Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 7 Number 10 (2018) Journal homepage: http://www.ijcmas.com

Review Article https://doi.org/10.20546/ijcmas.2018.710.118

Ecosystem Services of the Eco-Engineers: The Earthworms

Mansi Ramesh Das, Amruta Chandrakant Nimbalkar*, Samiksha Sunil Pisal and Vitthalrao B. Khyade

Science Association, Shardabai Pawar Mahila Mahavidyalaya, Shardanagar Tal. Baramati Dist. Pune – 413115, India

*Corresponding author

ABSTRACT

Although most earthworms live at or under the surface of the soil, other factors influence their choice of habitat. Two key factors are climate and vegetation. Earthworms tend not to K e yw or ds live in exceptionally dry or cold places. The earthworms live in indigenous forests and tussock grassland, while introduced species are most commonly found in cultivated soils Vermicomposting , such as pasture, croplands and lawns. A more specific way to describe where earthworms Earthworm, Diversity, live is their niche – the position of the species within its habitat. A species’ niche includes Ecosystem services, Threat both its physical location and the role it plays within the environment. By occupying a specific niche, earthworms make use of conditions that are best suited to their survival. Article Info Although all earthworms have common characteristics, features like size, pigmentation

Accepted: (skin colour) and quickness of movement reflect which niche different species occupy. 10 September 2018 Soil-dwelling earthworms fall into three main niche groupings: compost and soil-surface Available Online: dwellers (epigeic), top-soil dwellers (endogeic) and deep-burrowing subsoil dwellers 10 October 2018 (anecic). The present attempt intends to communicate the importance of earthworm

diversity conservation. Development of conservation management to prevent earthworm diversity decline should be done wisely and involve all stakeholders. Introduction Timmenga, 1990; Zachmann and Linden, 1989). Quality, quantity and placement of Earthworms can play a variety of important organic matter is a main determinant of roles in agroecosystems. Their feeding and earthworm abundance and activity in burrowing activities incorporate organic agricultural soils (Edwards, 1983; Lofs- residues and amendments into the soil, Holmin, 1983), as are disturbances of the soil enhancing decomposition, humus formation, by tillage, cultivation, and the use of nutrient cycling, and soil structural pesticides (Doran and Werner, 1990). development (Mackay and Kladivko, 1985; Biodiversity loss has become one of the Kladivko et al., 1986). Earthworm burrows leading global issues, with a rapid loss of persist as macropores which provide low biodiversity reported worldwide. The rate of resistance channels for root growth, water species loss is predicted to increase infiltration, and gas exchange (Kladivko and considerably over the next 50 years.

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Biodiversity is classified into above-ground functions affect ecosystem services (Jouquet biodiversity and below-ground biodiversity et al., 2014). Ecosystems services were (soil biodiversity) that mutually interact estimated to account to up to U.S. $33 trillion (Wardle, 2002; Wardle et al., 2004). dollars per year of human capital equivalent. Functioning of terrestrial ecosystems greatly Soil biota contributes to approximately 38% of depends on below-ground biodiversity. Soil this amount (Skubala, 2013). The rapid growth biodiversity is vital to humans as it supports a of human population leads to increased wide range of ecosystem processes, functions, pressure on soil. Anthropogenic activities and services (Costanza et al., 1997; Blouin et accelerate the loss of biodiversity and al., 2013; Skubala, 2013; Jouquet et al., 2014). ecosystem services in soil. Currently, However, the importance of below-ground approximately 60% of ecosystem services is biodiversity has often been ignored or degraded because soil is not used in a undervalued (Secretariat of the Convention on sustainable manner (Skubala, 2013). Biological Diversity, 2010). Soil biodiversity in many areas worldwide has already been Earthworms represent an important soil faunal declining (Jeffery and Gardi, 2010). group that is distributed worldwide. Furthermore, biodiversity loss results in the Earthworm populations contribute to decline of ecosystem resilience. When approximately 40-90% of soil macrofaunal elements of biodiversity are lost or threatened, biomass and 8% of total soil biomass in many ecosystem services degrade (Black et al., ecosystems (Sinha et al., 2013). However, in 2003). Ecosystems with heterogeneous intensively cultivated annual crops biodiversity tend to be more stable, whereas earthworms have lower contribution to total those with homogeneous biodiversity are often soil biomass (Fragoso et al., 1999; Tondoh et more vulnerable to environmental stress al., 2007; Blouin et al., 2013). Earthworms are (Hunter Jr., 1999). Healthy soil biodiversity the most valuable animals that influence the provides a number of natural services that are functioning of soil ecosystems (Hendrix and useful to human being. Bohlen 2002; Gonzales et al., 2006). Earthworms increase soil bulk density, pore Ecosystem services are defined as size, water infiltration rate, soil water content, contributions of ecosystem structure and and water holding capacity. They also increase functions, in combination with other inputs, to litter decomposition, soil organic matter human well-being. Essentially, these are dynamics, nutrient cycles, promote plant services provided by biodiversity that link the growth and reduce some soil-borne diseases functioning of ecosystems to their benefit (Brusaard, 1997; Chandran et al., 2012; extended to humans. Ecosystem processes are Elmer, 2012). Earthworms produce organo- the changes or reactions occurring in an mineral biogenic structures (Lavelle, 2000), ecosystem, such as, for instance, biophysical and influence gaseous composition of the processes (decomposition, production, nutrient atmosphere (Kibblewhite et al., 2008). cycling, energy, and nutrient fluxes) Earthworms are also involved in restoring (Crossman et al., 2013). Ecosystem functions ecosystem services via direct and indirect occupy an intermediate position between mechanisms (Jouquet et al., 2014), especially ecosystems processes and services. Ecosystem in the situations when soil is degraded or land function can be defined as the capacity of is under rehabilitation after mining (Boyer and ecosystem to provide goods and services that Wratten, 2010). Earthworms represent an satisfy human needs, both directly and essential component of soil nutrient cycling indirectly (de Groot et al., 2002); these (Lavelle and Spain, 2001). They maintain

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 good soil health through the comminution of Five forces are considered to accelerate the organic debris, enhance microbial activity, and decline of earthworm diversity: contribute to the increase of nutrient availability in soil and mineral absorption by Soil degradation and habitat loss, plants. Burrowing and grazing activity of earthworms modifies the soil structure and its Climate change, capacity to absorb water. These advantages increase crop productivity. Earthworms Excessive nutrient and other forms of represent a unique indicator of soil health contamination load, (Science for Environment Policy, 2009; Elmer, 2012), and a good bio-indicator of Over-exploitation and unsustainable degraded land due to anthropogenic activities management of soil, and (Tondoh et al., 2007). Earthworm diversity is a key determinant of ecosystem stability that Invasive species (Moore, 2005; Secretariat of is responsible for the provision of many the Convention on Biological Diversity, ecosystem services (Eisenhauer and Schädler 2010). 2011; Blouin et al., 2013). Global increase in human population and Earthworm communities consist of many demand for resources has led conversion of different species, and each plays a unique role forests to agricultural or urban land in soil processes. To understand the function worldwide. This largely contributes to the of earthworms in soil ecosystems, first the decrease and loss of earthworm biodiversity. species valuable to ecosystem services should Habitat loss and soil degradation, caused by be identified. Research on earthworm species agricultural activities and unsustainable forest diversity has been carried out, but only in a management, represent the greatest pressure limited number of geographical regions. on earthworm diversity. Some researchers According to a previous study, less than 50% have reported that earthworm diversity has of earthworm species in the world have been been reduced, and some native species have described (Brown et al., 2003). The been lost, because of forest conversion to knowledge of earthworm species diversity is agriculture and presence of invasive species. still limited in many countries (Brown et al., Such species loss results in negative impacts 2006), and especially in tropics (Suthar, 2011; on ecosystem services (Dewi et al., 2006; Chandran et al., 2012). Moreover, earthworm Loss et al., 2012; Hairiah et al., 2014). diversity studies have mostly focused on taxonomy and have not evaluated the Soils represent the main habitat for association with ecosystem services. Soil earthworms. However, many soils undergo systems provide an excellent basis to degradation processes (Lavelle et al., 2006; investigate the relationship between Lavelle, 2009), thereby endangering earthworm diversity and ecosystem earthworm diversity. Soil degradation is one functioning (Lavelle, 2000). A clear of the most dangerous threats to earthworm understanding of the relationships between diversity in this century that should receive earthworm diversity and ecosystem services is more attention around the world (Skubala, required to evaluate the influence of 2013). Understanding how earthworm species anthropogenic activities on ecosystems, and to adapt to disturbances and survive in develop management strategies aiming to agriculture soils can help to develop strategies preserve earthworm diversity. to earthworm biodiversity conservation.

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Moreover, the importance of earthworm earthworms are living and feeding in the soil, diversity to ecosystem services and human so they are considered soil feeders. They play well-being needs to be communicated to a key role in soil aggregate formation. different stakeholders, including farmers. Endogeic species have a body size of Local ecological knowledge can be used to approximately 5-10 cm and are usually not facilitate the communication between farmers pigmented. Their activity creates a network of and scientists (Zúñiga et al., 2013). horizontal branching burrows, which increase porosity, and release nutrients from their feces Ecosystem services availed by the (Jones, 2003). Inoculation of endogeic earthworm earthworm Pontoscolex corethrurus in agroforestry mesocosms increased mean Earthworms are soil inhabitants. However, weight diameter, C and N storage in large different earthworm species have different macro-aggregates (>2000 μm) (Keith and feeding and living preferences, as well as Robinson, 2012). Soil ecosystems inhabited burrowing behaviors. Hence, earthworms by epigeic, endogeic, and anecic earthworms species show different ecological functions. have better physical, chemical, and biological They can be classified into epigeic, endogeic, properties than other ecosystems inhabited by and anecic species (Fragoso and Lavelle, only one or two levels of earthworm 1995; Fragoso et al., 1997; Brusaard, 1997). functional groups. Moreover, the presence of Epigeic earthworms eat and live on rich litter different earthworm functional groups in soil surface layer and do not form burrows; they has a positive effect on ecosystem services. have small size body (5-15 cm body length at The summary of relationships between maturity), and bright color (Jones, 2003). earthworm functional groups, soil processes Epigeic species play an important role in litter and ecosystems services are shown in Figure comminution and decomposition of organic 1. material at the soil surface that increase nutrient transformation and stimulate activity In addition to the earthworm classification of microorganisms. Anecic species live in sub- based on functional groups, earthworms can vertical burrows in the mineral soil, feed on be classified based on biogeography, into fresh litter from surface soil and bring it into native species and exotic species. Native the soil profile (Fragoso et al., 1997); these species of earthworms evolve in the given site worms are colored on the dorsal side and often or region (Fragoso et al., 1999). Such have a large size body (15-20 cm) (Keith and earthworm species usually live in one region, Robinson, 2012). Anecic earthworms can in contrast to species that have been burrow into the deeper layers of the soil, and introduced by human activity. Exotic or reach depth of 1-2 m. Their feeding activity introduced earthworm species are those modifies the soil structure through the creation earthworm species that have been transported of vertical burrows and increases macro- to areas where these species do not live porosities, aeration, and water infiltration into naturally, either on purpose or by accident. the deeper soil. Anecic burrow entrances Most research has focused on this group of called “midden” that are surrounded by a earthworms. mound of cast material and usually crowned with fragmented plant litter. Anecic Earthworm life is influenced by the earthworms also affect litter breakdown rate availability of suitable food, soil moisture, soil and nutrient cycling by combining surface temperature, oxygen exchange, soil texture, litter into the soil profile. Endogeic soil pH, and presence of predators (Edward

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 and Lofty, 1977; Lee, 1985). Earthworms like the microflora and microfauna in earthworms moist soil, because the water protection guts (Lavelle and Spain, 2001). Earthworm mechanisms in their bodies are not well life is also affected by predators, and developed. Respiration rate depends on the especially birds (Lee, 1985). Ecosystem gas diffusion through the body wall, which services provided by earthworms relate to the must always be moist. Earthworms can effects of earthworm activity on soil systems survive in a range of soil temperatures varying (Moreira et al., 2008). Earthworms play an between 0°C and 35°C (Lee, 1985). The important role in soil ecosystem functioning optimum soil water content varies and human welfare (Hendrix and Bohlen, considerably depending on the species and 2002; Gonzales et al., 2006; Ernst and ecological group earthworm belongs to, that Emmerling, 2009; Science for Environment can differ even within the same species, Policy, 2009). Earthworm diversity plays an depending on its ability to adapt to local important role in agricultural systems and is environmental conditions (Lee, 1985). an integral part of soil health and fertility. Earthworms are most active in moist soil Earthworms consume decomposable organic conditions (Lee, 1985; Lavelle and Spain, matter and break it down into smaller pieces 2001). The earthworm community structure is providing food to almost all soil controlled by the nutrient content of soil and microorganisms. Their excrements or the amount of seasonal rainfall (Fragoso and “casting” supports highly diverse microbial Lavelle, 1995). communities, including beneficial fungi and bacteria (Elmer, 2012). As a result of The main food source for earthworms is microbial activity, availability of nutrients to decaying organic waste (Lee, 1985). plants also enhances. Earthworms also provide Earthworms prefer decomposed organic food benefits to farmers. Earthworms contribute to larger than 50 µm in size (Lavelle et al., the improvement of plant resistance to pests 2001). Because of the limited movement and indirectly suppress soil-borne diseases. As capability, earthworms like to live close to a result, crop productivity improves (Ernst and source of the food source. Population density Emmerling, 2009). and distribution of earthworms in forest ecosystems is strongly influenced by the Earthworms have been called “ecosystem quantity, quality, and timing of litter inputs to engineers.” They are capable of modifying the soil system. The high content of their physical environment by mixing soil polyphenols and other secondary compounds layers from the bottom to the top and vice in litter affects the density of earthworms in versa incorporating organic matter into the soil tropical forests (Fragoso and Lavelle, 1995). and producing biogenic structures. This way, Epigeic earthworms prefer high-quality litter earthworms change the structure of the soil. soil layer (Tian, 1992; Lavelle and Spain, Different types of earthworms' functional 2001). Earthworm communities are also groups can create horizontal and vertical influenced by biological processes occurring tunnels, which can be quite deep in soil. These within the soil environment. Earthworms tunnels form pores that facilitate oxygen and develop various interactions with microflora carbon dioxide exchange, and allow water (bacteria, fungi), microfauna (protozoa and penetration into the soil. Thus, water, gas and nematodes), and other macrofauna groups solute transfer processes and soil water (ants in particular) (Wardle, 2002). Digestion holding capacity improve (Capowiez et al., in earthworms is mediated by the enzyme 2001). Earthworms' burrows serve as soil mixture produced by the intestinal wall, and macro-porosities (Lal, 1991; Brusaard et al.,

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1993; Jimenez et al., 1998; Stott et al., 1999; castings produced by large-sized endogeic Lavelle et al., 2001). Soil porosity is crucial earthworms (compacting species), so that the property because it determines: (1) rate of organic matter content of the casting water infiltration, (2) water holding capacity, decreased. Casting with lower organic matter (3) the drainage of water excess, (4) soil will be broken easily by raindrops, resulting moisture, and (5) the exchange rate of CO2 the compacted soil. Fresh earthworm casting from soil to atmosphere and vice versa (Wolf is soft and fragile, and vulnerable to raindrops, and Snyder, 2003). The disruption of but it becomes harder, and more resistant to earthworm diversity impedes water infiltration water and wind erosion with time. Effect of into the soil thus resulting in increased surface compacting species on soil structure is run-off, erosion, flooding, and drought. strongly influenced by the presence of organic debris on the soil surface. Blanchart et al., Earthworm casts (earthworms' feces) are also (1999) reported that activity of Pontoscolex crucial to the structure of soils. Earthworm corethrurus (compacting species) in activity has a positive impact on the formation agroecosystems with low soil organic matter of soil structure, through the improvement of in Yurimaguas (Peru) leads to hardening of infiltration rate, water absorption, and soil soil surface that inhibits the infiltration. resistance against the erosive of rainfall and However, in the soil with high organic matter surface run-off (Glinski and Lipiec, 1990; content or soil mulched with legumes, Stott et al., 1999). Earthworms make earthworms enhance soil macro-aggregate continuous channels from the soil surface to development. Lavelle (2000) also reported that the deeper layers, so that water can infiltrate P. corethrurus invaded a pasture in Central quickly into the subsoil. Therefore, the soil Amazonia, and produced an excessive amount with higher earthworm activity has better of unstable large cast. This cast formed 5 cm infiltration rate than soil without or with small impermeable crust inhibiting plant growth. earthworm community. Hence, earthworm Soils with low organic matter and low activity reduces the risks of run-off and water earthworm diversity and abundance s tend to logging. be more sensitive to erosion than soils with high earthworm population and diversity (Lal, In addition to these indirect advantages, 1991). Management of soil organic matter is earthworms also directly benefit humans, keys factor affecting the ecosystem services being for example a food source for fish (and performed by earthworms. used as a fish bait), and being part of vermicomposting. Some Amerindian Earthworms play an important role in communities in South America utilize determining the greenhouse-gas balance of earthworm as a source of seasonal food and an soils worldwide. Whether earthworms essential source of protein in their diet (Keith represent a “sink” or “source” of greenhouse and Robinson, 2012). Earthworms contribute gas remains highly debated. Earthworms cast up to €723 million per year in terms of the is stable soil aggregate, is recognized as a livestock product value (Bullock et al., 2008). “sink”. It stimulates carbon sequestration and Earthworms, like all other organisms, have enhances long-term protection of C in soil. certain advantages and disadvantages. Some However, earthworms can accelerate the species of earthworms were reported to have decomposition of C by microorganisms in the adverse impacts on soil structure (Lal, 1991; soil and thus enhance CO2 emission or as Blanchart et al., 1999). Small-sized endogeic “source” of greenhouse gas (Simek and Pizl earthworms, a “de-compacting species,” eat 2010). Earthworm gut is ideal environment for

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 denitrifying bacteria as it is anaerobic structure of biochar makes it chemically and microsite enriched by available carbon, biologically stable, allowing it to persist in soil nitrogen, with favorable moisture level, for centuries. Biochar decreases N2O essential for stimulating activity of denitrifiers emissions since N2O emissions are enhanced and high potential to increase N2O emission. by high soil organic matter content. Endogeic Earthworms activity in fertilized grasslands earthworms, P. corethrurus, can grind the enhances grass N uptake. However, biochar and reject it in their casts, which affect earthworms, and epigeic earthworm species biochar distribution in the soil profile. (Lumbricus rubellus) in particular, may also Agricultural management, such as tillage and have side effects in ecosystems, and increase fertilization with N fertilizers in particular, N2O emissions by 10% (Lubbers et al., 2011, plays a significant role in greenhouse gas Lubbers et al., 2013). Based on the meta- emission by influencing soil analysis using 237 observations of 57 articles microenvironment (Plaza-Bonilla et al., 2014). published on the ISI-Web of Science between Earthworms and biochar application on soil is 1990 and 2011, it can be concluded that one of the best technique to improve soil earthworms increased 33% and 42% of CO2 fertility and health (Asuming-Brempong and and N2O emissions, respectively. These Nyalemegbe, 2014). The best technology for effects depend on some controlling factors, sustainable management of land and water such as earthworm functional groups, resources should maintain and protect population size, experimental period, earthworm abundance and diversity (Blanchart experiment type, nutrient input, soil organic et al., 1999). matter content, C/N ratio of soil, and type of ecosystem. Over a longer period (> 30 days), Earthworm diversity under threat earthworms tend to increase N2O emissions, but decrease CO2 emission. Increase of N2O There are thousands of earthworms species emissions by earthworms correlates to the with different biogeography. They have increase of organic C input as well as to the different morphological characteristics, height of soil organic matter layer having low although some of these characteristics are C/N ratio (Lubbers et al., 2013). This difficult to determine by naked eye. conclusion was mainly derived based on Earthworm species can be identified based on laboratory experiments and only one article three complementary approaches: taxonomy, based on field experiments. Moreover, most biogeography, and ecological functional experiments can only be conducted during less groups. Each identification method has than 200 days. Hence, the effect of disadvantages. Therefore, identification of earthworms on greenhouse gas balance is still earthworm species should be done using more unclear and needs further understanding. The than one method. A taxonomic approach use of biochar in agricultural practices implies studying earthworm diversity based on potentially reduces N2O emissions produced the number and identity of different species by earthworms (Asuming-Brempong and (species richness), regardless of their Nyalemegbe, 2014). Biochar or charcoal has a ecological role. Taxonomic identity can be porous physical structure, and thus increases determined using conventional methods oxygen diffusion into the soil and creates (observing internal and external aerobic conditions providing a suitable habitat morphological characteristics), or by advanced for aerobic soil microorganisms, and molecular genetics and genomic analysis potentially reducing the activity of anaerobic techniques (Dupon, 2009; Chang and James, denitrifying bacteria. The polycyclic aromatic 2011). However, molecular techniques have

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 been rarely applied in earthworm research services provided by earthworms is still (Dupon, 2009). The disadvantage of needed (Brown et al., 2003). Identification of identification based on external morphological earthworms based on ecological functional characteristics is that this way immature groups is an important goal in soil ecology earthworm cannot be identified. However, (Keith and Robinson, 2012), and a big identification based on internal morphological challenge for earthworms taxonomists (Giller characteristics is quite difficult, especially for et al., 1997). beginners. Molecular methods are more promising but involve high costs, and not Patterns of earthworm distribution and species affordable to everyone. Systematics of richness were described to be directly related earthworms still faces many problems and is to biogeography, local microclimate and not complete (Fragoso et al., 1999; Jones, human activities (Suthar, 2011). Earthworm 2003). General identification keys for tropical species of family Megascolecidae were found and subtropical earthworm species are not in many tropical regions in East and Southeast available and still need to be developed. Asia, and Australia (Edward and Lofty, 1977; Currently, there are only few professional Lee, 1985; Jones, 2003; Fragoso and Csuzdi, taxonomists in the world. Hence basic training 2004). Species from family Glossoscolecidae on earthworm species identification has to be are widespread in the regions of Central undertaken by new taxonomists (Brown et al., America, South and North, while species of 2013). The difficulties in identifying family Ocnerodrilidae family are mainly earthworm species can inhibit researcher's found in India, Central and South America, interest to become an earthworm taxonomy and Africa. Earthworm species of family expert. Acanthodrilidae are commonly found in India, Burma, New Zealand, and Australia (Fragoso Based on the taxonomic identification, and Csuzdi, 2004). earthworms belong to phylum Annelida, sub- phylum Clitellata, and class Oligochaeta that Why is it essential to study the earthworm consists of 20 families, 693 genera, and more diversity? Earthworms represent an important than 6000 species. Currently, 3627 species group of soil macrofauna that provides have been described (Giller et al., 1997; ecosystem services for human well-being. At Fragoso et al., 1997; Lavelle and Spain, the same time, earthworms are very sensitive 2001). It was estimated that less than 50% of to anthropogenic activities. Earthworm species exist worldwide (Fragoso et al., 1997) diversity is important to study because the and only a few dozen have been studied different ecological groups of earthworms extensively (Brown et al., 2003). Earthworm play important role in soil processes and species are found mainly in tropics, but most ecosystem services. Different species of of the tropical regions, such as Southeast Asia, earthworms are also characterized by different Africa, and South America have not been levels of sensitivity to habitat disruption, and widely surveyed for earthworm diversity are good indicators of land management (Jones, 2003). In Indonesia, the research on practices. Estimation of earthworm species earthworm diversity is still limited and richness can help determine the redundancies receives little attention. Despite the high and keystone species in ecosystem processes. importance of earthworms that were Different earthworm species provide a various introduced in Indonesia by Darwin in 1938 functions in different soil layers (Bullock et and many ecological researches in the al., 2008). Earthworm diversity is clearly can following years, more research on ecosystems be used as an estimate of ecosystem services

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(Keith and Robinson, 2012). One more million ha of forest per year. Furthermore, the important factor affecting earthworm diversity greatest conversion rates in the world are is environment variability, such as the amount happening in tropics (USDA Forest Service and quality of nutrients and energy sources, International Programs, 2014). Forest seasonal changes, spatial differences in soil conversion to agricultural and other types of and, climate variability, and biotic interactions land use leads to disruption of taxonomic and within the community (Breure, 2004). Soil functional diversity, and loss of native management in agricultural ecosystems earthworm species (Rao, 2013). There is a strongly influences earthworm diversity. strong correlation between an increase in land Different management practices affect the use intensity and decrease in earthworm habitat quality and the availability of substrate diversity. Forest conversion to coffee to earthworms, hence resulting the change in plantations and other agricultural land in abundance and diversity of earthworms. Sumberjaya (West Lampung, Indonesia) led to Intensive soil tillage drastically reduces the reduction or loss of epigeic native earthworm earthworm populations, especially in areas species, such as Metaphire javanica. where the land has been conversed to Subsequently, the population of small body- monoculture (Bullock et al., 2008). Habitat size endogeic-exotic earthworm species such loss and soil degradation, caused by as P. corethrurus increased but did not affect agriculture and unsustainable forest the population abundance (Table 1). Native management create the biggest pressure on species are more sensitive to land-use change earthworm diversity. Some researchers have than exotic species (Dewi et al., 2007). reported cases of earthworm diversity Previous studies have also shown that the decrease and loss of native species as a result body size of earthworms tends to be smaller in of forest conversion to agriculture. Forest areas with more intensive land management conversion also increases invasive species (Figure 2) (Susilo et al., 2009). Earthworm domination that has a negative impact on abundance is higher in areas with more ecosystem services (Dewi et al., 2006; Loss et intensive management than in areas with less al., 2012; Hairiah et al., 2014). intensive management. This is especially true in areas with higher plant rotation and larger Earthworms are sensitive to land use change, waste harvests left in the soil (Bullock et al., ecosystem perturbations, and rehabilitation 2008). Similarly, the forest conversion to (Tondoh et al., 2007). Human activities intensified agricultural land in Ivory Coast represent an important factor causing resulted in potential increase in relative reduction of earthworm diversity. Global abundance and biomass of earthworm species, increase in human population and high particularly in areas with medium level demand for resources has led to the intensification agriculture, as reported by conversion of forests to agricultural land. Tondoh et al., (2007). These researchers found Intensified agricultural management can lead that some earthworms species were highly to the decrease or loss of earthworm sensitive to land use changes, i.e., Dichogaster biodiversity. The USDA Forest Services saliens Beddard 1893, Hyperiodrilus africanus International Programs reported that every Beddard 1891, Millsonia omodeoi Sims 1986, year the world loses 14.6 million hectares (ha) Dichogaster baeri Sciacchitano 1952, of forest that is converted to agricultural or Dichogaster ehrhardti Michaelsen 1898, residential land. Although parts of forests have Agastrodrilus sp., Stuhlmannia palustris been used as estates, reforestation and natural Omodeo and Vaillaud 1967 and, to some forest extension, the world still loses 9.6 extent, Millsonia sp. (Tondoh et al., 2007).

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http://www.agrsci.jp/ras/article/view/13/27

Ecological aspects of earthworm Species which build permanent, vertical burrows that penetrate the soil deeply were Earthworm species can be classed in one of termed anecics by Bouche. These species are three morpho- ecological groupings (Bouche, detritivores and come to the surface to feed on 1977). Epigeic species live in organic partially decomposed litter, manure, and other horizons and ingest large amounts of organic matter. The permanent burrows of undecomposed litter. These species produce anecics create a microclimatic gradient, and ephemeral burrows into the mineral soil for the earthworms can be found shallow or deep diapause periods only. They are relatively in their burrows depending on the prevailing exposed to climatic fluctuations and predator conditions. Anecics have profound effects on pressures, and tend to be small with rapid organic matter decomposition, nutrient generation times. A common example is cycling, and soil formation. The most Eisenia foetida (redworm, manure worm) common examples are the nightcrawlers sold which is used in vermicomposting. by fish-bait dealers consisting of Lumbricus terrestris and Aporrectodea longa. Endogeic species forage below the surface, ingest large quantities of soil with a Palatability of different types of litter to preference towards organic rich soil, and earthworms may depend on nitrogen and build continuously ramifying burrows that are carbohydrate content, and the presence of mostly horizontal. These species are polyphenolics such as tannins (Satchell, apparently not of major importance in litter 1967). Earthworms prefer materials with a incorporation and decomposition since they low C/N ratio, such as clovers, to grasses feed on subsurface material. which have a higher C/N ratio (Ruz Jerez et al., 1988). Colonization of litter residues by They are important in other soil formation microorganisms also increases palatability processes including root decomposition, soil (Cortez et al., 1989), as does leaching of mixing, and aeration. feeding inhibitors.

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Epigeic: surface dwellers Anecic: subsoil dwellers

Epigeic earthworms live in areas containing Anecic earthworms live in permanent burrows high amounts of organic matter. They live at as deep as 3 m below the soil surface. They or near the soil surface and feed on leaf litter, collect food from the soil surface and ingest decaying plant roots or dung. These organic matter from the soil. Anecic earthworms do not form permanent burrows. earthworms form extensive burrows that Epigeic species tend to have dark skin colour extend laterally and vertically through the (pigmentation). The pigmentation acts as subsoil. Their burrows can be up to 2 cm in camouflage as they move through the leaf diameter. Introduced anecic earthworms have litter. some pigmentation. Indigenous anecic species tend to be sluggish and have weakly It also helps to protect them from UV rays. developed muscles. Because they live so Being close to the ground surface exposes the deeply in the soil, native anecic species have earthworms to predators so their muscles are little pigmentation, and being so pale, they are strong and thick in proportion to their length, often referred to as milk worms. These deep- allowing for quick movement. Being so close burrowing species are also the longest, to the surface also makes them vulnerable to ranging from 3 cm up to a very large 1.4 m. stock treading in intensively grazed paddocks. Treetop dwellers and other unusual Epigeic species tend to be small (1–18 cm in habitats length). Introduced epigeic earthworms tend to live in compost (such as the introduced Earthworm habitats and niches are not all tiger worm Eisenia fetida, which cannot under the ground. Native earthworms are survive in soil) and under logs and dung. frequently found under the bark of dead trees, Native species usually live in forest litter. in the litter of epiphytes and sometimes in the crooks of tree branches! There are also a Endogeic: top-soil -dwellers number of aquatic earthworms that live in semi-saturated habitats. Endogeic earthworms are the most common earthworm species found in New Zealand. Beneficial aspects of earthworms Their niche is the top 20 cm depth of soil. Endogeic earthworms eat large amounts of Deep burrowing species such as L. terrestris soil and the organic matter in it, although can burrow through compacted soil and species sometimes come to the surface to penetrate plough pans, creating channels for search for food. drainage, aeration, and root growth (Joschko et al., 1989). Recent work by Shipitalo and They form shallow semi-permanent burrows. Protz (1989) elucidated some of the Endogeic earthworms have some mechanisms by which earthworms enhance pigmentation. Their muscle layers are not as soil aggregation. Ingested aggregates are thick nor do they move as quickly as epigeic broken up in a liquid slurry that mixes soil earthworms. Endogeic species range in size with organic material and binding agents. The from 2.5–30 cm. Introduced endogeic defecated casts become stable after drying. earthworms are often found in agricultural Stewart et al., (1988) also presented evidence soils, while native endogeic earthworms are that earthworms initiate the formation of often found in tussock grasslands. stable soil aggregates in land degraded by

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 mining. In forest ecosystems earthworms, Earthworms may increase levels of metabolic especially litter feeders such as L. terrestris, activity in soils, as measured by the amount of can consume all the litter deposited on the soil CO2 evolved, yet nematode abundance and surface within a period of several weeks microbial biomass may decrease (Yeates, (Knollenberg et al., 1985) or months 1981; Ruz Jerez et al., 1988). This occurs (Satchell, 1967). Incorporation of litter by because earthworms reduce the amount of earthworms in apple orchards can be an substrate available to other decomposers, and important mechanism for preventing because earthworms ingest other decomposer outbreaks of scab fungus, spores of which are organisms as they feed. This process would transmitted from litter to new foliage by tend to accelerate nutrient cycling rates. spring rains. Raw (1962) found a high correlation between L. terrestris biomass and Management effects on earthworms apple leaf litter incorporation, with over 90 percent of litter incorporated during the Earthworms are not favored by tillage, and in winter when this species was abundant. general the greater the intensity and frequency of disturbance, the lower the population Incorporation of surface litter may be an density or biomass of earthworms (Haukka, important function of earthworms in no- 1988; Mackay and Kladivko 1985; Edwards, tillage agroecosystems. Introduction of 1980; Gerard and Hay, 1979; Barnes and earthworms to areas not previously populated Ellis, 1979). Agricultural soils are generally has led to improvement of soil quality and dominated by species adapted to disturbance, productivity in New Zealand grassland low organic matter content, and a lack of (Martin, 1977), on drained Dutch polders surface litter. Earthworms are dependent on (Van Rhee, 1977), in heathland in Ireland moderate soil moisture content, and (Curry and Bolger 1984), and in mining spoils cultivation tends to have a negative effect on in the U.S. (Vimmerstedt and Finney, 1973). earthworms by decreasing soil moisture (Zicsi, 1969). Some common agricultural Earthworm casts are sources of nutrients for lumbricids are Allolobophora chlorotica, the plants. Lumbricids in a pasture soil produced Aporrectodea caliginosa species complex (A. casts that contained 73 percent of the nitrogen trapezoides, A. turgida, and A. tuberculata), found in the ingested litter; indicating both the and L. terrestris. Species common to organic importance of earthworms in incorporating rich habitats, such as E. foetida are rarely litter nitrogen into the soil and the found (Lee, 1985). inefficiency of nitrogen digestion by earthworms (Syers et al., 1979). Earthworms Earthworm populations are usually increase the amount of nitrogen mineralized significantly depressed in cropped fields from organic matter in soil. Because relative to pasture or undisturbed lands. nitrification is enhanced in earthworm casts, Lumbricids in a South African soil were the ratio of nitrate-N to ammonium-N tends to decreased by cultivation to about one-third of increase when earthworms are present (Ruz original levels. Aporrectodea trapezoides was Jerez et al., 1988). Nitrogen-fixing bacteria less affected than Eisenia rosea, possibly are found in the gut of earthworms and in because it is able to burrow more deeply in earthworm casts, and higher nitrogenase the soil and escape the zone of disturbance activity, meaning greater rates of N-fixation, (Reinecke and Visser; 1980). Gerard and Hay are found in casts when compared with soil (1979) reported 93 earthworms per square (Simek and Pizl, 1989). meter in normally plowed plots, including A.

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 caliginosa, A. chlorotica, A. longa, and L. Organic mulches enhance earthworm habitat terrestris. Earthworm abundance increased in by moderating microclimate and supplying a plots that received disk cultivation, or no-till food source. In corn plots in Pennsylvania, treatment Earthworm abundance doubled in earthworms were most abundant in the fall in no-till soybeans as compared with plowing treatments that were not plowed before winter (Mackay and Kladivko, 1985). and where corn residues had been chopped and left as a mulch, regardless of whether the The major function of tillage is to decrease plots were organically or conventionally bulk density of soil and increase porosity, it managed (Werner and Dindal, 1990). only increases microporosity. Macropores, which may be of physical or biological origin Effects of agricultural pesticides on and which can play an important role in earthworms depend on the chemical used. conducting water rapidly into the soil, are Herbicides tend to have low toxicity for destroyed by tillage. For instance, a 67 earthworms, but can cause population percent decrease in the rate of infiltration after reductions by decreasing organic matter input plowing a tropical forest soil was attributed to and cover from weed plants. Fungicides and the destruction of earthworm burrows. fumigants tend to be very toxic to earthworms. Application methods may have Infiltration in an adjacent arable soil, which unique effects on ecological groups of soil was initially much lower than in the forest animals. For instance, the fungicide benomyl soil, increased by 23 percent after plowing caused reductions of field populations of because the surface crust was broken (Aina, earthworms. Anecics such as L. terrestriswere 1984). Infiltration increases in cropped soils most susceptible to surface applications, and when an organic mulch is added in the fall, were less affected by incorporation of the due to the increased activities of earthworms pesticide into the soil. Because L. terrestris in these soils and the production of forms permanent burrows, it does not come macropores (Slater and Hopp, 1947). Soil into contact with subsurface soil beyond its compaction caused by agricultural traffic can burrow. However; endogeic species such as also decrease earthworm populations A. caliginosa, which continuously extend (Bostrom, 1986). their burrows as they feed in the subsurface soil, were most susceptible when benomyl A study in Denmark found that 200 T/ha of was incorporated (Edwards and Brown, manure was optimal for increased earthworm 1982). abundance and biomass (Andersen, 1980). L. terrestris, A. longa, and A. caliginosa were Enhancing earthworm populations increased by manure, while A. rosea and A. chlorotica were not influenced The There are many creative ways in which a Rothamsted Experiment Station plots in farmer can manage for earthworms. A first England which received manure for 118 years step might be to determine what earthworm also had increased earthworm abundance, and ecotypes are present, and how abundant they inorganic fertilizers in this case caused are. Endogeic species are most commonly decreases in earthworm populations (Edwards found. These are useful, but a mixed and Lofty, 1974). Heavy applications of community including anecic species as well inorganic fertilizers may cause immediate would be even more beneficial, especially for reductions in earthworm abundance incorporation of surface matter. Direct (Edwards, 1983). inoculation is one possible method, but

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 transferring blocks of soil (one cubic foot field. Rate of spread would vary with species each) from an area with a large earthworm and conditions in the field. Lumbricus population into a farm soil might work better. terrestris is capable of travelling at least 19 It is also important to consider what species meters on the soil surface in the course of one should be introduced, and this is where evening foray (Mather and Christensen, research specific to seasonally-dry climates in 1988). This is a long term process for California is needed. Much of our knowledge establishing earthworms, and would only be about earthworms concerns species of one successful if ample organic matter was family, the Lumbricidae, which are native to supplied to the soil where earthworms were moist temperate areas of Europe. The spread being introduced, and if physical and of these earthworms has paralleled European chemical disturbances of the soil were colonialism around the world. They are the minimized. Organically managed perennial only earthworms present in the northeastern crops would be ideal for this method. US and Canada, where glaciation killed the native fauna. In areas that have a native Future challenges in earthworm research earthworm fauna, lumbricids often dominate and implications in disturbed habitats. Morphologically, lumbricids are more muscular than any other Earthworms play an important role in soil family of earthworms, suggesting a greater processes and affect ecosystem services capacity for burrowing (Hartenstein, 1986). essential for human well-being (Skubala, 2013). These organisms have significant The earthworm fauna in California includes ecological functions in areas with agricultural some native species, lumbricid immigrants, as land use, but their existence is very sensitive well as immigrants from Asia and South to disturbances caused by anthropogenic America. From limited personal observations, activities that threaten biodiversity. The the lumbricids found in California agricultural impact of earthworm diversity and reduction soils tend to have small populations that are of environmental services on agricultural active for relatively short periods during the productivity has been frequently discussed at wet season. This may reflect agricultural various stakeholder levels, but serious actions management practices as well as climate have not been undertaken before (Van effects. There may be species that are adapted Noordwijk and Swift, 1999). That is because to seasonally-dry climates that would flourish the level of public understanding of benefits in California agricultural soils, if provided the provided by biodiversity is still inadequate proper conditions. (Van Noordwijk and Hairiah, 2006). The important role of the earthworm biodiversity One management idea for introducing desired in environmental services and human well- species is to set aside a small area of land on a being needs to be disseminated to all parties. farm to be managed exclusively as an Quantitative data showing the evidence of earthworm reservoir. If needed, the soil could earthworms role in ecological services and be limed to bring it near pH 7, fertilized, and their benefits to human well-being need to be a cover crop established and cut periodically communicated to public. to provide an organic mulch as food and physical cover. In this area a community of Dissemination of knowledge on earthworm the desired species could be established and diversity conservation to farmers needs to be built up. From this reservoir blocks could prioritized because they are the direct “actors” periodically be taken and introduced into the in agricultural activities. The level of farmers'

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Int.J.Curr.Microbiol.App.Sci (2018) 7(10): 1065-1086 knowledge about earthworms and their is necessary for earthworm experts to train benefits in agricultural land varies depending inexperienced earthworm taxonomists. Thus, on gender, education level, and age of farmers comprehensive earthworm identification keys (Zúñiga et al., 2013). Such scientific that can be used worldwide need to be made knowledge on the importance of earthworm available. Influence of earthworms on soil diversity in soils needs to be imparted in processes and ecosystem services is the result languages easily understood by farmers. The of not only earthworm activities but also entry point of communication between earthworm interaction with other organisms scientists and farmers is to obtain local and environmental factors related to human knowledge that farmers have about activities. Hence, future research should be earthworms. For examples, what is their directed to study the relationships between perception of earthworms in their land, how earthworms, other factors in order to improve many types of earthworms farmers observe, ecosystems services beneficial to human whether earthworms have a different roles, welfare. A good understanding of species where they prefer to live in deep soil, and performance within different functional what are their characteristics. Such questions groups in relation to environmental services is can be used by scientists to determine what necessary to develop land management farmers know about earthworms. This practices having a positive impact on knowledge can be used to develop proposals environmental services. for earthworm diversity conservation and rural development. Agricultural management practices oriented to sustainable production, such as reduced Not all earthworms have the same function in tillage, minimum tillage, legume cover crop, soil processes. Which species plays an mixed farming, and green manuring, should important role in ecosystems services? How be applied to soil biota. The quality of soil many ecosystem services can be restored and must be preserved or restored if it provides how? Studies on earthworm diversity are crucial services, such as nutrient cycling, indispensable. The study of key species and water, air, and supports biodiversity. redundancy of ecosystem processes are necessary. Understanding the mechanisms Acknowledgement underlying the survival of earthworm species in agroecosystems and protected areas can Present attempt on “Ecosystem Services of help to develop biodiversity conservation the Eco-engineers: the Earthworms” is the strategies (Zúñiga et al., 2013). Diversity of part of Environmental Science Project for S. earthworms is highly sensitive to land use Y. B. Sc. (Academic Year: 2018 – 2019) changes and human activities. The estimation submitted by Mansi Ramesh Das; Amruta of earthworm species richness, abundance, Chandrakant Nimbalkar and Samiksha Sunil and biomass represents the potential tool to Pisal to Savitribai Phule Pune University, evaluating land management practices and Pune through Science Association, Shardabai soil ecosystem services. Pawar Mahila Mahavidyalaya, Shardanagar. Authors are highly grateful to Agriculture What questions scientific research should Development Trust, Shardanagar (Baramati) address to achieve an accurate estimation of for valuable help, providing facilities at the earthworm diversity threats and essential Malegaon sheti farm & laboratory facilities at ecosystem services? To study the diversity of Shardabai Pawar Mahila College to carry out earthworms in different parts of the world, it the experimentations.

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How to cite this article:

Mansi Ramesh Das, Amruta Chandrakant Nimbalkar, Samiksha Sunil Pisal and Vitthalrao B. Khyade. 2018. Ecosystem Services of the Eco-Engineers: The Earthworms. Int.J.Curr.Microbiol.App.Sci. 7(10): 1065-1086. doi: https://doi.org/10.20546/ijcmas.2018.710.118

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