Sustainable use of termite activity in agro-ecosystems with reference to earthworms. A review
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Sustainable agriculture and agro-ecology justify the need to study and understand the role played by ecological processes, and soil biodiversity in particular, in agro-ecosystem functioning. A large number of studies have focused on earthworms in temperate and humid tropical ecosystems and have demonstrated their importance for improving soil biological, physical, and chemical properties in agro-ecosystems. Their “success” is so essential that earthworms are widely considered key species and relevant indicators of soil health in temperate ecosystems. In arid and sub-arid ecosystems, the role of “soil engineer” is usually attributed to termites, and especially fungus-growing termites in Africa and Asia. However, despite this recognition, significant effort is spent eradicating them in plantations because of their pest status. In this review, we discuss the status of termites (“pests” vs. “soil engineers”) and question whether termites play similar roles to earthworms in arid- and sub-arid agroecosystems, with a focus on their influence on nutrient cycling and water dynamics. We argue that the dream of controlling natural interactions and ridding plantations of termites remains a costly legacy of the green revolution. We review the agricultural practices that have been used to reduce termite damage in plantations by restoring refuges to predators or by reorienting termite foraging activity towards organic amendments. Then, we show that the stimulation of termite activity can be used to improve key ecological functions in agro-ecosystems, such as increasing water availability to plants or producing fertility hot-spots. Finally, we suggest that more research on how termites can be used for improving ecosystem services, as is actually done with earthworms in temperate and humid tropical countries, could lead to a paradigm shift in our understanding of the impact of termites in tropical agro-ecosytems.
KeywordsAgro-ecology Sustainability Dryland Heterogeneity Pests Ecosystem services Ecosystem disservices
The green revolution in the 1940s and blue revolution in the 2000s, which led to the intensive use of fertilizers, pesticides, irrigation, and high-yield crop varieties, have undoubtedly increased crop production and reduced the number of chronically undernourished people. Unfortunately, these gains in production have come at high environmental costs with the degradation and over-exploitation of terrestrial and aquatic ecosystems, hence threatening their sustainability and the services they provide to society (Tilman et al. 2002). It is in this context that the concepts of sustainable agriculture and agro-ecology have emerged as paradigm shifts, justifying the need to study and understand the roles played by ecological processes, and soil biodiversity in particular, in (agro)ecosystem functioning (Altieri 1995, 2002; Tilman et al. 2002; Wezel et al. 2009; Wilkinson et al. 2009).
The aim of this article is to review the value of termites (“pests” vs. “key decomposers and soil engineers”) in the context of sustainable development and agro-ecology concepts. We discuss the use of termite bioturbation to improve agro-ecosystem services, as is actually done with earthworms, and thus “ask whether termites have the right” to request a similar status to that of earthworms in arid and sub-arid tropical ecosystems.
2 Termites as pests
2.1 Damage resulting from termite activity
2.2 Why do termites become pests?
Agricultural practices that lead to termites becoming pests in agro-ecosystems
Mechanism leading to termites gaining pest status
Deforestation and overgrazing
Reduction in food (less litter, lower diversity) leading to a reduction in termite diversity, lower inter-specific competition, and proliferation of resistant or invasive species
Ecosystem simplification and hunting
Less predators (arthropods, mainly ants, and mega-fauna such as bears, aardvark, pangolins, chimpanzees) leading to a lower control of termite populations
Plants are less resistant
3 Termites as key decomposers and engineers in agro-ecosystems
Statements from soil ecologists such as “although termites pose potentially negative effects, their positive effects may be the overriding factors” are common (Lamoureux and O’Kane 2012). Hence, an abundant literature presents termites as ecosystem services providers. In agro-ecosystems, termites have an impact on three major ecological functions: (i) litter decomposition and nutrient recycling, (ii) water dynamics in soil, and (iii) ecosystem complexity and the distribution of nutrients at the landscape scale.
3.1 Influence of termites on C and nutrient cycling
In agro-ecosystems, termites can feed on plant material and/or soil humus and they are of the greatest importance in recycling C and nutrients from wood, other plant materials, and herbivore dung (e.g., Yamada et al. 2005a, b; Freymann et al. 2008; Noble et al. 2009; Veldhuis et al. 2017). If their impact on litter decomposition can be considered positive in fire-prone ecosystems where C and nutrients can be lost by fire (Konaté et al. 2003), termite foraging activity appears as a drawback when C and nutrients from the litter could have participated in the formation of humus without the action of termites (Potineni 1986). This is typically observed in dry tropical forests where most of the aboveground litter can be consumed by termites before it enters the soil layer (Yamada et al. 2005a). This is also true in agro-ecosystems where organic amendments (e.g., mulch, farmyard manure, or compost) are consumed by litter-feeder termites before being incorporated into the soil. In this case, nutrients become temporarily immobilized in the termite biomass and their symbiotic fungus (in the case of the fungus-growing termite species), thus limiting the positive outcomes of conservation farming practices in terms of soil chemical fertility and C sequestration (Potineni 1986). Organic matter can also be temporarily incorporated in termite sheetings and mounds. However, the low stability of termite-worked soil aggregates (Jouquet et al. 2004b, 2015a) suggests a rapid mineralization of this soil organic matter pool but a non-significant impact on nitrate and phosphate contents in soil (Harit et al. 2017). Since termites prefer some organic substrates to others, low palatable organic matter (e.g., compost) can be preferred to fresh residues (e.g., manure or straw) if the aims are to reduce the exportation of C from the field by termites and to increase the C content of soils. Finally, although less abundant in agro-ecosystems, the impact of soil-feeding termites on C sequestration and nutrient dynamics can also be considered as a drawback when they consume the C stock and nutrients from soil, thus hampering C sequestration in soils (Dahlsjö et al. 2014) (e.g., the 4p1000 initiative, see: http://4p1000.org/ and Minasny et al. 2017).
3.2 Influence of termites on soil water dynamics
The beneficial impact of termites on water dynamics in soil appears to be more important than their impact on nutrient cycling at the field scale (Kaiser et al. 2017). Indeed, termite foraging activity is often associated with the production of belowground galleries which increase soil macroporosity, create “preferential flow paths” and increase water infiltration in soil (Elkins et al. 1986; Mando et al. 1996, 1999; Mando and Miedema 1997; Léonard et al. 2001, 2004; Evans et al. 2011; Kaiser et al. 2017). The influence of termites on water infiltration is obviously influenced by the number of tunnels, their depths, size, etc. On average, it is considered that termites increase water infiltration above the natural rate by a factor of 1 to 4, depending on termite activity, soil type, and rainfall intensity (Lamoureux and O’Kane 2012; Kaiser et al. 2017). However, this effect is only significant in soils with low hydraulic conductivity. In the Chihuahuan desert, USA, termite foraging activity increases water infiltration from 51.3 to 88.4 mm h−1 (Elkins et al. 1986). However, to be significant at the plot scale, a large number of foraging holes is sometimes needed (e.g., > 30 m−2 in Sub-Sahelian ecosystems, Léonard and Rajot 2001). Termite foraging activity can be associated with the production of large amounts of sheetings which are usually enriched in clay, silt, and organic matter compared to the surrounding top-soil (Harit et al. 2017). Especially in compacted and gravelly soils in semi-arid regions, sheetings can locally improve soil physical and chemical properties. On the other hand, in sloping land in a humid tropical climate, Jouquet et al. (2012) observed that sheeting degradation might also be related to crust formation, higher water runoff, and soil detachment.
3.3 Influence of termites on ecosystem complexity
At the landscape scale, termites also act as heterogeneity drivers when they produce aboveground mounds that appear like nutrient “hot-spots” or “fertility islands” in which primary productivity is locally increased and water flow improved. Although termite mounds usually represent a small proportion of the landscape, they might constitute a mosaic of comparatively more productive areas in an ecosystem (e.g., Lamoureux and O’Kane 2012). In contrast to the surrounding savanna soil, these constructions are usually enriched in cations (magnesium, potassium, calcium…) and clay (Arshad 1981; Coventry et al. 1988; Mills et al. 2009; Jouquet et al. 2004a, 2015b; Brossard et al. 2007; Lopez-Hernandez et al. 2004; Sileshi et al. 2010; Seymour et al. 2014). Depending on the feeding group (e.g., soil feeding termites vs. fungus-growers) and the pedoclimatic properties of the environment, these mounds can also have higher C and N contents compared to the surrounding soil. The higher clay content along with the higher proportion of swelling clay in termite mounds also explain their higher water retention (Konaté et al. 1999). As shown in African savanna ecosystems, these aboveground constructions also provide refuges for plants and soil biodiversity, offer a better resistance of plants to fire, represent foraging hot-spots for herbivores, and increase the robustness of dryland ecosystems to climatic change (Mobaek et al. 2005; Traoré et al. 2008, 2015; Choosai et al. 2009; Moe et al. 2009; Brody et al. 2010; Erpenbach et al. 2013, Erpenbach et al. 2017; Davies et al. 2014, 2016; Seymour et al. 2014; Tobella et al. 2014; Bonachela et al. 2015).
4 Towards the sustainable application of termite activity in agro-ecosystems
Two main types of agricultural practices have been proposed for improving the services termites provide in agro-ecosytems while reducing their negative impacts. The first focuses on the provision of refuges for predators, which control termite populations, and of food for stimulating termite foraging activity and improving soil properties. The second relies on taking advantage of the heterogeneity created by termites at the landscape scale.
4.1 Less intensive agricultural practices providing litter, predators, and pathogens
Reduced food availability (litter) and the loss of termites’ natural predators (e.g., ants, bears, aardvark, pangolins), parasites, and pathogens (e.g., nematodes, fungi) are reported to be among the major factors explaining why termites are destructive in grasslands and for crops (Snyder 1929; Mugerwa 2015a, b). Hence, one promising strategy is the development of practices that provide other food besides crops for termites and which stimulate predators and/or entomopathogens for controlling termite populations. For example, studies carried out in Africa and Asia showed that termite infestation and crop damage could be reduced by inter-cropping with legumes, mulching in crop plantations, or by keeping leaf litter on the ground in tree plantations (Pong 1974; Sands 1977; Shivashankar et al. 1991; Sekamatte et al. 2001, 2003; Girma et al. 2009; Kihara et al. 2015). Less damage to crops and tree attacks result from ants nesting and feeding on termites (e.g., Leptogenys processionalis in India, which live in temporary nests and always forage under low-intensity sunlight conditions (Rajagopal and Ali 1984); or Pheidole megacephala and Megaponera foetens in Africa (Sheppe 1970; Longhurst et al. 1978; Lepage 1981)), as well as the fact that termites prefer feeding on mulch and litter, a more palatable food resource for termites than crops and trees (Shivashankar et al. 1991; Mugerwa 2015a, b). The above examples are important because they show that termite attacks on crops and trees can be reduced to a level acceptable for farmers if termite populations are limited (but not eradicated) by stimulating predators or entomopathogens, such as fungi, ants, spiders, beetles and lizards, and/or if more palatable food is given to them (mulch and litter in these cases). Interestingly, several studies also showed that the application of mulch or different organic amendments (e.g., cattle or goat dung, urine, or a mixture) increases termite foraging activity which in turn enhances soil porosity, water infiltration, and water holding capacity in soil (Mando et al. 1996, 1999; Roose et al. 1999; Léonard and Rajot 2001; Dawes 2010; Kaiser et al. 2017), while reducing termite damage on crops (Mugerwa 2015a, b), and increasing plant growth and yield. For example, in the case of the agricultural and forestry Zaï systems, the application of organic matter into the soil triggers termite activity which then create burrows through the crusted soil surface, thus improving the productivity of the ecosystems from 0.5 to 5.3 tons ha−1 for straw and from 0.15 to 1.7 tons ha−1 for Sorghum (Roose et al. 1999). The main obstacle to the widespread uptake of this technique is, however, that it is labor intensive (300 h ha−1 of work), requires a huge amount of organic substrates (3 tons ha−1), and is limited to semi-arid environments receiving between 300 and 800 mm water (Roose et al. 1999). These results are also likely to be context dependent, and perhaps species dependent. Indeed, no significant influence on soil aggregate stability and C content was measured in sub-humid tropical ecosystems by Paul et al. (2015), who even measured an increase in crop yield (+ 34% for maize and 22% for soybean) after the eradication of termites in the field.
Tillage has a negative impact on termites and ants (Sanabria et al. 2016). The influence of zero or low tillage on termites has also been investigated in wheat and maize plantations in India (Reddy et al. 1994; Sharma et al. 2004). These practices were associated with lower termite damage compared to rotary and conventional tillage, probably because of the higher soil moisture that could favor pathogenic fungi (e.g., Metarhizium anisopliae, Grace 1997; Wright et al. 2005) or predators (e.g., ants) throughout the crop growth period. However, it is worth mentioning that zero and low tillage were also associated with weed development, potentially more herbicides for their control, and lower yield (Reddy et al. 1994; Sharma et al. 2004), thereby highlighting the limits of this approach.
4.2 Considering agro-ecosystems as heterogeneous and complex environments.
Aboveground termite mounds, especially those built by fungus-growing termites, create hot-spots of nutrients in ecosystems (Sileshi et al. 2010; Jouquet et al. 2016). Termite mounds are usually enriched in clay, exchangeable cations, and macronutrients compared with the surrounding top-soil layers (Holt and Lepage 2000; Jouquet et al. 2011). Their positive influence on plant growth and diversity, hydrology, and ecosystem resistance to drought was mainly found in non-cultivated environments (Collins 1983; Dangerfield et al. 1998; Yamada et al. 2005a; Pringle et al. 2010; Bonachela et al. 2015; Bottinelli et al. 2015; Jouquet et al. 2016). However, studies carried out in Africa highlight that these structures can also help farmers to reduce the risks of crop failure (Brouwer et al. 1993; Harris et al. 1994, cited by Tilahun et al. 2012). Subsistence farmers in Africa and Asia commonly destroy and spread termite mound soils in their fields to improve soil fertility (Fairhead and Scoones 2005; Verlinden et al. 2006). Termite mounds can also be associated with fruit trees, as shown in Namibia by Verlinden et al. (2006). They provide numerous ecosystem services in paddy fields in Thailand such as shade for cattle and for growing vegetables, proteins from insects, mushrooms, medicines from the diversity of trees growing on mounds, or even refuges for predators such as ants (Choosai et al. 2009; Choosai 2010). In Africa, traditional soil classification is also based on the abundance of termite mounds (Adamou et al. 2007, Tilahun et al. 2012). Fairhead and Scoones (2005) mentioned that traditional farming practices in Africa consist in selecting lands with many large termite mounds, which can be used for gardening. These authors also report direct and indirect methods for triggering termite activity in the fields, for example through the maintenance of trees that offer a beneficial environment to termites (Fairhead and Scoones 2005).
5 Conclusion and implications
The relationship between termites and humans can be seen as another example of the numerous conflicts between humans and wildlife, such as those that exist between men and elephants, leopards, or tigers in India. As we learn to share our environment with large herbivores and predators, a new challenge for agronomists is to develop agricultural practices that get the best from termites (e.g., their abilities to improve water dynamics in soil and to improve soil fertility close to their nests) while making their negative impacts on plant growth and yield acceptable to farmers.
The green revolution led to a simplification and homogenization of agro-ecosystems and to an overuse of chemicals, thereby precluding termites from our cultivated lands. In retrospect, we know that the utilization of these chemicals is of concern as they create problems for our health and the environment. The dream of ridding termites from plantations thus appears today as a costly legacy from the green revolution. In contrast, the development in agroecology highlights the importance of considering the soil as a living system (e.g., Okwakol and Sekamatte 2007; Gobat et al. 2010), and of the enhanced use of biodiversity as an essential element of agroecological approaches (Altieri 1995). New, environmentally friendly and more ecological approaches have also to emerge to give termites a status similar to that of earthworms in arid and sub-arid ecosystems. It is stated in the Biodiversity Atlas (Jeffery et al. 2010) that “termites and ants appear to have a similar role to earthworms and enchytraeids in more temperate and tropical organic soils (…)”. This review highlights that termites are obviously not playing the same roles as earthworms in arid- and sub-arid cultivated ecosystems, and that they provide both ecosystem services and disservices. However, the examples given in this article emphasize that (i) not all termite species are harmful in plantations and that a first step towards a more sustainable use of biodiversity is perhaps to teach farmers to recognize the different species and/or functional groups that occupy their lands and to adapt their management accordingly, (ii) termite damage can be reduced by restoring refuges to predators or by reorienting termite foraging activity towards organic amendments (litter and dung or compost materials), and (iii) the stimulation of termite activity improves key ecological functions in agro-ecosystems (water availability to plants and the creation of fertility hot-spots in the examples given above). This review also stresses the need for a better understanding of the services that termite mounds can provide in agro-ecosystems. We believe that one of the challenges for sustainable agriculture is to consider drylands as complex and heterogeneous systems where termite mounds can provide numerous services and contribute to ensure food security and improve the resistance to environmental change.
This review article is the outcome of a discussion initiated at the XI National Symposium on Soil Biology and Ecology on Soil Biota and Social Insects for Sustainable Organic Farming that took place at the University of Agricultural Science GKVK, Bangalore, India.
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