. In the greenhouse experiment, we found soils with the highest macro nutrient levels (formed by Trinervitermes) promoted the quality and biomass of both a lawn (Digitaria longiflora) and a bunch (Sporobolus pyramidalis) grass species. In the field we found that soils with the highest micro nutrient levels (formed by Macrotermes) showed the largest increase in cover of grazing lawn species. By linking the different nutrient availability of the mounds to the development of different grassland states, we conclude that the presence of termite mounds influences grassland mosaics, but that the type of mound plays a crucial role in determining the nature of the effects.     

Role of termites in the restoration of soils and plant richness on bowé in West Africa

Bowé (hardened ferricrete soils formed by erosion, drought or deforestation) are often associated with termite mounds, but little is known about these mounds and their role in the restoration of soils and plant biodiversity on bowé. This study examined termite mounds on bowé and their effects on soil depth and plant richness. Sixty-four sampling plots were laid out randomly on bowé sites with mounds and on adjacent bowé sites without mounds. The height and circumference of each mound were measured. Species inventories were made and soil depth measured in each plot. Linear mixed effects and generalised mixed effects models with Poisson error distribution were used to assess the variation in soil depth and plant species richness in mound and nonmound microsites. Two types of mounds (small vs. large) associated with different termite species were observed on bowé, with the small mounds being most common. Plots with either large or small mounds had deeper soils and higher plant richness than the adjacent plots without mounds. Conservation of termite mounds is important for restoring soils and plant richness on bowé, and termite mounds should be taken into consideration in biodiversity and soil management strategies for bowé.     

Nutrient dynamics and plant assemblages of Macrotermes falciger mounds in a savanna ecosystem

Termites through mound construction and foraging activities contribute significantly to carbon and nutrient fluxes in nutrient-poor savannas. Despite this recognition, studies on the influence of termite mounds on carbon and nitrogen dynamics in sub-tropical savannas are limited. In this regard, we examined soil nutrient concentrations, organic carbon and nitrogen mineralization in incubation experiments in mounds of Macrotermes falciger and surrounding soils of sub-tropical savanna, northeast Zimbabwe. We also addressed whether termite mounds altered the plant community and if effects were similar across functional groups i.e. grasses, forbs or woody plants. Mound soils had significantly higher silt and clay content, pH and concentrations of calcium (Ca), magnesium (Mg), potassium (K), organic carbon (C), ammonium (NH₄⁺) and nitrate (NO₃⁻) than surrounding soils, with marginal differences in phosphorus (P) and sodium (Na) between mounds and matrix soils. Nutrient enrichment increased by a factor ranging from 1.5 for C, 4.9 for Mg up to 10.3 for Ca. Although C mineralization, nitrification and nitrification fraction were similar between mounds and matrix soils, nitrogen mineralization was elevated on mounds relative to surrounding matrix soils. As a result, termite mounds supported unique plant communities rich and abundant in woody species but less diverse in grasses and forbs than the surrounding savanna matrix in response to mound-induced shifts in soil parameters specifically increased clay content, drainage and water availability, nutrient status and base cation (mainly Ca, Mg and Na) concentration. In conclusion, by altering soil properties such as texture, moisture content and nutrient status, termite mounds can alter the structure and composition of sub-tropical savanna plant communities, and these results are consistent with findings in other savanna systems suggesting that increase in soil clay content, nutrient status and associated changes in the plant community assemblage may be a general property of mound building termites.     

Geophagy by African ungulates: the case of the critically endangered giant sable antelope of Angola (Hippotragus niger variani)

The giant sable antelope (Hippotragus niger variani) is a critically endangered subspecies with a range restricted to a small area in the Angolan plateau. It is known to display geophagic behaviour, eating the soil of some Macrotermes termitaria. The aim of this study was to understand the importance of this behaviour for the giant sable and other ungulates sharing its range. We identified termite mounds used for geophagy based on local information confirmed by self‐triggering cameras. We collected and analysed soil samples of seven termitaria consumed by ungulates, the adjacent topsoil 50 m away from each, and seven control nonconsumed termitaria. Consumed termite mounds were richer in minerals than control mounds, and both were richer than the surrounding topsoil. Sodium levels showed the greatest contrasts and were about 20 times more abundant in consumed termitaria than in controls. The amount of sodium in background soil was extremely low (9.3 ppm), suggesting that this mineral is a limiting nutrient in the range of the giant sable. These results indicate that the observed geophagic habits may be driven by a need to compensate for a sodium deficiency. This situation should be considered in the planning of the species' conservation.     

Reduction of the resistome risk from cow slurry and manure microbiomes to soil and vegetable microbiomes

In cow farms, the interaction between animal and environmental microbiomes creates hotspots for antibiotic resistance dissemination. A shotgun metagenomic approach was used to survey the resistome risk in five dairy cow farms. To this purpose, 10 environmental compartments were sampled: 3 of them linked to productive cows (fresh slurry, stored slurry, slurry-amended pasture soil); 6 of them to non-productive heifers and dry cows (faeces, fresh manure, aged manure, aged manure-amended orchard soil, vegetables-lettuces and grazed soil); and, finally, unamended control soil. The resistome risk was assessed using MetaCompare, a computational pipeline which scores the resistome risk according to possible links between antibiotic resistance genes (ARGs), mobile genetic elements (MGEs) and human pathogens. The resistome risk decreased from slurry and manure microbiomes to soil and vegetable microbiomes. In total (sum of all the compartments), 18,157 ARGs were detected: 24% related to ansamycins, 21% to multidrugs, 14% to aminoglycosides, 12% to tetracyclines, 9% to β-lactams, and 9% to macrolide–lincosamide–streptogramin B. All but two of the MGE-associated ARGs were only found in the animal dejections (not in soil or vegetable samples). Several ARGs with potential as resistome risk markers (based on their presence in hubs of co-occurrence networks and high dissemination potential) were identified. As a precautionary principle, improved management of livestock dejections is necessary to minimize the risk of antibiotic resistance.     

A model of litter harvesting by the Western Australian wheatbelt termite,Drepanotermes tamminensis (Hill), with particular reference to nutrient dynamics

A series of papers have been published which describe the influence of vegetation and soil type on the Western Australian wheatbelt termite,Drepanotermes tamminensis (Hill), and also on its litter harvesting levels and contribution to the soil nutrient budget. This paper integrates these findings by means of a computer simulation model. The model consists of three modules which respectively describe the dynamics of litter on the ground, the dynamics of litter within termite mounds and how these in turn influence nutrient loads within the habitat. The outputs of the model suggest that this litter harvesting termite plays an important role in the nutrient dynamics of the area and it provides an estimate of the unmeasured variable, litter consumed in mounds by termites, which is consistent with measurements for other termite species with similar feeding habits.     

Soil microbial community analysis of between no-till and tillage in a controlled horticultural field

The present study evaluated the changes of soil microbial communities that were subjected to no-till and compared the results to those subject to tillage for organic farming in a controlled horticultural field by fatty acid methyl ester. Fungi (P < 0.001), gram-positive bacteria (P < 0.001), arbuscular mycorrhizal fungi (P < 0.01), and actinomycetes (P < 0.01) in the no-till soils were significantly larger than those in the tillage soils. The no-till in the subsoil had a significantly lower ratio of cy17:0 to 16:1ω7c compared to that of tillage, indicating that microbial stress decreased because the soils were not disturbed (P < 0.05). Fungi should be considered as a potential factor responsible for the obvious microbial community differentiation that was observed between the no-till and tillage areas in a controlled horticultural field.     

The Culturable Soil Antibiotic Resistome: A Community of Multi-Drug Resistant Bacteria

Understanding the soil bacterial resistome is essential to understanding the evolution and development of antibiotic resistance, and its spread between species and biomes. We have identified and characterized multi-drug resistance (MDR) mechanisms in the culturable soil antibiotic resistome and linked the resistance profiles to bacterial species. We isolated 412 antibiotic resistant bacteria from agricultural, urban and pristine soils. All isolates were multi-drug resistant, of which greater than 80% were resistant to 16–23 antibiotics, comprising almost all classes of antibiotic. The mobile resistance genes investigated, (ESBL, bla _NDM-1, and plasmid mediated quinolone resistance (PMQR) resistance genes) were not responsible for the respective resistance phenotypes nor were they present in the extracted soil DNA. Efflux was demonstrated to play an important role in MDR and many resistance phenotypes. Clinically relevant Burkholderia species are intrinsically resistant to ciprofloxacin but the soil Burkholderia species were not intrinsically resistant to ciprofloxacin. Using a phenotypic enzyme assay we identified the antibiotic specific inactivation of trimethoprim in 21 bacteria from different soils. The results of this study identified the importance of the efflux mechanism in the soil resistome and variations between the intrinsic resistance profiles of clinical and soil bacteria of the same family.     

Termite mounds differ in their importance for herbivores across savanna types,seasons and spatial scales

Herbivores do not forage uniformly across landscapes, but select for patches of higher nutrition and lower predation risk. Macrotermes mounds contain higher concentrations of soil nutrients and support grasses of higher nutritional value than the surrounding savanna matrix, attracting mammalian grazers that preferentially forage on termite mound vegetation. However, little is known about the spatial extent of such termite influence on grazing patterns and how it might differ in time and space. We measured grazing intensity in three African savanna types differing in rainfall and foliar nutrients and predicted that the functional importance of mounds for grazing herbivores would increase as the difference in foliar nutrient levels between mound and savanna matrix grasses increases and the mounds become more attractive. We expected this to occur in nutrient‐poor areas and during the dry season when savanna matrix grass nutrient levels are lower. Tuft use and grass N and P content were measured along transects away from termite mounds, enabling calculation of the spatial extent of termite influence on mammalian grazing. Using termite mound densities estimated from airborne light detection and ranging (LiDAR), we further upscaled field‐based results to determine the percentage of the landscape influenced by termite activity. Grasses in close proximity to termite mounds were preferentially grazed at all sites and in both seasons, but the strength of mound influence varied between savanna types and seasons. In the wet season, mounds had a relatively larger effect on grazers at the landscape scale in the nutrient‐poor, wetter savanna, whereas in the dry season the pattern was reversed with more of the landscape influenced at the nutrient‐rich, driest site. Our results reveal that termite mounds enhance the value of savanna landscapes for herbivores, but that their functional importance varies across savanna types and seasons.     

An assessment of soil bacterial community structure and physicochemistry in two microtopographic locations of a palustrine forested wetland

We studied redoximorphic features, field indicators and bacterial communities of soils in hummocks and hollows of a palustrine forested wetland in Virginia. We hypothesized that presence of hydric soils, soil physicochemistry and soil bacterial community structure would differ between hummocks and hollows. We fingerprinted soils collected from different microtopographic locations using Length Heterogeneity Polymerase Chain Reaction (LH-PCR) to study their bacterial community structures. Two hummocks had silty/sandy loam soils with mean chroma values of > 4, showing no indication of ‘hydric soils’ (i.e., wetland soils). Two hollows, however, had clay loam soils with mean chroma values of 2 with gleying and redox concentrations observed, indicative of seasonally inundated wetlands. The soils of hollows also had higher organic matter content and soil moisture compared to the soils of hummocks (P < 0.05). Multidimensional scaling (MDS) and Analysis of similarity (ANOSIM) of the fingerprints revealed differences in soil microbial community structures between hummocks and hollows (Global R = 0.30, P < 0.01). The diversity measures of the fingerprints (Shannon’s H′) were also different by microtopography with higher diversity in hollows relative to hummocks (P < 0.05). LH-PCR proves to be a useful tool in examining bacterial community composition of wetland soils in this study. However, cloning and sequencing of specific community LH-PCR profiles of interest is necessary to fully characterize the community down to genus/species level. With species identities we should be able to not only better explain differences observed in the community profiles, but study their relations to hydrologic and/or physicochemical conditions of wetlands.     

Mulga log mounds: Fertile patches in the semi-arid woodlands of eastern Australia

In the semi-arid woodland of eastern Australia, soil mounds are often associated with fallen mulga (Acacia aneura) trees. Measurements of the physical and chemical properties of the soils in these mounds compared with surrounding soils, together with differences in herbage growth responses, indicate that these mounds are fertile patches, with possible importance as habitats for soil fauna and as refugia for a range of organisms during drought. The mound soil material may accumulate by fluvial, aeolian or rain-splash deposition about the fallen log, however, some of the mound material was derived from termite feeding gallery structures. The surface feeding gallery material may be comprised of soil particles from within the mound or from tunnels and storage galleries below the mound, and probably depends on the termite species.     

Termite mounds as browsing hotspots: an exception to the rule

In African savannas, termite mounds usually serve as browsing hotspots for mammals because of their soil fertility. Van der Plas et al., in this issue, describe that browsers avoid the unpalatable, evergreen tree species on mounds of Macrotermes natalensis in a mesic savanna, preferring mainly leguminous species with high leaf N and P concentrations in the matrix. This exception is probably a consequence of the fertile soils of the study area, and highlights the importance of environmental context for assessing ecological interactions.     

Abundance of Antibiotic Resistance Genes in Bacteriophage following Soil Fertilization with Dairy Manure or Municipal Biosolids,and Evidence for Potential Transduction

Animal manures and municipal biosolids recycled onto crop production land carry antibiotic-resistant bacteria that can influence the antibiotic resistome of agricultural soils, but little is known about the contribution of bacteriophage to the dissemination of antibiotic resistance genes (ARGs) in this context. In this work, we quantified a set of ARGs in the bacterial and bacteriophage fractions of agricultural soil by quantitative PCR. All tested ARGs were present in both the bacterial and phage fractions. We demonstrate that fertilization of soil with dairy manure or human biosolids increases ARG abundance in the bacterial fraction but not the bacteriophage fraction and further show that pretreatment of dairy manure can impact ARG abundance in the bacterial fraction. Finally, we show that purified bacteriophage can confer increased antibiotic resistance to soil bacteria when combined with selective pressure. The results indicate that soilborne bacteriophage represents a substantial reservoir of antibiotic resistance and that bacteriophage could play a significant role in the horizontal transfer of resistance genes in the context of an agricultural soil microbiome. Overall, our work reinforces the advisability of composting or digesting fecal material prior to field application and suggests that application of some antibiotics at subclinical concentrations can promote bacteriophage-mediated horizontal transfer of ARGs in agricultural soil microbiomes.     

Comprehensive analysis of autophagy‐related prognostic genes in breast cancer

Accumulating evidence revealed that autophagy played vital roles in breast cancer (BC) progression. Thus, the aim of this study was to investigate the prognostic value of autophagy‐related genes (ARGs) and develop a ARG‐based model to evaluate 5‐year overall survival (OS) in BC patients. We acquired ARG expression profiling in a large BC cohort (N = 1007) from The Cancer Genome Atlas (TCGA) database. The correlation between ARGs and OS was confirmed by the LASSO and Cox regression analyses. A predictive model was established based on independent prognostic variables. Thus, time‐dependent receiver operating curve (ROC), calibration plot, decision curve and subgroup analysis were conducted to determine the predictive performance of ARG‐based model. Four ARGs (ATG4A, IFNG, NRG1 and SERPINA1) were identified using the LASSO and multivariate Cox regression analyses. A ARG‐based model was constructed based on the four ARGs and two clinicopathological risk factors (age and TNM stage), dividing patients into high‐risk and low‐risk groups. The 5‐year OS of patients in the low‐risk group was higher than that in the high‐risk group (P < 0.0001). Time‐dependent ROC at 5 years indicated that the four ARG–based tool had better prognostic accuracy than TNM stage in the training cohort (AUC: 0.731 vs 0.640, P < 0.01) and validation cohort (AUC: 0.804 vs 0.671, P < 0.01). The mutation frequencies of the four ARGs (ATG4A, IFNG, NRG1 and SERPINA1) were 0.9%, 2.8%, 8% and 1.3%, respectively. We built and verified a novel four ARG–based nomogram, a credible approach to predict 5‐year OS in BC, which can assist oncologists in determining effective therapeutic strategies.     

Effects of exotic guava (Psidium guajava L.) invasion on soil properties in Limpopo,South Africa

Many studies in South Africa have examined the impacts of alien plants on ecosystems, but none have assessed the impact of guava (Psidium guajava L.) invasion on soil properties. In this study, soils underneath guava-invaded sites were assessed to determine if they had different soil physico-chemical properties (pH, P, C, N, Na, K, Ca, Mg, moisture, penetration resistance, infiltration and water repellency) as compared to soils underneath uninvaded sites. Comparisons were made from three different sites over three autumn months. Results show that soil pH was significantly (p < 0.005) higher underneath uninvaded than guava-invaded sites. Soil P was three times higher underneath guava-invaded as compared to invaded sites. The soils collected underneath guava-invaded sites had a significantly (p < 0.001) higher moisture content and were less compact but more repellent than soils from the uninvaded sites. Infiltration rate was significantly (p < 0.001) higher in the uninvaded than the guava-invaded sites. The study concludes that guava invasion alters some soil properties, thus creating favourable conditions for its growth and making it potentially more invasive. From a management standpoint, guava removal is encouraged; however, given guava's socio-economic importance more research on cost and benefits is required.