Use of RAPD markers for the study of microbial community similarity from termite mounds and tropical soils

In this study, we test the use of the RAPD (Random Amplified Polymorphic DNA) molecular markers as a way to estimate the similarity of the microbial communities in various termite mounds and soils. In tropical ecosystems, termite activities induce changes in the chemical and physical properties of soil. The question then arises as to whether or not termites affect the presence of natural microbial communities. Successful 16S rDNA amplifications provided evidence of the occurrence of bacterial DNA in termite constructions including both soil feeder and fungus grower materials. A phenetic dendrogram using the similarity distance calculated from pairwise data including 88 polymorphic RAPD markers was reconstructed and bootstrap scores mapped. The microbial communities of the mounds of the four soil-feeding termites were clustered in the same clade, while those of the mounds of the fungus-growing species were distinct like those of control soils. Microbial changes in nests result from termite building behavior, depending on whether they include feces in their constructions for soil-feeders or use saliva as particle cement for fungus-growers. It is argued that RAPDs are useful markers to detect differences in microbial community structure not only between termitaries and control soils but also between mounds of soil-feeders.     

Chemical,physical and micromorphological properties of termite mounds and adjacent soils along a toposequence in Zona da Mata,Minas Gerais State,Brazil

Little is known about the effects of neotropical mound-building termites in soil chemical and physical properties. The influence of soil termite activity on soil characteristics was studied by assessing chemical, physical and micromorphological properties of a toposequence of Latosols (Oxisols). Soil samples were collected from the walls and inner parts of termite mounds and also from adjacent soil. A high diversity of termite genera was found in the mounds along the toposequence, together with the inquiline termites and other soil-dwelling arthropods. Chemical analyses showed that pH and the contents of organic C and N, P, Ca and Mg were significantly higher in termite mounds compared with adjacent areas, with an inverse trend for Al content. Significant differences in pH and exchangeable Al were observed between soil and mound across the slopes. The mound density across the landscape was higher at the upper slope segment, followed by the hill top, middle slope and lower slope segments. Considering a lifespan of 30 years and dimensions of termite mounds found in the toposequence we conclude that the textural and chemical uniformity of Latosols may be increased, following the pedobiological turnover during mound building, with local rates varying from 2.1 to 7.5 m³ ha^− 1.     

Effects of termites on the physical and chemical properties of the acid sandy soils of southern Nigeria

Abstract

This study was aimed at characterizing the effects of the activity of termites of the genus Nasutitermes on the physico‐chemical properties of the acid sandy soils of southern Nigeria. Selected morphological properties of the termite mounds were measured in the field. Outside portions of the termite mound and surface (0–15 cm) soil were collected and analyzed for some physical and chemical properties. Results obtained showed a density of 112 mounds ha^‐1 with average height of 0.85 m. There were significantly higher proportions of clay, silt, and organic carbon, and higher pH, exchangeable potassium (K), calcium (Ca), magnesium (Mg), available phosphorus (P), effective cation exchange capacity and base saturation in the mounds of the Nasutitermes than in the surrounding topsoil. Mounds of Nasutitermes termites, if returned to the soil, could improve the properties of the soil in areas where termites occur in large numbers.     

Incidence of fungus-growing termites (Isoptera, Macrotermitinae) on the structure of soil microbial communities

The aim of this study was to investigate the impact of subterranean fungus-growing termites on the structure of soil microorganism communities. We tested whether termites significantly modify the abundance and structure of microbial communities within their below-ground nests (fungus-comb chambers) and whether these effects are species-specific.The investigations were carried out in a humid savanna reserve with material collected from the fungus-comb chamber walls of two widespread species differing in the mode of nest construction. Ancistrotermes builds diffuse and ephemeral nests while chambers of Odontotermes are mostly concentrated and occupy the same area for a comparatively much longer period of time then creating lenticular mounds. The soil properties (pH, texture and C, N content) and the microbial biomass were analysed and automated rRNA intergenic spacer analysis (ARISA) was used to characterise bacterial (B-ARISA) and fungal (F-ARISA) communities. Our results illustrate that the nest structures created by termites offer a diverse range of physical and chemical environments that differ strongly from those present in the general soil mass. Odontotermes had strong effects on microbial properties at the scale of the fungus-comb chamber and at the scale of the lenticular mound. In the fungus-comb chambers, the microbial biomass is not affected by termites but the structure of microbial community is different from that in the control open savanna soil. In the lenticular mound, the microbial biomass is higher and the structure of bacterial community is distinct than that in the fungus-comb chambers. Ancistrotermes also strongly influenced the structure of soil bacterial and fungal communities in the open savanna. However, we did not find any significant modification of bacterial and fungal community structures in the lenticular mound. The impact of fungus-growing termites is, therefore, species-specific and varies depending on the study site (open savanna vs. lenticular mound).     

Transformation and mineralization of 14C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termite Cubitermes orthognathus

 We performed feeding trials with the soil-feeding termite Cubitermes orthognathus using soil spiked by uniformly ¹⁴C-labeled preparations of cellulose, peptidoglycan, protein, and bacterial cells (Bacillus megaterium and Escherichia coli). When incubated in soil for 8 days in the absence of termites, cellulose and peptidoglycan showed low mineralization rates (0.5% and 0.2%, respectively). However, when termites were present, their mineralization rates strongly increased (21.6% and 30.6%, respectively). The mineralization rate of protein was 12.4% in the control soils and increased to 36.2% in the presence of termites. Mineralization of bacterial cells in control soils occurred in two phases (rapid mineralization during the first 4–5 days and stabilization thereafter). When termites were present, the rates of mineralization of bacterial cells increased and the stabilization phase was abolished. In all cases, radiolabel accumulated in the termites and the solubility of the labeled compounds located in the gut increased strongly. Mineralization was accompanied by transformation of residual carbon from the humic acid fraction to the fulvic acid fraction during gut passage. High-performance gel permeation chromatography demonstrated a strong shift in the size distribution of the residual carbon from high-molecular-weight towards low-molecular-weight molecules in the gut of termites and an accumulation of small molecules in the termite bodies. The present study provides strong evidence that structural polysaccharides of plants and bacteria and microbial biomass are carbon and energy sources for soil-feeding termites. Received: 29 May 2000     

Impact of subterranean fungus-growing termites (Isoptera, Macrotermitiane) on chosen soil properties in a West African savanna

Fungus-growing termites (Isoptera, Macrotermitinae) play an important role in tropical ecosystems in modifying soil physical properties. Most of the literature regarding the impact of termites on soil properties refers to termite epigeous mounds. In spite of their abundance and activity in African savannas, few studies deal with the properties of underground nest structures (fungus-comb chambers) built by subterranean Macrotermitinae termites. We tested whether these termites significantly modify the soil physico-chemical properties within their nests in a humid tropical savanna and whether these effects are different for two termite species with differing building behaviour. Termite-worked soil material was collected from fungus-comb chamber walls of two widespread species: Ancistrotermes cavithorax, which builds diffuse and ephemeral nests and Odontotermes nr pauperans, which most often builds concentrated and permanent nests for a comparatively much longer period of time. Neither species influenced soil pH but both significantly modified soil texture and C-N content in their nest structures. A strong impact on clay-particle size was also detected but no significant differences in clay mineralogy. Thus Odontotermes has a greater effect on soil properties, that could be explained by its building behaviour and the concentration in space of its nest units. Therefore, spatial pattern and life-span of fungus-comb chambers should be an important parameter to be considered in the functional role of subterranean Macrotermitinae termites in the savanna.     

埃塞俄比亚罗毕高原含铬雏形土地区凋落物饲喂的白蚁(Macrotermes spp)的化学性质及其生化活动的研究

Termite(Macrotermes spp.) mounds are complex biological habitats originated by the termite activity and possessing peculiar physical, chemical and biochemical properties. In this study we examined the concentration of nutrients and the biochemical activity of abandoned soil and mounds colonized by termites of the genera Macrotermes located in the Borana District, Ethiopia. To elucidate the magnitude and persistence of the termite-induced effects, we also studied an abandoned mound, previously colonized by termites of the same genera formed on the same soil. Results confirmed that termite-colonized mounds are ‘hot spots' of nutrient concentration and microbial activity in tropical soils. This is due to the termite driven litter input and decomposition. The abandoned mounds showed higher microbial biomass and activity and displayed a nutrient redistribution and a greater microbial activity than the adjacent soils. These findings allowed us to hypothesize a model of nutrient cycling in colonized soils and a partition of the relative roles of termites and soil microorganisms in nutrient location and turnover in tropical soils. These results may be also useful for the optimal management of termite-colonized soils.     

C and N concentrations in biogenic structures of a soil-feeding termite and a fungus-growing ant in the Colombian savannas

Soil ecosystem engineers such as termites and ants are able to modify physico-chemically the surrounding environment through the production of biogenic structures, thus affecting the availability of trophic and spatial resources for other organisms. The aim of this study was to assess the concentrations of C_org, NH₄⁺ and NO₃⁻ in the biogenic structures produced by a soil-feeding termite (Spinitermes sp.; Termitinae) and a fungus-grower ant species (Atta laevigata; Myrmicinae; tribe Attini) and the surrounding soil in the Colombian “Llanos”. We tested the hypothesis that higher concentrations occur in the biogenic structures compared to control soil and that deposition of new building material at the top of the biogenic structures also increases nutrient concentrations. Sampling was conducted along a transect, at regular intervals proportional to the size of the biogenic structure. Average C_org and NH₄⁺ concentrations were significantly higher in termite mounds than in ant nests and the control soil, whereas NO₃⁻ concentrations were similar. For both types of biogenic structures, the highest difference in nutrient concentrations was found between the top centre of the biogenic structure and the control soil, but significant differences were only reported for Spinitermes mounds and the control soil. No significant effect of land use on nutrient concentrations in the biogenic structures produced by either species was observed. We conclude that the activities of soil ecosystem engineers contribute to the variability of nutrient concentrations through the formation of biogenic structures.     

Impact of a soil feeding termite,<Emphasis Type="Italic"> Cubitermes niokoloensis</Emphasis>, on the symbiotic microflora associated with a fallow leguminous plant<Emphasis Type="Italic"> Crotalaria ochroleuca</Emphasis>

The influence of a soil-feeding termite nest (Cubitermes nikoloensis) on the development of a symbiotic microflora (rhizobia, arbuscular mycorrhizas) was tested in a pot experiment with a tropical legume (Crotalaria ochroleuca). Our results confirmed the role of soil-feeding termite nests as sites of high nutrient concentration, as a significantly higher content of available P and mineral-N was found in the mound wall. Arbuscular mycorrhizal spores increased in the soil near the termite mound. The mound soil itself almost totally depressed mycorrhizal establishment. The positive effect of the soils close to the mound was also evidenced by the number of nodules per root system as well as the nodule biomass per legume plant grown on this medium. Better growth of Crotalaria seedlings was observed in the soils from the mound wall; the shoot biomass increased by a factor of 9 and the root biomass by a factor of 6 as compared to the control soil (10 m away from the mound). Plant growth on soils from the immediate vicinity of the mound showed intermediate results but a higher N content per biomass unit. This probably reflected the association with arbuscular mycorrhiza and rhizobia. This work evidenced the linkage of plant nutrition to nutrient availability in mound material and the indirect mediating effect of the symbiotic microflora.     

Some effects of mound-building termites on the soils of a semi-arid area of Kenya

The nutrient status of soils from Macrotermes termite mounds, in and around Kajiado District, reflects that of the subsoils more closely than in some other studies, notably Watson (1977). Consequently the growth of vegetation on and around mounds was not noticeably enhanced, except in grasslands and in higher rainfall areas. There was no evidence that mounds acted as wicks. Mound soils contained greater concentrations of calcium, magnesium and potassium than subsoils in almost all cases where subsoil values were low, suggesting that the termites’ activities enhanced the nutrient status of mound soils. The nutrients were probably derived from their food, and the effects increased in some cases by their selection of clay on clay-poor soils. Nevertheless, the overall effects of Macrotermes on rangeland soils are probably small. The distribution of Macrotermes is remarkably unaffected by soil types; they construct mounds on almost all soils except those consisting largely of montmorillonite.     

The physical and chemical composition of mounds of Macrotermes carbonarius (Hagen) (Termitidae, Macrotermitinae), in Penang, Malaysia

The mound of the fungus-growing termite Macrotermes carbonarius (Hagen) contained significantly larger proportions of clay (P<0.05) than the adjacent soil. The largest clay content was found in the brood chamber. Concentrations of organic carbon, nitrogen, potassium and calcium in various parts of the mound were enriched compared to the adjacent soil at 10–40 cm depth from which they might have been derived. The activities of M. carbonarius did not significantly alter the pH or the bulk density of the mound soil compared to the adjacent topsoil.     

Effects of Ant Mounds on the Plant and Soil Microbial Community in an Alpine Meadow of Qinghai–Tibet Plateau

Ants are important soil engineers, affecting the structure and function of ecosystems. To address the impacts of ants (Camponotus herculeanus ) on the properties of an alpine meadow ecosystem of Qinghai–Tibet Plateau, we investigated the effects of ant mounds on plant biomass, soil physicochemical properties, microbial diversity, and functions. We found that the total biomass of plant community was significantly greater in ant mound periphery. Plant species richness in ant mounds was reduced compared with that of control plots without ant mounds. Significant changes in physicochemical properties of soil were also observed. Soil organic matter, total nitrogen, available phosphorous, total potassium, and available potassium increased in ant mound soil due to the excavation activities by ants as well as the accumulation of organic matter and other nutrients during mound construction. For example, roots/soil contents (g/g) and soil moisture in ant mound soils were lower than those in controls. Microbial community composition and microbial biomass were clearly changed in ant mound soils. BIOLOG analysis further indicated that the functional diversity of the microbial community of ant mound soil increased and differed from that of controls. This study indicates that ant‐induced modification of soil properties indirectly influences plant biomass and species composition, and ant mounds have different microbial communities from those of control soil. Copyright © 2016 John Wiley & Sons, Ltd.     

Nutrient storage in termite (Macrotermes bellicosus) mounds and the implications for nutrient dynamics in a tropical savanna Ultisol

The role of mounds of the fungus-growing termite Macrotermes bellicosus (Smeathman) in nutrient recycling in a highly weathered and nutrient-depleted tropical red earth (Ultisol) of the Nigerian savanna was examined by measuring stored amounts of selected nutrients and estimating their rates of turnover via the mounds. A study plot (4?ha) with a representative termite population density (1.5?mounds?ha^?1) and size (3.7?±?0.4?m in height, 2.4?±?0.2?m in basal diameter) of M. bellicosus mounds was selected. The mounds were found to contain soil mass of 9249?±?2371?kg?ha^?1, composed of 7502?±?1934?kg?ha^?1 of mound wall and 1747?±?440?kg?ha^?1 of nest body. Significant nutrient enrichment, compared to the neighboring topmost soil (Ap1 horizon: 0–16?cm), was observed in the nest body for total nitrogen (N) and exchangeable calcium (Ca), magnesium (Mg) and potassium (K), and in the mound wall for exchangeable K only. In contrast, available (Bray-1) phosphorus (P) content was found to be lower in both the mound wall and the nest body than in the adjacent topmost soil horizon. Consequently, the mounds formed by M. bellicosus contained 1.71?±?0.62?kg?ha^?1 of total N, 0.004?±?0.003?kg?ha^?1 of available P, 3.23?±?0.81?kg?ha^?1 of exchangeable Ca, 1.11?±?0.22?kg?ha^?1 of exchangeable Mg and 0.79?±?0.21?kg?ha^?1 of exchangeable K. However, with the exception of exchangeable K (1.2%), these nutrients amounted to less than 0.5% of those found in the topmost soil horizon. The soil nutrient turnover rate via M. bellicosus mounds was indeed limited, being estimated at 1.72?kg?ha^?1 for organic carbon (C), 0.15?kg?ha^?1 for total N, 0.0004?kg?ha^?1 for available P, 0.15?kg?ha^?1 for exchangeable Ca, 0.05?kg?ha^?1 for exchangeable Mg, and 0.06?kg?ha^?1 for exchangeable K per annum. These findings suggest that the mounds of M. bellicosus, while being enriched with some nutrients to create hot spots of soil nutrients in the vicinity of the mounds, are not a significant reservoir of soil nutrients and are therefore of minor importance for nutrient cycling at the ecosystem scale in the tropical savanna.     

Termite hills in Africa: Their characteristics and evolution

Small dome-shaped hills are recurrent and common landforms associated with plateau surfaces in the savanna woodland landscapes, both to the north and south of the Congo Basin. They may be occupied in part by termite colonies or be moribund. Previous ideas on the relationships between termite hills and termite mounds are discussed. The evolution of the hills is discussed in the light of evidence from variious parts of Zambia. It is concluded that the interaction of mound building by termites and mound destruction by rain beat and rain wash is complicated by plant colonisation, interference and use by animals, the incidence of fire and the activities of agricultural man. These are also factors which might explain the distribution of termite hills. The apparent fossilisation of the termite hills through the development of thicket vegetation is not regarded as necessarily dependent on climate change but could be the result of other changing ecosystem factors.     

The impact of termite sheetings age on their fungal communities

In previous studies, we have shown that fungal communities in soil are quantitatively and qualitatively modified when termite sheetings are constructed, but the reasons for these changes are unknown. In this work we described the succession of fungal communities in the sheetings of three fungus-growing termite species by combining cultivation techniques and culture-independent methods specially DNA extraction, PCR and denaturing gradient gel electrophoresis (DGGE). We also estimated the abundance of fungi by using plate-count technique. The fungal communities of these sheetings were sampled at different ages. The potential functions of fungal communities was assessed by their capabilities of degrading different substrates including proteins, polysaccharides and tannins. Significant differences were found between the fungal communities of termite sheetings and those of surrounding soil. These differences were observed at quantitative, qualitative and functional level as well and were marked particularly in the fresh sheetings of termites. The characteristics of fungal communities of the surrounding soil were quite similar with those observed in the old sheetings of termites. These results show that the fungal communities are modified at once in freshly built sheetings, rather than by a progressive succession, as had been expected.     

Effect of different termite feeding groups on P sorption and P availability in African and South American savannas

Nest structures of six termite species, four with epigeous (above-ground) and two with subterranean nests were analysed to find out how their building and feeding habits could be related to their nests phosphorus status compared with control soils. Termite nest structure was found to affect significantly the P status in savanna soils: mounds of the African Trinervitermes geminatus and the South American Nasutitermes ephratae (both grass-feeders) displayed a greater amount of available P, especially in the inner part of the nest, than the surrounding soil. The abundant quantities of dead grass material stored in the mound can explain the available soil P increase. A similar increase in P availability was also found for the soil-feeder Cubitermes severus. In mounds of Macrotermes bellicosus, on the other hand, there was a drastic increase in P sorption (and a corresponding decrease in available P) compared to adjacent soils, which was attributed to the building strategy of this species. M. bellicosus selected clay from subsoil to build its nest structure. The data obtained for the subterranean species Ancistrotermes cavithorax and Microtermes toumodiensis indicated also that there is an increase in P sorption in mounds when compared with associated topsoils. Consequently, the nest structures of only certain termite species should be considered, and utilised, as a soil amendment in place of fertilisers. This impact on the P cycle in savannas seems to be related to the termite feeding status and to the type of material utilised in nest building. This should be taken into account before using termite nest material in soil fertility status improvement.     

Nutrient storage in soils and nests of mound-building <Emphasis Type="Italic">Trinervitermes</Emphasis> termites in Central Burkina Faso: consequences for soil fertility

Nest structures of two termite species (Trinervitermes spp.) with epigeal (above-ground) mounds were analyzed to compare their nutrient status with that of adjacent soils. To take into account soil variability, the observations and samplings were made in three toposequences of different and representative West African savanna soils. The data showed the high degree of adaptation of these termite species to a large range of soil types and environments. Mounds of Trinervitermes geminatus and Trinervitermes trinervius, both grass-feeders, contained more clay, organic matter (OM), and exchangeable cations than the surrounding surface layer soil. The storage of OM and exchangeable cations was determined for T. geminatus nests and compared to the surrounding soil. Despite substantial nutrient storage in mounds, its total weight appeared low when compared to the nutrient storage in the surrounding 0–15 cm of soil surface layer. This illustrates how contradictory points of view on the use of termite mounds in agriculture need to be clarified using a classical approach that takes into account data by species; and this also evaluates the contribution of different termite mounds to nutrient fluxes and storage and the exact stocking rate of living mounds.     

Diurnal and seasonal variations in CH4 flux from termite mounds in tropical savannas of the Northern Territory, Australia

Termites are estimated to contribute between <5 and 19% of the global methane (CH₄) emissions. These estimates have large uncertainties because of the limited number of field-based studies and species studied, as well as issues of diurnal and seasonal variations. We measured CH₄ fluxes from four common mound-building termite species (Microcerotermes nervosus, M. serratus, Tumulitermes pastinator and Amitermes darwini) diurnally and seasonally in tropical savannas in the Northern Territory, Australia. Our results showed that there were significant diel and seasonal variations of CH₄ emissions from termite mounds and we observed large species specific differences. On a diurnal basis, CH₄ fluxes were least at the coolest time of the day (∼07.00 h) and greatest at the warmest (∼15.00 h) for all species for both wet and dry seasons. We observed a strong and significant positive correlation between CH₄ flux and mound temperature for all species. A mound excavation experiment demonstrated that the positive temperature effect on CH₄ emissions was not related to termite movement in and out of a mound but probably a direct effect of temperature on methanogenesis in the termite gut. Fluxes in the wet season were 5-26-fold greater than those in the dry season. A multiple stepwise regression model including mound temperature and mound water content described 70-99% of the seasonal variations in CH₄ fluxes for different species. CH₄ fluxes from M. nervosus, which was the most abundant mound-building termite species at our sites, had significantly lower fluxes than the other three species measured. Our data demonstrate that CH₄ flux estimates could result in large under- or over-estimation of CH₄ emissions from termites if the diurnal, seasonal and species specific variations are not accounted for, especially when flux data are extrapolated to landscape scales.     

Abundance,perceptions and utilizations of termite mounds in Cambodia

In the Lower Mekong Basin, paddy fields often appear as mosaics, with soil mounds covered by trees or other plants in a spotty distribution. These soil mounds are commonly named termite ‘lenticular mounds’ because termite bioturbation is considered to be at their origin. Termite mounds host a large diversity of animals and plants, increasing landscape patchiness. Because the preservation of these islands of biodiversity is threatened by modern agricultural practices, the aim of this study was to quantify their abundance and the services they provide to the local population. The abundance of mounds and their use by the population were quantified in a catchment in Cambodia. We found that mounds density reached ~2 mounds ha⁻¹. Interviews carried out within the catchment showed that most of the interviewees used mounds for increasing the fertility of their field and for the cultivation of rice and other plants (e.g. sponge gourd and pumpkin). In addition to their potential to increase plant productivity, the survey revealed that animals (rats and snakes), mushrooms and 13 plant species found on or in mounds were consumed by the population. In addition to potentially contributing to an increase in food diversity, mounds also impacted farmers' health by allowing access to 20 medicinal plant species and indirectly via a reduction in pesticide use. In conclusion, this study is the first attempt to quantify the large number of services provided by termite mounds in Cambodia. This increase in the knowledge of the diversity of environmental and socioeconomic services provided by termite mounds is likely to contribute to their preservation and provide a basis for the sustainable management of biodiversity in paddy fields in the Lower Mekong Basin region.     

Impacts of termites on selected soil physicochemical characteristics in the highlands of Southwest Ethiopia

Termites are reported to improve soil physicochemical properties thereby enhance soil fertility of their mound and foraging areas. Empirical study pertaining to these effects is missing in Southwest Ethiopia. For this study, soil samples affected by termite activities were collected at 1 m interval within 0–3 m distance from the base of six termite mounds on gently sloping and sloping land and analyzed for physicochemical parameters. The result of the analysis depicted that soil bulk density (1.38–1.15 g cm^?3) and moisture content (21.1–9.9%) decreased with increased distance from the mound base. While clay content decreased with increased distance from the mound base from72.0% to 45.5%, sand and silt contents increased from 8.0% to 21.3% and 19.3% to 28.5%, respectively. PH (6.23), organic carbon (3.85%), total nitrogen (0.4%), cation exchange capacity CEC (30.43 cmol kg^?1), exchangeable Ca (13.73 cmol kg^?1), Mg (3.15 cmol kg^?1), and PBS (56.8%) were higher on termite mounds. While, electrical conductivity (0.03 dS m^?1–0.06 dS m^?1), exchangeable K (0.52–0.93 cmol kg^?1) and Na (0.02–0.03 cmol kg^?1) showed increasing trend with the distance from the mound base. Our results indicated that termite mounds are important sinks of organic matter and mineral nutrients, and hence contribute to the enhancement of soil fertility. Thus, for subsistent farmers the uses of termite mounds as a fertilizer present an opportunity to improve agricultural production.