Background

Anthropogenic processes for the treatment of biodegradable solid waste revolve round the use of aerobic, anaerobic, and facultative bacteria [1,2]. Be it a sanitary landfill, a composting system, a solid-feed anaerobic digester, or a bioprocess of some other kind, bacterial digestion has been central to the treatment of biodegradable solid wastes [3-7]. The only exception to this general rule has been vermicomposting wherein the action of bacteria and enzymes on solid waste is mediated (and controlled) by earthworms. The animal ingests solid waste along with soil and deposits the digested material in the form of seed-like vermicast. During the passage through the worm gut, the feed is acted upon by the gut microflora and gets significantly stabilized. The resulting vermicast is a good soil conditioner and fertiliser [8-13].

But neither vermicomposting nor direct bacterial action during any of the economically viable solid waste degradation processes can handle lignin ([4,5] a, b). ‘Hard’ biowastes such as coconut shells and woody biomass also defy swift biodegradation.

In an attempt to find a quicker and more widely applicable way to dispose large volumes of biowaste, especially the type of biowaste - mentioned above - which resists treatment methods currently in general use, we have begun exploring a new frontier: termigradation. This is one of the first reports, perhaps the first ever, on the use of termites in disposing solid waste. Termites are among the nature’s most powerful scavengers and earth movers, alongside earthworms and ants [14-16]. But unlike the other two, termites harbour in their midst microflora which have the special ability not possessed by other animals: ability to digest lignin [17]. In case of lower termites, ligneous material is masticated and ingested which is then digested by microflora present in certain species of protozoa living symbiotically in the termite gut [18,19]. In case of higher termites, the microflora capable of digesting lignin is present directly in the animal gut [18,19].

Other characteristics of termites which make them potential candidates for bioprocessing of solid waste are [20]: a) their voracious appetite; b) their ability to consume a wide variety of wastes; c) diversity of their habitat preference which makes it possible to always find one or other species suitable for a given geo-climatic situation [21-23]; d) their very fast rate of population growth; and e) good quality of protein represented by termite bodies, making them ideal as poultry feed or source of chemicals such as biofuel [24,20].

But any endeavour to develop bioreactors based on termites has to overcome a unique challenge. It lies in the fact that termites are ‘eu-social’ animals with well-defined and uncompromising social hierarchy [25]. Unlike earthworms, of which every single individual has the potential to reproduce sexually while it is feeding upon the waste in a bioreactor, the worker termites cannot breed. It is, therefore, not possible to inoculate a pile of waste with worker termites and expect that the workers would feed and breed till the entire waste is consumed. For any termireactor to function sustainably, it has to be ensured that the workers keep coming from termite nests where the workers are being born and reared continuously (along with, of course, other termites of higher caste viz soldiers). To achieve this objective, we have explored the concept of in situ termireactor wherein chambers containing the waste are placed near pre-existing termite mounds. The chambers have sufficient openings to allow access to termites but are otherwise closed from all sides.

Methods

Substrate

Different constituents of municipal solid waste (MSW) were assessed including cardboard, paper waste, pieces of jute and cotton, coconut shells, leaf litter, etc. Paper waste, tattered jute bags, pieces of cardboard, and coconut shells were collected from the piles of municipal solid waste generated at the residential quarters of the Pondicherry University campus. Scraps and pieces of wood were obtained from a saw mill. Fresh cow dung and paddy straw were collected from a cattle farm. Tissue paper rolls made out of recycled paper, and cosmetic grade cotton were purchased from the market.

Leaf litter from 13 different types of trees: asoka (Polyalthia longifolia), pencil tree (Acacia auriculiformis), coconut (Cocos nucifera), cashew (Anacardium occidentale), palm (Borassus flabellifer), guava (Psidium guajava), mango (Mangifera indica), teak (Tectona grandis), banyan (Ficus benghalensis), jack (Artocarpus heterophyllus), tamarind (Tamarindus indica), peepal (Ficus religiosa), and pungam (Pongamia pinnata) was assayed in the experiments. The litter was collected from below the tree canopies. After removing the debris and leaves of other species, dry weight of the leaf litter of each tree species was estimated by oven drying weighed samples at 105°C to constant weight.

In situ termireactors

To assess the consumption of different MSW constituents by termites, each constituent was kept in an in situ termireactor of rectangular shape, made up from 3-mm-thick aluminium sheets. Each of the termireactors was placed in a shallow pit (45 × 30 × 2 cm), dug by us in the ground, at a measured distance away from the termite mound. All termireactors had holes of 1 cm diameter at the sides and the bottom to allow termites to access the waste.

Assessment of termigradation

The termireactors were located in such a way that the minimum distance between any two reactors as well as the distance between the reactors and the mound was 30 cm. This setup helped to spatially demarcate one substrate from the other as well as to keep the distance travelled by the termites from the nest to the pit almost equal. In each of the termireactors, 100 g (fresh weight) of the substrate was placed. The equivalent dry weight of each substrate was concurrently determined by oven-drying a known mass to a constant weight at 105°C. The substrates were moistened with tap water, to the extent that the contents become damp but not soggy. To protect the substrates from rainfall, direct sunlight, and disturbance by other animals, the pits were covered with polythene sheets reinforced with aluminium mesh. The covers were removed once in 10 days, to assess the termite action, to maintain adequate moisture content and to see if any interference of other soil macro fauna like ants, was occurring. After 60 days, the substrate remaining unconsumed by the termites was carefully removed from the termireactors and air-dried. Care was taken to brush off any soil particles adhering to the surface of the residue. Then, the residue was oven dried at 105°C to constant weight.

Experiments were also conduced to see whether the termites go to the nearest available substrate or go further in search of more favoured substrate if the one available at shorter distance is less agreeable. Termireactors of the type identical to ones described above were set up at varying distances away from the mounds. The substrates were kept in the termireactors in such a way that different substrates were located at different distances from the mound. The first substrate was kept 1 ft away from the mound, the second 2 ft away and the third 3 ft away. In all, 14 different substrates were placed at distances progressively away from the mound. The farthest a substrate was placed was 14 ft away from the mound.

Results and discussion

The ‘termigradability’ of 25 different substrates studied by us, in terms of fraction of the substrate consumed (dry weight basis), is presented in Figure 1.

Figure 1
figure 1

Average consumption of quadruplicate samples of the substrates by the termites.

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The results (Figure 2) show that not only ligninous material but other tough-to-degrade substrates like cardboard were also consumed by termites (up to 41.65%). Moreover, substrates such as cotton waste and torn jute bags, which resist bioprocessing during composting or vermicomposting, were also successfully consumed by termites. The studies thus confirm the potential of termites in processing ligninous and other ‘hard’ substances which defy composting, vermicomposting, and other forms of bacterial action in conventional solid waste management systems. Of special significance is our finding that pernicious weeds, like ipomoea, can be termidegraded. This is a finding of high promise. It is also significant that termites were able to degrade about 40% of cardboard within 60 days because otherwise cardboard is resistant to biodegradation [26]. Indeed, due to their resistance to biodegradation, cardboard pieces are often used as bulking agents in composting/vermicomposting systems [27].

Figure 2
figure 2

Consumption of the substrates by termites in the distance-based experiment.

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Several species of white rot fungi (WRF) notably Phanerochaete chrysosporium, Ceriporiopsis subvermispora, Pycnoporus cinnabarinus, Fuscoporia ferrea, Trametes pubescens, T. multicolor, Coriolus versicolor, and Pleurotus sajar-caju are known to degrade lignin [28,29]. Attempts to utilize this ability in treating ligninous wastes have been made since long, with increasing intensity since early 1970s [30-34]; But the rate at which WRF acts is very very slow [35,32] and, due to this, not a single process has been developed till now which makes use of WRF in degrading lignin on a commercial scale [36]. The present work suggests that termites may be able to process lignin at rates that are faster than possible with WRF but further work is needed to get a confirmation of this indication.

Figure 2, which indicates how far will termites venture out from some substrates in preference to others, indicates that the two substrates most voraciously consumed - sawdust and wood scrap (Figure 1) - are also the ones to which termites will go even if they lie a little farther away than the other substrates.

The preceding discussion is based on the extent of substrate consumed and does not give any information on the quantity or the characteristics of termicast. The reason is that in contrast to vermicomposting - which happens to be the only pre-existing bioprocess used in pollution control that is mediated by a multi-cellular animal - 50% to 60% of the substrate is converted to vermicast, termites produce no ‘termicast’. This is because termites are extremely efficient utilizers of food due to the staggering diversity of the microflora present in their gut [37]. Up to 93% of the ingested food is assimilated by termites [38,39]. Very little of what termites ingest is excreted; the excreta are made up of organomineral aggregates which are carried away by the worker termites to line the termite nests [40,16]. As a result, no ‘termicast’ is obtained in the termireactors and the extent of substrate consumption is quantified on the basis of what is left off [10].

Moreover, whereas in a vermireactor, we can control the number of the feeders (adult earthworm) and can work out per capita vermicast production, per unit time, such assessments are not possible in termite-based systems - for reasons that have been explained in the paper (last para of the ‘Background’ section). Hence, the rate of disposal of the waste is assessed on the basis of the fraction consumed rather than on the basis of cast produced (as is done in vermireactors).

In summary, there is really no way to precisely determine how much of the ingested lignin is decomposed in the ‘termireactors’ but given the fact that termites leave little residue, it can be easily surmised that the bulk of the ligneous material that termites eat is converted to termite zoomass. Also, evidence of termite action is very stark in all these reactors while no other organisms are seen who could have contributed to the consumption.

Conclusions

The studies provide a fairly convincing ‘proof-of-concept’, and we are now aiming to translate these findings into practicable waste treatment systems. At present, attempts are underway to develop captive colonies of some of the termite species within the confines of laboratories so that they can be used in a controlled fashion to treat specific components, as well as unsorted forms, of municipal solid waste.

We hope that further work on this new frontier would lead to new technology which could have great potential in handling ‘difficult’ organic solid waste - including that which is generated in several industries.