Reviews in Agricultural Science, 3: 25-35, 2015.
doi: 10.7831/ras.3.25

EARTHWORM DIVERSITY AND ECOSYSTEM SERVICES UNDER THREAT

Widyatmani S Dewi1, Masateru Senge2


1 Faculty of Agriculture, Sebelas Maret University, Jl. Ir. Sutami No.36A, Kentingan, Surakarta, Indonesia 57126

2 Faculty of Applied Biological Sciences, Gifu University, Yanagido 1-1, Gifu 501-1193, Japan

(Received: October 24, 2014. Accepted: May 7, 2015. Published online: June 30, 2015)

 

ABSTRACT

Biodiversity affects human well-being and represents an essential determinant of ecosystem stability. However, the importance of below-ground biodiversity, and earthworm biodiversity in particular, has not received much attention. Earthworms represent the most important group of soil macrofauna. They play a crucial role in various biological processes in soil, and affect ecosystem services such as soil health and productivity, water regulation, restoration of degraded lands, and the balance of greenhouse gases. Anthropogenic activities can lead to a rapid reduction or loss of earthworm diversity, and threaten ecosystem services as well as human well-being. Therefore, conservation of earthworm diversity should receive urgent attention. Farmers need to be made aware of the importance of earthworm diversity conservation and its benefits. Local ecological knowledge is required for communication between scientists and farmers; moreover, efficient strategies for earthworm diversity conservation need to be developed. This paper 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.

Keywords:Earthworm, Diversity, Ecosystem services, Threat

Introduction

Biodiversity loss has become one of the leading global issues, with a rapid loss of biodiversity reported worldwide. The rate of species loss is predicted to increase considerably over the next 50 years. Biodiversity is classified into above-ground biodiversity and below-ground biodiversity (soil biodiversity) that mutually interact (Wardle, 2002; Wardle et al., 2004). Functioning of terrestrial ecosystems greatly depends on below-ground biodiversity. Soil biodiversity is vital to humans as it supports a wide range of ecosystem processes, functions, and services (Costanza et al., 1997; Blouin et al., 2013; Skubala, 2013; Jouquet et al., 2014). However, the importance of below-ground biodiversity has often been ignored or undervalued (Secretariat of the Convention on Biological Diversity, 2010). Soil biodiversity in many areas worldwide has already been declining (Jeffery and Gardi, 2010). Furthermore, biodiversity loss results in the decline of ecosystem resilience. When elements of biodiversity are lost or threatened, ecosystem services degrade (Black et al., 2003). Ecosystems with heterogeneous biodiversity tend to be more stable, whereas those with homogeneous biodiversity are often more vulnerable to environmental stress (Hunter Jr., 1999). Healthy soil biodiversity provides a number of natural services that are useful to human being.
     Ecosystem services are defined as contributions of ecosystem structure and functions, in combination with other inputs, to human well-being. Essentially, these are services provided by biodiversity that link the functioning of ecosystems to their benefit extended to humans. Ecosystem processes are the changes or reactions occurring in an ecosystem, such as, for instance, biophysical processes (decomposition, production, nutrient cycling, energy, and nutrient fluxes) (Crossman et al., 2013). Ecosystem functions occupy an intermediate position between ecosystems processes and services. Ecosystem function can be defined as the capacity of ecosystem to provide goods and services that satisfy human needs, both directly and indirectly (de Groot et al., 2002); these functions affect ecosystem services (Jouquet et al., 2014). Ecosystems services were estimated to account to up to U.S. $33 trillion dollars per year of human capital equivalent. Soil biota contributes to approximately 38% of this amount (Skubala, 2013). The rapid growth of human population leads to increased pressure on soil. Anthropogenic activities accelerate the loss of biodiversity and ecosystem services in soil. Currently, approximately 60% of ecosystem services is degraded because soil is not used in a sustainable manner (Skubala, 2013).
     Earthworms represent an important soil faunal group that is distributed worldwide. Earthworm populations contribute to approximately 40-90% of soil macrofaunal biomass and 8% of total soil biomass in many ecosystems (Sinha et al., 2013). However, in intensively cultivated annual crops earthworms have lower contribution to total soil biomass (Fragoso et al., 1999; Tondoh et al., 2007; Blouin et al., 2013). Earthworms are the most valuable animals that influence the functioning of soil ecosystems (Hendrix and Bohlen 2002; Gonzales et al., 2006). Earthworms increase soil bulk density, pore size, water infiltration rate, soil water content, and water holding capacity. They also increase litter decomposition, soil organic matter dynamics, nutrient cycles, promote plant growth and reduce some soil-borne diseases (Brusaard, 1997; Chandran et al., 2012; Elmer, 2012). Earthworms produce organo-mineral biogenic structures (Lavelle, 2000), and influence gaseous composition of the atmosphere (Kibblewhite et al., 2008). Earthworms are also involved in restoring ecosystem services via direct and indirect mechanisms (Jouquet et al., 2014), especially in the situations when soil is degraded or land is under rehabilitation after mining (Boyer and Wratten, 2010). Earthworms represent an essential component of soil nutrient cycling (Lavelle and Spain, 2001). They maintain good soil health through the comminution of organic debris, enhance microbial activity, and contribute to the increase of nutrient availability in soil and mineral absorption by plants. Burrowing and grazing activity of earthworms modifies the soil structure and its capacity to absorb water. These advantages increase crop productivity. Earthworms represent a unique indicator of soil health (Science for Environment Policy, 2009; Elmer, 2012), and a good bio-indicator of degraded land due to anthropogenic activities (Tondoh et al., 2007). Earthworm diversity is a key determinant of ecosystem stability that is responsible for the provision of many ecosystem services (Eisenhauer and Schädler 2011; Blouin et al., 2013).
     Earthworm communities consist of many different species, and each plays a unique role in soil processes. To understand the function of earthworms in soil ecosystems, first the species valuable to ecosystem services should be identified. Research on earthworm species diversity has been carried out, but only in a limited number of geographical regions. According to a previous study, less than 50% of earthworm species in the world have been described (Brown et al., 2003). The knowledge of earthworm species diversity is still limited in many countries (Brown et al., 2006), and especially in tropics (Suthar, 2011; Chandran et al., 2012). Moreover, earthworm diversity studies have mostly focused on taxonomy and have not evaluated the association with ecosystem services. Soil systems provide an excellent basis to investigate the relationship between earthworm diversity and ecosystem functioning (Lavelle, 2000). A clear understanding of the relationships between earthworm diversity and ecosystem services is required to evaluate the influence of anthropogenic activities on ecosystems, and to develop management strategies aiming to preserve earthworm diversity.
     Five forces are considered to accelerate the decline of earthworm diversity: (1) soil degradation and habitat loss, (2) climate change, (3) excessive nutrient and other forms of contamination load, (4) over-exploitation and unsustainable management of soil, and (5) invasive species (Moore, 2005; Secretariat of the Convention on Biological Diversity, 2010). Global increase in human population and demand for resources has led conversion of forests to agricultural or urban land worldwide. This largely contributes to the decrease and loss of earthworm biodiversity. Habitat loss and soil degradation, caused by agricultural activities and unsustainable forest management, represent the greatest pressure on earthworm diversity. Some researchers have reported that earthworm diversity has been reduced, and some native species have been lost, because of forest conversion to agriculture and presence of invasive species. Such species loss results in negative impacts on ecosystem services (Dewi et al., 2006; Loss et al., 2012; Hairiah et al., 2014).
     Soils represent the main habitat for earthworms. However, many soils undergo degradation processes (Lavelle et al., 2006; Lavelle, 2009), thereby endangering earthworm diversity. Soil degradation is one of the most dangerous threats to earthworm diversity in this century that should receive more attention around the world (Skubala, 2013). Understanding how earthworm species adapt to disturbances and survive in agriculture soils can help to develop strategies to earthworm biodiversity conservation. Moreover, the importance of earthworm diversity to ecosystem services and human well-being needs to be communicated to different stakeholders, including farmers. Local ecological knowledge can be used to facilitate the communication between farmers and scientists (Zúñiga et al., 2013).

Earthworm and Ecosystem Services

Earthworms are soil inhabitants. However, different earthworm species have different feeding and living preferences, as well as burrowing behaviors. Hence, earthworms species show different ecological functions. They can be classified into epigeic, endogeic, and anecic species (Fragoso and Lavelle, 1995; Fragoso et al., 1997; Brusaard, 1997). Epigeic earthworms eat and live on rich litter surface layer and do not form burrows; they have small size body (5-15 cm body length at maturity), and bright color (Jones, 2003). Epigeic species play an important role in litter comminution and decomposition of organic material at the soil surface that increase nutrient transformation and stimulate activity of microorganisms. Anecic species live in sub-vertical burrows in the mineral soil, feed on fresh litter from surface soil and bring it into the soil profile (Fragoso et al., 1997); these worms are colored on the dorsal side and often have a large size body (15-20 cm) (Keith and Robinson, 2012). Anecic earthworms can burrow into the deeper layers of the soil, and reach depth of 1-2 m. Their feeding activity modifies the soil structure through the creation of vertical burrows and increases macro-porosities, aeration, and water infiltration into the deeper soil. Anecic burrow entrances called “midden” that are surrounded by a mound of cast material and usually crowned with fragmented plant litter. Anecic earthworms also affect litter breakdown rate and nutrient cycling by combining surface litter into the soil profile. Endogeic earthworms are living and feeding in the soil, so they are considered soil feeders. They play a key role in soil aggregate formation. Endogeic species have a body size of approximately 5-10 cm and are usually not pigmented. Their activity creates a network of horizontal branching burrows, which increase porosity, and release nutrients from their feces (Jones, 2003). Inoculation of endogeic earthworm Pontoscolex corethrurus in agroforestry mesocosms increased mean weight diameter, C and N storage in large macro-aggregates (>2000 μm) (Keith and Robinson, 2012). Soil ecosystems inhabited by epigeic, endogeic, and anecic earthworms have better physical, chemical, and biological properties than other ecosystems inhabited by only one or two levels of earthworm functional groups. Moreover, the presence of different earthworm functional groups in soil has a positive effect on ecosystem services. The summary of relationships between earthworm functional groups, soil processes and ecosystems services is shown in Figure 1.


Fig.1. Diagrammatic outline of the relationships among earthworm functional groups, soil processes, and ecosystem services (Modified from Keith and Robinson, 2012). The width of arrows represents the relative significance.


In addition to the earthworm classification based on functional groups, earthworms can be classified based on biogeography, into native species and exotic species. Native species of earthworms evolve in the given site or region (Fragoso et al., 1999). Such earthworm species usually live in one region, in contrast to species that have been introduced by human activity. Exotic or introduced earthworm species are those earthworm species that have been transported to areas where these species do not live naturally, either on purpose or by accident. Most research has focused on this group of earthworms.
     Earthworm life is influenced by the availability of suitable food, soil moisture, soil temperature, oxygen exchange, soil texture, soil pH, and presence of predators (Edward and Lofty, 1977; Lee, 1985). Earthworms like moist soil, because the water protection mechanisms in their bodies are not well developed. Respiration rate depends on the gas diffusion through the body wall, which must always be moist. Earthworms can survive in a range of soil temperatures varying between 0°C and 35°C (Lee, 1985). The optimum soil water content varies considerably depending on the species and ecological group earthworm belongs to, that can differ even within the same species, depending on its ability to adapt to local environmental conditions (Lee, 1985). Earthworms are most active in moist soil conditions (Lee, 1985; Lavelle and Spain, 2001). The earthworm community structure is controlled by the nutrient content of soil and the amount of seasonal rainfall (Fragoso and Lavelle, 1995).
     The main food source for earthworms is decaying organic waste (Lee, 1985). Earthworms prefer decomposed organic food larger than 50 µm in size (Lavelle et al., 2001). Because of the limited movement capability, earthworms like to live close to source of the food source. Population density and distribution of earthworms in forest ecosystems is strongly influenced by the quantity, quality, and timing of litter inputs to the soil system. The high content of polyphenols and other secondary compounds in litter affects the density of earthworms in tropical forests (Fragoso and Lavelle, 1995). Epigeic earthworms prefer high-quality litter soil layer (Tian, 1992; Lavelle and Spain, 2001).
     Earthworm communities are also influenced by biological processes occurring within the soil environment. Earthworms develop various interactions with microflora (bacteria, fungi), microfauna (protozoa and nematodes), and other macrofauna groups (ants in particular) (Wardle, 2002). Digestion in earthworms is mediated by the enzyme mixture produced by the intestinal wall, and the microflora and microfauna in earthworms guts (Lavelle and Spain, 2001). Earthworm life is also affected by predators, and especially birds (Lee, 1985).
     Ecosystem services provided by earthworms relate to the effects of earthworm activity on soil systems (Moreira et al., 2008). Earthworms play an important role in soil ecosystem functioning and human welfare (Hendrix and Bohlen, 2002; Gonzales et al., 2006; Ernst and Emmerling, 2009; Science for Environment Policy, 2009). Earthworm diversity plays an important role in agricultural systems and is an integral part of soil health and fertility. Earthworms consume decomposable organic matter and break it down into smaller pieces providing food to almost all soil microorganisms. Their excrements or “casting” supports highly diverse microbial communities, including beneficial fungi and bacteria (Elmer, 2012). As a result of microbial activity, availability of nutrients to plants also enhances. Earthworms also provide benefits to farmers. Earthworms contribute to the improvement of plant resistance to pests and indirectly suppress soil-borne diseases. As a result, crop productivity improves (Ernst and Emmerling, 2009).
     Earthworms have been called “ecosystem engineers.” They are capable of modifying their physical environment by mixing soil layers from the bottom to the top and vice versa incorporating organic matter into the soil and producing biogenic structures. This way, earthworms change the structure of the soil. Different types of earthworms' functional groups can create horizontal and vertical tunnels, which can be quite deep in soil. These tunnels form pores that facilitate oxygen and carbon dioxide exchange, and allow water penetration into the soil. Thus, water, gas and solute transfer processes and soil water holding capacity improve (Capowiez et al., 2001). Earthworms' burrows serve as soil macro-porosities (Lal, 1991; Brusaard et al., 1993; Jimenez et al., 1998; Stott et al., 1999; Lavelle et al., 2001). Soil porosity is crucial property because it determines: (1) rate of water infiltration, (2) water holding capacity, (3) the drainage of water excess, (4) soil moisture, and (5) the exchange rate of CO2 from soil to atmosphere and vice versa (Wolf and Snyder, 2003). The disruption of earthworm diversity impedes water infiltration into the soil thus resulting in increased surface run-off, erosion, flooding, and drought.
     Earthworm casts (earthworms' feces) are also crucial to the structure of soils. Earthworm activity has a positive impact on the formation of soil structure, through the improvement of infiltration rate, water absorption, and soil resistance against the erosive of rainfall and surface run-off (Glinski and Lipiec, 1990; Stott et al., 1999). Earthworms make continuous channels from the soil surface to the deeper layers, so that water can infiltrate quickly into the subsoil. Therefore, the soil with higher earthworm activity has better infiltration rate than soil without or with small earthworm community. Hence, earthworm activity reduces the risks of run-off and waterlogging.
     In addition to these indirect advantages, earthworms also directly benefit humans, being for example a food source for fish (and used as a fish bait), and being part of vermicomposting. Some Amerindian communities in South America utilize earthworm as a source of seasonal food and an essential source of protein in their diet (Keith and Robinson, 2012). Earthworms contribute up to €723 million per year in terms of the livestock product value (Bullock et al., 2008).
     Earthworms, like all other organisms, have certain advantages and disadvantages. Some species of earthworms were reported to have adverse impacts on soil structure (Lal, 1991; Blanchart et al., 1999). Small-sized endogeic earthworms, a “de-compacting species, ” eat castings produced by large-sized endogeic earthworms (compacting species), so that the organic matter content of the casting decreased. Casting with lower organic matter will be broken easily by raindrops, resulting the compacted soil. Fresh earthworm casting is soft and fragile, and vulnerable to raindrops, but it becomes harder, and more resistant to water and wind erosion with time. Effect of compacting species on soil structure is strongly influenced by the presence of organic debris on the soil surface. Blanchart et al. (1999) reported that activity of Pontoscolex corethrurus (compacting species) in agroecosystems with low soil organic matter in Yurimaguas (Peru) leads to hardening of soil surface that inhibits the infiltration. However, in the soil with high organic matter content or soil mulched with legumes, earthworms enhance soil macro-aggregate development. Lavelle (2000) also reported that P. corethrurus invaded a pasture in Central Amazonia, and produced an excessive amount of unstable large cast. This cast formed 5 cm impermeable crust inhibiting plant growth. Soils with low organic matter and low earthworm diversity and abundance s tend to be more sensitive to erosion than soils with high earthworm population and diversity (Lal, 1991). Management of soil organic matter is keys factor affecting the ecosystem services performed by earthworms.
     Earthworms play an important role in determining the greenhouse-gas balance of soils worldwide. Whether earthworms represent a “sink” or “source” of greenhouse gas remains highly debated. Earthworms cast is stable soil aggregate, is recognized as a “sink”. It stimulates carbon sequestration and enhances long-term protection of C in soil. However, earthworms can accelerate the decomposition of C by microorganisms in the soil and thus enhance CO2 emission or as “source” of greenhouse gas (Simek and Pizl 2010). Earthworm gut is ideal environment for denitrifying bacteria as it is anaerobic microsite enriched by available carbon, nitrogen, with favorable moisture level, essential for stimulating activity of denitrifiers and high potential to increase N2O emission. Earthworms activity in fertilized grasslands enhances grass N uptake. However, earthworms, and epigeic earthworm species (Lumbricus rubellus) in particular, may also have side effects in ecosystems, and increase N2O emissions by 10%(Lubbers et al., 2011, Lubbers et al., 2013). Based on the meta-analysis using 237 observations of 57 articles published on the ISI-Web of Science between 1990 and 2011, it can be concluded that earthworms increased 33% and 42% of CO2 and N2O emissions, respectively. These effects depend on some controlling factors, such as earthworm functional groups, population size, experimental period, experiment type, nutrient input, soil organic matter content, C/N ratio of soil, and type of ecosystem. Over a longer period (> 30 days), earthworms tend to increase N2O emissions, but decrease CO2 emission. Increase of N2O emissions by earthworms correlates to the increase of organic C input as well as to the height of soil organic matter layer having low C/N ratio (Lubbers et al., 2013). This conclusion was mainly derived based on laboratory experiments and only one article based on field experiments. Moreover, most experiments can only be conducted during less than 200 days. Hence, the effect of earthworms on greenhouse gas balance is still unclear and needs further understanding.
     The use of biochar in agricultural practices potentially reduces N2O emissions produced by earthworms (Asuming-Brempong and Nyalemegbe, 2014). Biochar or charcoal has a porous physical structure, and thus increases oxygen diffusion into the soil and creates aerobic conditions providing a suitable habitat for aerobic soil microorganisms, and potentially reducing the activity of anaerobic denitrifying bacteria. The polycyclic aromatic structure of biochar makes it chemically and biologically stable, allowing it to persist in soil for centuries. Biochar decreases N2O emissions since N2O emissions are enhanced by high soil organic matter content. Endogeic earthworms, P. corethrurus, can grind the biochar and reject it in their casts, which affect biochar distribution in the soil profile. Agricultural management, such as tillage and fertilization with N fertilizers in particular, plays a significant role in greenhouse gas emission by influencing soil microenvironment (Plaza-Bonilla et al., 2014). Earthworms and biochar application on soil is one of the best technique to improve soil fertility and health (Asuming-Brempong and Nyalemegbe, 2014). The best technology for sustainable management of land and water resources should maintain and protect earthworm abundance and diversity (Blanchart et al., 1999).

Earthworm Diversity under Threat

There are thousands of earthworms species with different biogeography. They have different morphological characteristics, although some of these characteristics are difficult to determine by naked eye. Earthworm species can be identified based on three complementary approaches: taxonomy, biogeography, and ecological functional groups. Each identification method has disadvantages. Therefore, identification of earthworm species should be done using more than one method. A taxonomic approach implies studying earthworm diversity based on the number and identity of different species (species richness), regardless of their ecological role. Taxonomic identity can be determined using conventional methods (observing internal and external morphological characteristics), or by advanced molecular genetics and genomic analysis techniques (Dupon, 2009; Chang and James, 2011). However, molecular techniques have been rarely applied in earthworm research (Dupon, 2009). The disadvantage of identification based on external morphological characteristics is that this way immature earthworms cannot be identified. However, identification based on internal morphological characteristics is quite difficult, especially for beginners. Molecular methods are more promising but involve high costs, and not affordable to everyone. Systematics of earthworms still faces many problems and is not complete (Fragoso et al., 1999; Jones, 2003). General identification keys for tropical and subtropical earthworm species are not available and still need to be developed. Currently, there are only few professional taxonomists in the world. Hence basic training on earthworm species identification has to be undertaken by new taxonomists (Brown et al., 2013). The difficulties in identifying earthworm species can inhibit researcher's interest to become an earthworm taxonomy expert.
     Based on the taxonomic identification, earthworms belong to phylum Annelida, sub-phylum Clitellata, and class Oligochaeta that consists of 20 families, 693 genera, and more than 6000 species. Currently, 3627 species have been described (Giller et al., 1997; Fragoso et al., 1997; Lavelle and Spain, 2001). It was estimated that less than 50% of species exist worldwide (Fragoso et al., 1997) and only a few dozen have been studied extensively (Brown et al., 2003). Earthworm species are found mainly in tropics, but most of the tropical regions, such as Southeast Asia, Africa, and South America have not been widely surveyed for earthworm diversity (Jones, 2003). In Indonesia, the research on earthworm diversity is still limited and receives little attention. Despite the high importance of earthworms that were introduced in Indonesia by Darwin in 1938 and many ecological researches in the following years, more research on ecosystems services provided by earthworms is still needed (Brown et al., 2003). Identification of earthworms based on ecological functional groups is an important goal in soil ecology (Keith and Robinson, 2012), and a big challenge for earthworms taxonomists (Giller et al., 1997).
     Patterns of earthworm distribution and species richness were described to be directly related to biogeography, local microclimate and human activities (Suthar 2011). Earthworm species of family Megascolecidae were found in many tropical regions in East and Southeast Asia, and Australia (Edward and Lofty, 1977; Lee, 1985; Jones, 2003; Fragoso and Csuzdi, 2004). Species from family Glossoscolecidae are widespread in the regions of Central America, South and North, while species of family Ocnerodrilidae family are mainly found in India, Central and South America, and Africa. Earthworm species of family Acanthodrilidae are commonly found in India, Burma, New Zealand, and Australia (Fragoso and Csuzdi, 2004).
     Why is it essential to study the earthworm diversity? Earthworms represent an important group of soil macrofauna that provides ecosystem services for human well-being. At the same time, earthworms are very sensitive to anthropogenic activities. Earthworm diversity is important to study because the different ecological groups of earthworms play important role in soil processes and ecosystem services. Different species of earthworms are also characterized by different levels of sensitivity to habitat disruption, and are good indicators of land management practices. Estimation of earthworm species richness can help determine the redundancies and keystone species in ecosystem processes. Different earthworm species provide a various functions in different soil layers (Bullock et al., 2008). Earthworm diversity is clearly can be used as an estimate of ecosystem services (Keith and Robinson, 2012).
     Another important factor affecting earthworm diversity is environment variability, such as the amount and quality of nutrients and energy sources, seasonal changes, spatial differences in soil and, climate variability, and biotic interactions within the community (Breure, 2004).
     Soil management in agricultural ecosystems strongly influences earthworm diversity. Different management practices affect the habitat quality and the availability of substrate to earthworms, hence resulting the change in abundance and diversity of earthworms. Intensive soil tillage drastically reduces the earthworm populations, especially in areas where the land has been conversed to monoculture (Bullock et al., 2008). Habitat loss and soil degradation, caused by agriculture and unsustainable forest management create the biggest pressure on earthworm diversity. Some researchers have reported cases of earthworm diversity decrease and loss of native species as a result of forest conversion to agriculture. Forest conversion also increases invasive species domination that has a negative impact on ecosystem services (Dewi et al., 2006; Loss et al., 2012; Hairiah et al., 2014).
     Earthworms are sensitive to land use change, ecosystem perturbations, and rehabilitation (Tondoh et al., 2007). Human activities represent an important factor causing reduction of earthworm diversity. Global increase in human population and high demand for resources has led to the conversion of forests to agricultural land. Intensified agricultural management can lead to the decrease or loss of earthworm biodiversity. The USDA Forest Services International Programs reported that every year the world loses 14.6 million hectares (ha) of forest that is converted to agricultural or residential land. Although parts of forests have been used as estates, reforestation and natural forest extension, the world still loses 9.6 million ha of forest per year. Furthermore, the greatest conversion rates in the world are happening in tropics (USDA Forest Service International Programs, 2014). Forest conversion to agricultural and other types of land use leads to disruption of taxonomic and functional diversity, and loss of native earthworm species (Rao, 2013).
     There is a strong correlation between an increase in land use intensity and decrease in earthworm diversity. Forest conversion to coffee plantations and other agricultural land in Sumberjaya (West Lampung, Indonesia) led to reduction or loss of epigeic native earthworm species, such as Metaphire javanica. Subsequently, the population of small body-size endogeic-exotic earthworm species such as P. corethrurus increased but did not affect the population abundance (Table 1). Native species are more sensitive to land-use change than exotic species (Dewi et al., 2007). Previous studies have also shown that the body size of earthworms tends to be smaller in areas with more intensive land management (Figure 2) (Susilo et al., 2009). Earthworm abundance is higher in areas with more intensive management than in areas with less intensive management. This is especially true in areas with higher plant rotation and larger waste harvests left in the soil (Bullock et al., 2008). Similarly, the forest conversion to intensified agricultural land in Ivory Coast resulted in potential increase in relative abundance and biomass of earthworm species, particularly in areas with medium level intensification agriculture, as reported by Tondoh et al. (2007). These researchers found that some earthworms species were highly sensitive to land use changes, i.e., Dichogaster saliens Beddard 1893, Hyperiodrilus africanus Beddard 1891, Millsonia omodeoi Sims 1986, Dichogaster baeri Sciacchitano 1952, Dichogaster ehrhardti Michaelsen 1898, Agastrodrilus sp., Stuhlmannia palustris Omodeo and Vaillaud 1967 and, to some extent, Millsonia sp. (Tondoh et al., 2007).


Table 1 Earthworm diversity, abundance and estimate of individual size after forest conversion to agriculture land uses in Sumberjaya, West Lampung, Indonesia (Dewi et al., 2007; *Susilo et al., 2009)


Fig.2. The relationship between earthworm body size and land use intensity (Modified from Susilo et al., 2009).


The loss of biodiversity is likely linked to the reduction of ecosystem services provided by the biota in a given soil system (Jeffery and Gardi, 2010). There is a strong relationship between earthworm biodiversity changes and soil processes in forest conversion area in Sumberjaya. Changes in earthworm diversity lead to a decrease of soil macropores (Dewi et al., 2007), which can inhibit the infiltration rate and increase the potential of run-off and erosion. The changes in earthworm functional group composition were shown to be correlated to changes in microclimate and soil physicochemical characteristics in land use areas, such as surface litter thickness, temperature and soil moisture, and soil organic carbon and organic N content (Hairiah et al., 2014).
     Intensive agricultural land use has also been reported to reduce the diversity and abundance of earthworms, and significantly alter soil ecosystem processes and services in Europe (De Vries et al., 2013). The study focusing on agricultural intensification at 60 places of four European countries with different climate and soil types showed that areas with highly intensive land management have lower diversity and biomass of soil organisms including earthworms than areas with lower agricultural intensity (De Vries et al., 2013). The decline of earthworm biomass was correlated to the disturbance of plant roots systems caused by intensive land use and tillage practices. These processes had an impact on carbon and nitrogen cycles in the environment (De Vries et al., 2013).
     Invasive species induce a negative impact on native earthworm species s and ecosystem services provided by earthworms. Invasion of exotic earthworms (Lumbricide) to North America forests caused decline of ground-nesting songbirds (Seiurus aurocapilla) population, especially in maple-basswood (Tilia americana) forests (Loss et al., 2012). The invasive species of the New Zealand flatworms (Arthurdendyus triangulatus) were reported to considerably reduce the diversity of earthworm communities in the United Kingdom. These species also reduce around 12% of earthworm populations in some agricultural fields in Scotland (Jeffery and Gardi, 2010). Climate change has the potential to reduce earthworm diversity; however, more quantitative data is needed to support this conclusion.
     Earthworm diversity is a potential bio-indicator of land use change and land management intensity. Hence, to prevent ecosystem degradation, further research is needed to understand which earthworm species are more sensitive to land use changes. With the continued decline in the abundance of many earthworm species, the Secretariat of the Convention on Biological Diversity (2010) has promoted conservation of earthworm species diversity through restoring, maintaining, or inhibiting the population decline of selected earthworm species. The coherent approach to soil protection is now under development.

Future Challenges in Earthworm Research and Implications

Earthworms play an important role in soil processes and affect ecosystem services essential for human well-being (Skubala, 2013). These organisms have significant ecological functions in areas with agricultural land use, but their existence is very sensitive to disturbances caused by anthropogenic activities that threaten biodiversity. The impact of earthworm diversity and reduction of environmental services on agricultural productivity has been frequently discussed at various stakeholder levels, but serious actions have not been undertaken before (Van Noordwijk and Swift, 1999). That is because the level of public understanding of benefits provided by biodiversity is still inadequate (Van Noordwijk and Hairiah, 2006). The important role of the earthworm biodiversity in environmental services and human well-being needs to be disseminated to all parties. Quantitative data showing the evidence of earthworms role i ecological services and their benefits to human well-being need to be communicated to public.
     Dissemination of knowledge on earthworm diversity conservation to farmers needs to be prioritized because they are the direct “actors” in agricultural activities. The level of farmers' knowledge about earthworms and their benefits in agricultural land varies depending on gender, education level, and age of farmers (Zúñiga et al., 2013). Such scientific knowledge on the importance of earthworm diversity in soils needs to be imparted in languages easily understood by farmers. The entry point of communication between scientists and farmers is to obtain local knowledge that farmers have about earthworms. For examples, what is their perception of earthworms in their land, how many types of earthworms farmers observe, whether earthworms have a different roles, where they prefer to live in deep soil, and what are their characteristics. Such questions can be used by scientists to determine what farmers know about earthworms. This knowledge can be used to develop proposals for earthworm diversity conservation and rural development.
     Not all earthworms have the same function in soil processes. Which species plays an important role in ecosystems services? How many ecosystem services can be restored and how? Studies on earthworm diversity are indispensable. The study of key species and redundancy of ecosystem processes are necessary. Understanding the mechanisms underlying the survival of earthworm species in agroecosystems and protected areas can help to develop biodiversity conservation strategies (Zúñiga et al., 2013). Diversity of earthworms is highly sensitive to land use changes and human activities. The estimation of earthworm species richness, abundance, and biomass represents the potential tool to evaluating land management practices and soil ecosystem services.
     What questions scientific research should address to achieve an accurate estimation of earthworm diversity threats and essential ecosystem services? To study the diversity of earthworms in different parts of the world, it is necessary for earthworm experts to train inexperienced earthworm taxonomists. Thus, comprehensive earthworm identification keys that can be used worldwide need to be made available.
     Influence of earthworms on soil processes and ecosystem services is the result of not only earthworm activities but also earthworm interaction with other organisms and environmental factors related to human activities. Hence, future research should be directed to study the relationships between earthworms, other factors in order to improve ecosystems services beneficial to human welfare. A good understanding of species performance within different functional groups in relation to environmental services is necessary to develop land management practices having a positive impact on environmental services. Agricultural management practices oriented to sustainable production, such as reduced tillage, minimum tillage, legume cover crop, mixed farming, and green manuring, should be applied to soil biota. The quality of soil must be preserved or restored if it provides crucial services, such as nutrient cycling, water, air, and supports biodiversity.

Acknowledgement

The authors wish to acknowledge to the Directorate General of Higher Education of the Republic of Indonesia and the Japanese Society for the Promotion of Science (JSPS) for funding this paper. It is a part of a joint research project on water harvesting between Sebelas Maret University, Indonesia and Gifu University, Japan.

 

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