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Earthworm species in Musa spp. plantations in Brazil and worldwide
expand article infoMarcus Vinicius Cremonesi, Alessandra Santos, Danilo Eduardo Rozane§, Marie Luise Carolina Bartz|, George Gardner Brown
‡ Universidade Federal do Paraná, Curitiba, Brazil
§ Universidade Estadual Paulista Júlio de Mesquita Filho, Registro, Brazil
| University of Coimbra, Coimbra, Portugal
¶ Embrapa Forestry, Colombo, Brazil
Open Access

Abstract

Bananas and plantains are major commodity/food crops that represent an important habitat for earthworms, although so far, no review is available on earthworm communities associated with banana/plantain crops worldwide. The Vale do Ribeira region is among the largest banana producing areas in Brazil, but little is known of the earthworms living there. Hence, the present study assessed earthworm populations and species in three banana plantations and adjacent Atlantic forest fragments along the Ribeira de Iguape River using standard (hand sorting) methodologies. Furthermore, we review earthworm populations reported in banana/plantain plantations worldwide. Only two species (Pontoscolex corethrurus, Amynthas gracilis) belonging to two families (Rhinodrilidae, Megascolecidae) were found in the Ribeira River valley, occurring concurrently. Abundance was low (< 13 indiv. m-2) compared with other banana plantations worldwide, that frequently surpassed 100 indiv. m-2. More than 70 studies reported earthworms from >200 banana plantations in 28 countries, and mean species richness was 2.7 per site, ranging from 1 to 10 species. Exotics predominated in most sites and P. corethrurus was the most prevalent species encountered. Overall, more than 104 species from 10 families were reported, with around 61 native and 43 exotic widespread species, mainly of the Megascolecidae, Lumbricidae and Acanthodrilidae families. Richness was highest in India (27 spp.) and the Canary Islands (25 spp.), but native species dominated only in a few countries and sites, while exotics were prevalent especially in island countries and Brazil. Lower-input practices appear to be important for earthworm communities and banana plantations can have large earthworm populations in some cases, which may be contributing to soil processes and plant production, topics that deserve further attention. However, many important banana-producing countries have not yet been evaluated, so further work is warranted, both in terms of applied ecology and biodiversity.

Keywords

Annelida, banana, biodiversity, Oligochaeta, plantain, Pontoscolex corethrurus

Introduction

Bananas and plantains are large, perennial herbs belonging to the genus Musa, that evolved in Indochina and Southeast Asia, but with major secondary diversification in Africa, India and the Caribbean (Price 1995). Bananas are a major commodity, occupying over 6 million ha (FAO 2018) and representing an important contribution to the economy of many developing countries worldwide (OECD/FAO 2019). Plantains resemble bananas, but are generally longer, have more starch and are mostly eaten cooked, rather than raw (like the bananas). They are a major staple crop in several African, Asian, Pacific, Latin American and Caribbean countries (Price 1995; Norgrove and Hauser 2014). In 2018, the six main banana producers (total production) were India, China, Indonesia, Brazil, Ecuador and the Philippines, while the six countries with the greatest surface area devoted to banana production were India (884,000 ha), Tanzania (490,701 ha), Philippines (484,247 ha), Rwanda (464,321 ha), Brazil (449,284 ha) and China (383,216 ha) (FAO 2018). India accounts for around 24% of global production and Brazil around 5% (FAO 2018), while the whole of Latin America and the Caribbean (LAC) region account for around 25% of the world’s banana production (OECD/FAO 2019).

Throughout much of LAC, bananas and plantains are still cultivated at the subsistence level, often in agroforestry systems (Harvey and Villalobos 2007; Malézieux et al. 2009; Paul et al. 2015; Coelho 2017; Garcia et al. 2017; Salazar-Díaz and Tixier 2017). However, commercial plantations are also widespread, occupying large monoculture areas, particularly in warmer, wetter regions of the tropics (Campbell 2018; Yahia 2019). In Brazil, most of the area devoted to banana cultivation lies within the Atlantic Rainforest biome, a highly threatened hotspot of biodiversity (Myers et al. 2000). In fact, much of the banana and plantain cultivation worldwide is performed in wetter tropical climates, and frequently close to rainforest ecosystems, where they may represent a potential hazard to biodiversity conservation. In commercial plantations, conventional production practices are adopted, including frequent herbicide use to control weeds, fumigation to control fungal diseases (particularly Fusarium and Pythium) and root nematode infestation, as well as Sigatoka (Marin et al. 2003; Cordeiro et al. 2004; Gasparotto et al. 2006), although some resistant varieties for the latter are already available (Timm et al. 2016; Dale et al. 2017). These practices may have important negative impacts on earthworm populations (da Silva et al. 2006; Baretta et al. 2011), despite the high amounts of litter inputs, which represent C (food) sources for soil biota, and protection from soil erosion (Lombardi Neto and Moldenhauer 1992). Worldwide, however, little is known of the soil biota inhabiting banana plantations, and so far, there has not been an overview of true soil-inhabiting animals in banana plantations worldwide.

Earthworms are essential service providers for terrestrial ecosystems (Lavelle et al. 2006). Their activity, generating galleries and casts, contributes to formation and maintenance of soil structure (Lavelle 1997; Capowiez et al. 2012), increasing porosity, infiltration and water retention (Fiuza et al. 2012), as well as re-distribution and breakdown of soil organic matter (Brown et al. 2000). However, earthworms are sensitive to land use and management, and can be used as soil quality and management as well as environmental bioindicators (Brown and Domínguez 2010; Bartz et al. 2013; Bünemann et al. 2018). Brazil is home to more than 300 described earthworm species (Brown et al. 2013), but practically nothing is known of the species and populations inhabiting banana plantations in the country.

The Vale do Ribeira region, located in northeastern Paraná State and southern São Paulo State, has extensive areas (over 36,000 hectares; ABAVAR 2015) devoted to banana cultivation (Bueno 2003). In this region, banana fields are normally surrounded by Atlantic forest fragments (Cordeiro et al. 2017), that have been reduced to around 12% of their original surface area (Ribeiro et al. 2009). Although frequently disturbed with various management practices, banana plantations are perennial crops that could provide adequate habitats for the establishment of native earthworm species, especially when Atlantic forest fragments occur surrounding banana cropping areas (Cordeiro et al. 2017). However, little is known about the effects of banana crops on abundance and diversity of earthworm species, and the occurrence of these invertebrates in Atlantic forest fragments in the Ribeira valley region. Furthermore, little is known of the presence of native and exotic earthworm species in banana and plantain fields worldwide. Hence, the present study was undertaken to assess earthworm populations in banana plantations and native forest fragments in the Ribeira de Iguape River valley in the State of São Paulo, and evaluate earthworm communities (abundance, biomass, species composition) associated with banana and plantain crops worldwide.

Material and methods

Study sites in the Ribeira de Iguape River valley

Three counties in the lower Ribeira River valley, all of them in the State of São Paulo were selected for this study: Eldorado, Sete Barras and Registro (Fig. 1). The climate in Sete Barras and Registro is rainy tropical (Af-type according to Köppen), with mean rainfall greater than 60 mm in the driest month. In Eldorado, climate is Köppen Am tropical, with rainfall less than 60 mm in the driest month. The average annual rainfall for all counties ranges from 1500 to 1600 mm (CEPAGRI 2018; CIIAGRO 2018), with the highest concentration of rains occurring from January to March. The mean annual temperature ranges from 23.9 to 24.3 °C, with the lowest temperature (13 °C) in July and highest (34.2 °C) in February. Soils in the valley originate from sedimentary, metabasic and amphibolic rocks (Oliveira et al. 2002), with high natural fertility (calcium, magnesium, potassium, and phosphorus content) and high organic matter levels, due to seasonal river floods that deposit alluvial material. Soil texture varies from loam to clay. The areas chosen in the three counties are characterized by smaller watersheds that flow into the Ribeira River with banana crops on the high ground level and Atlantic forest sites (control sites) in advanced stages of regeneration close to the Ribeira River. General characteristics of the areas are given in Table 1.

Figure 1. 

Location of the counties sampled in the Ribeira de Iguape River valley, São Paulo State, Brazil.

Table 1.

Land use system, watershed number (WN), age of the land use, geographic coordinates and soil types according to FAO classification (IUSS/WRB 2015) of the sites evaluated in each county of the Ribeira de Iguape River Valley, São Paulo, Brazil.

Site County System WN1 Age (yrs) Latitude, Longitude Soil types
1 Eldorado Banana 344 50 24°29'35"S, 48°02'10"W Cambisols
2 Eldorado Atlantic forest 344 > 50 24°30'09"S, 48°02'30"W Cambisols
3 Sete Barras Banana 422 15 24°23'34"S, 47°53'51"W Cambisols
4 Sete Barras Atlantic forest 422 > 50 24°23'30"S, 47°53'22"W Cambisols
5 Registro Banana 379 40 24°26'56"S, 47°49'41"W Cambisols / Histosols
6 Registro Atlantic forest 389 45 24°26'47"S, 47°49'23"W Cambisols / Histosols

Earthworm sampling

Earthworms were collected using an adaptation of the standard sampling method proposed by the Tropical Soil Biology and Fertility (TSBF) Programme (Anderson and Ingram 1993). In each area 10 samples (25 × 25 cm square to 20 cm depth) were taken, divided into 2 equally-numbered transects with samples every 20 m. Distance between transects was ca 10 m. Earthworms were hand-sorted from the soil in the field and fixed in 80% alcohol. In the laboratory, earthworms were identified to species or family level (juveniles) using taxonomic keys (Michaelsen 1900; Righi 1990; Blakemore 2002). The material was deposited in the Fritz Müller Oligochaete collection (COFM) at Embrapa Forestry in Colombo, Brazil. The earthworm data obtained were used to determine the total species abundances (no. individuals and fresh mass m-2) and richness, per site and land use (banana, forest).

Literature review

Both the common and scientific names of banana were used for a bibliographic search online using the keywords for bananas and plantains in English, Portuguese, French and Spanish: Musa (genus), Musa acuminata, Musa balbisiana, banana, banane, banano, plátano and plantain. These were then crossed with the common names of earthworms in these languages: earthworms, minhoca, oligochaeta, oligoqueta, vers de terre and lombriz de tierra. Online scientific databases Web of Science, Science Direct, Scielo, google academic and the Base de Dados de Teses e Dissertações (BDTD – Thesis and Dissertation Database) of Brazil were consulted. All the resulting publications were consulted and those containing data on earthworm abundance (density and/or biomass) or species identification were selected and these data extracted, as well as information on sampling sites (counties, countries, management practices of the plantations). Earthworm species were separated into different families and into native or exotic to the region of occurrence, and species richness per site and for each group (native, exotic), when available. Although we treated bananas and plantains separately when possible, for most of the analysis we considered them together, since not all publications provided details regarding the types of bananas cultivated, and even plantains are often called ‘bananas.’ Details on the species and management data obtained and presented in this paper are available for download online from the open access repository Mendeley Data at http://dx.doi.org/10.17632/p8ywsnj8c5.1 (Cremonesi et al. 2020).

Data treatment

Quantitative data on the earthworm abundance and biomass obtained from the literature and from the present study were treated as follows. Means of earthworm abundance (no. individuals m-2) and biomass (fresh mass in gm-2) were calculated per sampling site (plantation), using data from the present study. When quantitative data from the literature was available for the individual site, it was used as is. When only means for several plantations in the same general location were provided, these were also used. As the interest of the present study was more at the spatial (site-level) rather than the temporal scale, when samples were taken on multiple occasions, and individual means per sampling date were not available, overall means were used. When taken in wet and dry seasons, both values were used as an interval of abundance and biomass (when measured).

Results and discussion

Specimens examined from the Ribeira de Iguape River valley sites

Family Rhinodrilidae

Pontoscolex (Pontoscolex) corethrurus (Müller, 1857)

COFMBRSP0231, 1 individual in Atlantic Forest, HMN 389, Registro – SP (24°26'16.85"S, 47°49'31.71"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0232, 2 individuals in Atlantic Forest, HMN 389, Registro – SP (24°26'16.82"S, 47°49'31.71"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0233, 2 individuals in Atlantic Forest, HMN 389, Registro – SP (24°26'16.28"S, 47°49'32.52"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0235, 2 individuals in Atlantic Forest, HMN 389, Registro – SP (24°26'15.71"S, 47°49'33.32"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0236, 1 individual in Atlantic Forest, HMN 389, Registro – SP (24°26'14.57"S, 47°49'35.35"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0238, 2 individuals in banana field, HMN 379, Registro – SP (24°26'54.25"S, 47°49'38.12"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0239, 1 individual in banana field, HMN 379, Registro – SP (24°26'54.81"S, 47°49'39.41"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0240, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.43"S, 47°55'11.56"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0241, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.46"S, 47°55'11.49"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0242, 2 individuals in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'43.79"S, 47°55'24.53"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0244, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'43.93"S, 47°55'10.17"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0245, 3 individuals in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.33"S, 47°55'09.65"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0248, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.90"S, 47°55'08.92"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0249, 1 individual in banana field, HMN 422, Sete Barras – SP (24°23'38.61"S, 47°55'23.49"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0251, 1 individual in banana field, HMN 422, Sete Barras – SP (24°23'43.01"S, 47°55'24.52"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0252, 3 individuals in banana field, HMN 422, Sete Barras – SP (24°23'42.54"S, 47°55'25.32"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0253, 1 individual in Atlantic Forest, HMN 344, Eldorado – SP (24°29'57.34"S, 48°02'41.68"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0255, 1 individual in Atlantic Forest, HMN 344, Eldorado – SP (24°29'55.69"S, 48°02'42.15"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0256, 2 individuals in banana field, HMN 344, Eldorado – SP (24°29'36.89"S, 48°02'09.43"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0258, 2 individuals in banana field, HMN 344, Eldorado – SP (24°29'37.11"S, 48°02'10.84"W), 2019, M. Cremonesi, A. Santos colls.

Rhinodrilidae juveniles. COFMBRSP0246, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.33"S, 47°55'09.65"W), 2019, M. Cremonesi, A. Santos colls.

Family Megascolecidae

Amynthas gracilis (Kinberg, 1867)

COFMBRSP0237, 1 individual in banana field, HMN 379, Registro – SP (24°26'54.25"S, 47°49'38.22"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0250, 3 individuals in banana field, HMN 422, Sete Barras – SP (24°23'38.61"S, 47°55'23.49"W), 2019, M. Cremonesi, A. Santos colls.

Megascolecidae juveniles. COFMBRSP0234, 1 individual in Atlantic Forest, HMN 389, Registro – SP (24°26'16.28"S, 47°49'32.52"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0243, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.06"S, 47°55'10.35"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0247, 1 individual in Atlantic Forest, HMN 422, Sete Barras – SP (24°23'44.33"S, 47°55'09.65"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0254, 1 individual in Atlantic Forest, HMN 344, Eldorado – SP (24°29'56.60"S, 48°02'42.23"W), 2019, M. Cremonesi, A. Santos colls. COFMBRSP0257, 1 individual in banana field, HMN 344, Eldorado – SP (24°29'36.89"S, 48°02'09.43"W), 2019, M. Cremonesi, A. Santos colls.

Earthworm populations in the Ribeira River valley and other sites in Brazil

Only two earthworm species belonging to two families (Rhinodrilidae, Megascolecidae) were found at the six sampling sites in the three counties (Table 2): Pontoscolex (Pontoscolex) corethrurus and Amynthas gracilis, both considered peregrine/exotic in southern Brazil (Brown et al. 2006). Pontoscolex corethrurus may have originated in the Guyana shield area (Righi 1984), and A. gracilis may be native to China (Blakemore 2002). The former species was found living in all sites, while the latter was found in both banana plantations and native forest in Sete Barras and in banana plantations in Registro. At the other sites, only juveniles of the Megascolecidae family were found. These were most likely A. gracilis as well, but could not be identified to species level. Maximum richness found per site was similar in banana crops and Atlantic forest fragments (two spp. in each land use), but with some variation between sites (Table 2).

Table 2.

Earthworm families, species, and richness in banana plantations and Atlantic Forest remnants, in three counties of the Ribeira de Iguape River valley (Eldorado, Sete Barras, Registro). + means presence and – means absence.

Earthworm family and species Eldorado Sete Barras Registro
Banana Atlantic Forest Banana Atlantic Forest Banana Atlantic Forest
Megascolecidae
Amynthas gracilis + + +
Megascolecidae juveniles + + + +
Rhinodrilidae
Pontoscolex corethrurus + + + + + +
Rhinodrilidae juveniles +
Species Richness 2 2 2 ≥2 2 2

Most of the individuals collected (76% of the total) were of P. corethrurus, representing 29% of the total abundance in banana crop sites and 46% in Atlantic forest fragments (Fig. 2). Amynthas gracilis, although not occurring in all areas, accounted for 12% of all individuals sampled, of which 10% were found in banana crops but only 2% in Atlantic forests. Rhinodrilidae juveniles represented only 2% of the earthworms found, and occurred only in the Atlantic forest, while Megascolecidae juveniles represented 10% of all earthworms, and were often found in Atlantic forest fragments. Both species are widespread in Brazil (Brown et al. 2006), especially in agricultural and disturbed ecosystems, and display relatively high tolerance to a range of abiotic/biotic conditions, which have allowed these species to spread throughout most of the tropics and subtropics worldwide (Brown et al. 2006; González et al. 2006; Taheri et al. 2018). They have also been recommended as indicators of soil quality in agroecosystems and of disturbance in natural landscapes (Nunes et al. 2007; Fernandes et al. 2010).

Figure 2. 

Frequency of earthworm species (% of total individuals collected) in each ecosystem sampled (A) in Atlantic Forest (AF) and banana plantations (BP) and by counties (B).

The predominance of P. corethrurus in both native forest and banana plantations of the Ribeira River valley indicate that non-native species have extensively colonized disturbed soils of this region. Nonetheless, this potentially widespread occurrence of exotics should be further evaluated both regionally and nationally, in order to better determine the extent of this phenomenon as well as its possible causes.

Mean overall abundance and biomass of earthworms found in the three sites studied here (6 to 13 indiv. m-2 and 2.5 to 9 g m-2) tended to be quite low compared with others observed overall in Brazil (21 to 459 indiv. m-2 and 3.1 to 177.4 g m-2; see Table 3). At sites near the Ribeira River valley in the neighboring state of Paraná (Römbke et al. 2009; Maschio et al. 2010), and within the Ribeira River watershed in the nearby Turvo River valley (a tributary of the Ribeira River; Brown et al. 2009), both abundance and biomass were generally much higher (Table 3), even though the predominant earthworm species was the same (P. corethrurus). This is probably due to the less intensive and more traditional agroforestry management practices used in these sites, including slashing and mulching, as well as the presence of other trees, particularly atmospheric N2-fixing leguminous trees, and the absence of or lower pesticide use (Brown et al. 2009; Römbke et al. 2009). These practices may benefit earthworm populations, particularly P. corethrurus, as observed comparing a mulched and non-mulched plantation in Antonina, where earthworm abundance was ~13 times higher with mulching (Maschio et al. 2010). Reasons for the lower values found in the Ribeira River valley sites may be due to the more intensive management practices typical of commercial banana plantations in the region, including insecticide and nematicide applications, which may reduce earthworm populations (Clermont-Dauphin et al. 2004).

Table 3.

Earthworm abundance and biomass found in banana plantations worldwide, and the predominant species encountered (when available).

Country Location Abundance (indiv. m–2) Biomass (g m–2) Predominant species References
Brazil Antonina (Monoculture) 71 35.1 P. corethrurus Römbke et al. (2009)
221 95.7 P. corethrurus
86 23.8 P. corethrurus
Antonina (Agroforestry) 173 77.1 P. corethrurus
338 69.6 P. corethrurus
117 43.5 P. corethrurus
21a 3.1b P. corethrurus Maschio et al. (2010)
293a 34.9b P. corethrurus
Adrianópolis (Agroforestry) 211–413c 37–71.2c P. corethrurus Brown et al. (2009)
Barra do Turvo (Agroforestry) 99–176c 11.2–17.3c P. corethrurus
229–459c 48.3–117.4c P. corethrurus
Casimiro de Abreu ~205–440c NA Quintero (2010)
Paraty 167 NA Correia et al. (2001)
Eldorado 8 3.9 P. corethrurus This study
Sete Barras 13 9.0 P. corethrurus
Registro 6 2.5 P. corethrurus
Cameroon Mbalmayo Forest Reserve 70 Legonodrilus sp. nov. 1, Eminoscolex lamani Norgrove et al. (2011)
121 Legonodrilus sp. nov. 1, Eminoscolex lamani
Campo Ma’an 16–92d NA Kanmegne (2004)
Colombia Quindío (Armenia) 9–16e 1.2–3.0e NAf Molina and Feijoo (2016)
Costa Rica Limón Province (Finca San Pablo) 83–812g NA Agüero et al. (2002)
Pueblo Nuevo de Villa Franca de Guácimo, Limón 29 6.2 NA Cornwell (2014)
Cahuita 350 144.6 P. corethrurus Lapied and Lavelle (2003)
Guadeloupe (France) Basse-Terre Andosols (mean of 23 sites) 88 23 NA Clermont-Dauphin et al. (2004)
Basse Terre Nitisols (mean of 11 sites) 54 17.5 NA
Capesterre-Belle-Eau (Gloria Bas) 168 27.6 P. corethrurus Burac et al. (2018)
Capesterre-Belle-Eau (Source) 288 42.2 P. corethrurus
Capesterre-Belle-Eau (Bergerie) 188 33.6 P. corethrurus
Baillif (Sextius) 336 112 P. corethrurus
Baillif (Grand Canon) 192 70.8 P. corethrurus
Saint-Claude (Saut d’Eau) 364 46 P. corethrurus
Ecuador Latacunga (La Maná) 168 NA Avilés (2017)
111 NA
Manabí (El Carmen) 78 NA
37 NA
El Carmen (Cijádi) 0–145h NA Figueroa (2019)
El Carmen (Nápoles) 34–144h NA
Santo Domingo de los Tsáchilas (Santa Patrícia) 83–548h NA
Santo Domingo de los Tsáchilas (La Floresta) 22–150h NA
India West Tripura 16–656i 4.8–453.6i P. corethrurus Dhar and Chaudhuri (2018)
Rajapalayam 116 48.8 Lampito mauritii, Perionyx excavatus Mariappan et al. (2013)
Ivory Coast Taabo (Lamto reservation) 186 8.5 Reginaldia anomala Tondoh (1994, 2007)
Martinique (France) Le Lorrain (Feugère) 244 67.6 P. corethrurus Burac et al. (2018)
Le Lorrain (Bellevue) 152 43.6 P. corethrurus
Le Lorrain (Limite) 52 26 P. corethrurus
L’Ajoupa-Bouillon (Allée Domergue 3) 148 49.6 P. corethrurus
Basse-Pointe (Fromager Rivière) 80 26 P. corethrurus
Basse-Pointe (Dantu Bas) 40 9 P. corethrurus
Mexico Tabasco, Pablo L. Sidar 25 10 P. corethrurus, Lavellodrilus bonampakensis Huerta et al. (2005)
Tabasco, Teapa 116 20.8 P. corethrurus, Drawida barwelli, Polypheretima elongata Geissen et al. (2009)
117 11.8 Balanteodrilus pearsei, Drawida barwelli
94 40.4 Balanteodrilus pearsei, Polypheretima elongata
125 35.6 P. corethrurus, Drawida barwelli
25 8.8 P. corethrurus, Lavellodrilus bonampakensis Huerta et al. (2007)
~350 2.5 Diplotrema murchiei Huerta et al. (2013)
~350 9.3 P. corethrurus
~470 16.2 P. corethrurus
~100 11 P. corethrurus
~80 2.8 P. corethrurus
~125 0.8 Dichogaster sp.
Nicaragua León (Finca Cony) 150 NA Hernández et al. (2015)
León (Finca San Martín) 325 NA
León (Finca Santa Isabel) 50 NA
León (Finca El verdon) 65 NA
Possoltega (Finca San Joaquin) 150 NA
Possoltega (Finca Los Ángeles) 225 NA
Possoltega (Finca Maria de los Ángeles) 100 NA
Possoltega (Finca Montes Verdes) 125 NA
Philippines Davao (Sumitomo Fruits Corporation) ~85–175j NA Fusilero et al. (2013)
~75–215j Metaphire cai
South Africa Kwazulu-Natal (Eshowe) 1500k 180 Amynthas rodericensis, Amynthas minimus, P. corethrurus Dlamini and Haynes (2004)
Uganda Kabanyolo University Farm 18–207l 0.1–9.4l Dichogaster sp. 2, Gordiodrilus sp. 1 Block and Banage (1968)
Mabira Forest reserve (1 yr old) 13 0.4 NA Okwakol (1994)
(2 yr old) 125 2.2 NA
(3 yr old) 131 1.3 NA
(5 yr old) 54 0.5 NA
(20 yr old) 154 4.2 NA

Earthworm communities in banana plantations worldwide

More than 70 studies were found from 28 countries with data on earthworms in banana and plantain fields (Tables 3, 4, 5). Of these studies, 49 had species data (Table 4; see also full dataset in Cremonesi et al. 2020), coming from ≥ 210 sites (Table 5), of which most were in the Spanish Canary Islands (N = 77), mainly due to the intensive sampling efforts of Talavera in Tenerife (Talavera 1992a). Interestingly, two of the major banana-producing countries in terms of area were not represented (Tanzania, Rwanda), and in China (another important producer), only one study reported earthworms from a single site (Sun et al. 2012). Plantain banana fields were sampled in only 22 locations (10% of total) in four countries (Colombia, Cameroon, Ivory Coast and Ecuador; Tondoh 2007; Norgrove et al. 2011; Avilés 2017; Feijoo et al. 2018), and involved traditional management practices, rather than conventional cultivation. Most of the fields evaluated were banana plantations, and only in Ecuador were mixed banana/plantain fields evaluated (Avilés 2017).

Table 4.

Earthworm species, richness and number of native and exotic species found in banana plantations under various management practices worldwide.

Country Location Management Culture type Earthworm species Richness Native (N) /Exotic (E) References
Bangladesh Lalmonirhat District NA NA Lampito mauritii, Metaphire posthuma, Pontoscolex corethrurus 3 2/1 Reynolds et al. (1995)
Bermuda Paget Parish NA NA Amynthas rodericensis 1 0/1 Reynolds and Fragoso (2004)
Southampton Parish NA NA Amynthas hupeiensis 1 0/1 Reynolds and Fragoso (2004)
Brazil Antonina, PR Agroforestry Monoculture Amynthas corticis, Pontoscolex corethrurus, two other spp. 4 0/4 Römbke et al. (2009)
Antonina, PR Agroforestry Monoculture Amynthas gracilis, Pontoscolex corethrurus, two other spp. 4 0/4 Römbke et al. (2009)
Antonina, PR Agroforestry Monoculture Dichogaster spp., Pontoscolex corethrurus 4 0/4 Römbke et al. (2009)
Antonina, PR Agroforestry Monoculture Ocnerodrilus occidentalis, Pontoscolex corethrurus, two other spp. 4 0/4 Römbke et al. (2009)
Antonina, PR Agroforestry Monoculture Pontoscolex corethrurus, one other sp. 2 0/2 Römbke et al. (2009)
Antonina, PR NA Polyculture Pontoscolex corethrurus, one other sp. 2 0/2 Römbke et al. (2009)
Antonina, PR Agroforestry Polyculture Dichogaster sp., Pontoscolex corethrurus, and one unidentified sp. 3 ?/2 Maschio et al. (2010)
Antonina, PR Agroforestry Polyculture Pontoscolex corethrurus 1 0/1 Maschio et al. (2010)
Adrianópolis, PR Agroforestry Polyculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 Brown et al. (2009)
Barra do Turvo, SP Agroforestry Polyculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 Brown et al. (2009)
Barra do Turvo, SP Agroforestry Polyculture Amynthas gracilis, Dichogaster sp., Pontoscolex corethrurus 3 0/3 Brown et al. (2009)
Areia, PB NA Polyculture Amynthas gracilis, Dichogaster affinis, Eudrilus eugeniae, Pontoscolex corethrurus 4 0/4 Guerra and Silva (1994)
Eldorado, SP Conventional Monoculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 This study
Jutaí River margin, AM NA NA Pontoscolex corethrurus ND 0/1 Righi (1990)
Registro, SP Conventional Monoculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 This study
Sete Barras, SP Conventional Monoculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 This study
Cameroon Mbalmayo Forest Reserve (low density cover) Organic Agroforestry Monoculture Dichogaster hauseri, Eminoscolex lamani, Eudrilidae gen. et sp. nov.1 & 2, Legonodrilus sp. nov.1, Malodrilus kamerunensis, Nematogenia panamaensis, Rosadrilus camerunensis 8 7/1 Norgrove et al. (2011)
Mbalmayo Forest Reserve (high density cover) Organic Agroforestry Monoculture Dichogaster annae, Dichogaster bolaui, Dichogaster sp., Eminoscolex lamani, Eudrilidae sp., Eudrilidae gen. et sp. nov. 1, Legonodrilus sp. nov. 1, Nematogenia panamaensis, Ocnerodrilidae gen. et sp. nov., Rosadrilus camerunensis, Scolecillus tantillus 10 7/3 Norgrove et al. (2011)
China Hainan Province NA NA Pheretima montana ND 0/1 Sun et al. (2012)
Colombia Quindío, Circasia, Barcelona (La Sofe farm) NA Monoculture Aptodrilus fuhrmanni, Amynthas minimus, Glossodrilus chaguala, Glossodrilus panikita, Martiodrilus quimbayaensis 5 4/1 Feijoo et al. (2018)
Quindío, Circasia, Barcelona (La Sofe farm) NA Polyculture Aptodrilus fuhrmanni, Amynthas minimus, Glossodrilus chaguala, Glossodrilus panikita, Martiodrilus quimbayaensis 5 4/1 Feijoo et al. (2018)
Quindío, Circasia, Barcelona (La Sofe farm) NA NA Amynthas gracilis, Periscolex columbianus 2 1/1 Feijoo et al. (2018)
Colombia Armenia, Niagara (La Catalina) NA NA Amynthas gracilis, Glossodrilus griseus, Pontoscolex corethrurus 3 1/2 Feijoo et al. (2018)
Quindio, Calarcá, Quebrada Negra NA NA Glossodrilus griseus 1 1/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm) NA Monoculture Glossodrilus lacteus 1 1/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm) NA Polyculture Glossodrilus lacteus 1 1/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm) NA NA Dichogaster affinis 1 0/1 Feijoo et al. (2018)
Armenia, La Revancha (Villa Sofia farm) NA NA Amynthas gracilis, Dichogaster affinis, Dichogaster bolaui, Glossodrilus griseus, Perionyx excavatus 5 1/4 Feijoo et al. (2018)
Armenia, La Revancha (Bella Marina farm) NA NA Dichogaster saliens, Periscolex columbianus 2 1/1 Feijoo et al. (2018)
Quindío, Armenia, El Rhin NA NA Periscolex columbianus 1 1/0 Feijoo et al. (2018)
Quindío, Armenia, La India (La Ermita farm) NA NA Periscolex coreguaje 1 1/0 Feijoo et al. (2018)
Circasia, Barcelona Baja rural (Buenos Aires farm) NA NA Amynthas gracilis, Dichogaster saliens, Pontoscolex corethrurus 3 0/3 Feijoo et al. (2018)
Quindío, Armenia, La India (La Miranda farm) NA NA Dichogaster saliens 1 0/1 Feijoo et al. (2018)
Quindío, Armenia, La Patria NA NA Dichogaster saliens 1 0/1 Feijoo et al. (2018)
Costa Rica Cahuita NA NA Pontoscolex corethrurus ND ?/1 Lapied and Lavelle (2003)
Cuba Boyeros Organic Monoculture Dichogaster affinis, Dichogaster bolaui, Onychochaeta elegans, Polypheretima elongata, Protozapotecia angelesae 5 2/3 Martínez-Leiva (2002)
Guadeloupe (France) Capesterre-Belle-Eau NA Monoculture Pontoscolex corethrurus ND ?/1 Lafont et al. (2007)
Capesterre-Belle-Eau (Gloria Bas) Conventional Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Capesterre-Belle-Eau (Source) Conventional Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Capesterre-Belle-Eau (Bergerie) Agroecological Monoculture Pontoscolex corethrurus, unknown sp. 2 2 ? Burac et al. (2018)
Baillilf (Sextius) Agroecological Monoculture Pontoscolex corethrurus, unknown sp. 2 ? Burac et al. (2018)
Baillilf (Grand Canon) Agroecological Monoculture Pontoscolex corethrurus, unknown sp. 3 2 ? Burac et al. (2018)
Saint-Claude (Saut d’Eau) Agroecological Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
India Dakshina Kannada District (Belthangady) NA NA Hoplochaetella kempi ND 1/0 Siddaraju et al. (2013)
Dakshina Kannada District (Mangalore) NA NA Konkadrilus bahli ND 1/0 Siddaraju et al. (2013)
Dakshina Kannada District (Mangalore) NA NA Dichogaster affinis ND 0/1 Siddaraju et al. (2013)
India Dakshina Kannada District (Bantwal) NA NA Octochaetona parva ND 1/0 Siddaraju et al. (2010)
Dakshina Kannada District (sites not detailed) NA NA Amynthas corticis, Hoplochaetella kempi, Hoplochaetella stuarti, Hoplochaetella suctoria, Megascolex konkanensis, Metaphire posthuma, Octochaetona paliensis, Octochaetona parva ND 7/1 Siddaraju et al. (2010, 2013)
Kerala (Vellayambalam) NA NA Perionyx excavatus, Pontoscolex corethrurus 2 0/2 Nair et al. (2007)
Mizoram NA Monoculture Drawida nepalensis, Drawida rangamatiana, Drawida sp., Metaphire houlleti, Perionyx excavatus 5 3/2 Lalthanzara (2007)
Mizoram NA Polyculture Drawida nagana, Drawida sp., Metaphire houlleti, Perionyx excavatus 4 2/2 Lalthanzara (2007)
Rajapalayam NA NA Lampito mauritii, Perionyx excavatus 2 1/1 Mariappan et al. (2013)
Udupi District (Adve) NA NA Megascolex konkanensis 1 1/0 Kumar et al. (2018)
Udupi District (Adve) NA NA Metaphire houlleti 1 0/1 Kumar et al. (2018)
Udupi District (Bellibetu) NA NA Metaphire houlleti, Pontoscolex corethrurus 2 0/2 Kumar et al. (2018)
Udupi District (Mudarangadi) NA NA Pontoscolex corethrurus 1 0/1 Kumar et al. (2018)
Udupi District (Nandikur) NA NA Drawida ampullacea, Drawida sulcata, Metaphire peguana 3 3/0 Kumar et al. (2018)
Udupi District (Nandikur) NA NA Drawida ampullacea 1 1/0 Kumar et al. (2018)
Udupi District (Padabettu) NA NA Perionyx excavatus 1 0/1 Kumar et al. (2018)
Udupi District (Yellur) NA NA Mallehulla indica, Megascolex konkanensis 2 2/0 Kumar et al. (2018)
West Tripura (Mohanpur, Maheshkhola, Rastermatha) Organic Monoculture Amynthas alexandri, Drawida assamensis, Drawida papillifer, Eutyphoeus comillahnus, Lampito mauritii, Lennogaster sp., Metaphire houlleti, Metaphire posthuma, Octochaetona beatrix, Perionyx excavatus, Pontoscolex corethrurus 3–7 4/7 Dhar and Chaudhuri (2018)
Indonesia Bangkalan (Kamal, Burneh, Socah, Bypass) NA NA Amynthas robustus, Metaphire californica, Metaphire javanica ND 1/2 Budijastuti (2019)
Bangkalan (Tanah Merah) NA NA Metaphire posthuma 1 0/1 Budijastuti (2019)
Bangkalan (Labang) NA NA Amynthas robustus, Metaphire javanica, Metaphire californica, Pheretima racemosa 4 2/2 Budijastuti (2019)
Gresik (Driyorejo, Kedamean, Ngipik, SumengkoLegundi) NA NA Amynthas robustus, Metaphire javanica ND 1/1 Budijastuti (2019)
Gresik (Wringinanamon) NA NA Amynthas robustus, Metaphire javanica, Metaphire posthuma 3 1/2 Budijastuti (2019)
Sidoarjo (Waru, Taman, Sidoarjo, Tulangan, Tanggulangin, Candi) NA NA Amynthas robustus, Metaphire javanica, Metaphire posthuma ND 1/2 Budijastuti (2019)
Surubaya (Pakal, Benowo, Tandes, Sukolilo, Gubeng, Gununganyar) NA NA Amynthas robustus, Metaphire javanica, Metaphire posthuma ND 1/2 Budijastuti (2019)
Ivory Coast Lamto region NA NA Dichogaster wenkei, Reginaldia anomala, Stuhlmannia palustris, Stuhlmannia zielae ND 4/0 Tondoh (1994)
Jamaica Clarendon, Crofts Mountain NA NA Drawida barwelli, Polypheretima elongata 2 0/2 Sims (1987)
Madagascar Ambatosoratra Ambatondrazaka NA NA Kynotus sihanakus, Kynotus sp.2 2 2/0 Razafindrakoto et al. (2016), Csuzdi et al. (2017)
Malaysia Serdang, Sengalor (Universiti Putra Malaysia) NA NA Pontoscolex corethrurus ND 0/1 Teng et al. (2006)
Martinique (France) Le Lorrain (Feugère) Conventional Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Le Lorrain (Limite) Agroecological Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Le Lorrain (Bellevue) Conventional Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
L’Ajoupa-Bouillon (Allée Domergue 3) Agroecological Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Basse-Pointe (Fromager Rivière) Conventional Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Basse-Pointe (Dantu Bas) Agroecological Monoculture Pontoscolex corethrurus 1 0/1 Burac et al. (2018)
Mexico Tabasco NA Monoculture Lavellodrilus bonampakensis, Pontoscolex corethrurus 2 1/1 Huerta et al. (2005)
Tabasco, Teapa B1 NA Monoculture Balanteodrilus pearsei, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus, Pontoscolex sp. 5 1/4 Geissen et al. (2009)
Tabasco, Teapa B2 NA Monoculture Balanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Periscolex brachycystis, Polypheretima elongata, Pontoscolex sp. 6 2/4 Geissen et al. (2009)
Tabasco, Teapa AF1 Agroforestry Polyculture Balanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus, Pontoscolex sp. 6 2/4 Geissen et al. (2009)
Tabasco, Teapa AF2 Agroforestry Polyculture Balanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus 5 1/4 Geissen et al. (2009)
Tabasco, Teapa (site 1) Conventional NA Dichogaster saliens, Diplotrema murchiei, Pontoscolex corethrurus 3 ½ Huerta et al. (2013)
Tabasco, Teapa (site 2) Conventional NA Dichogaster saliens, Pontoscolex corethrurus 2 0/2 Huerta et al. (2013)
Tabasco, Teapa (site 3) Conventional NA Diplotrema murchiei, Polypheretima elongata, Pontoscolex corethrurus 3 1/2 Huerta et al. (2013)
Tabasco, Teapa (site 4) Conventional Polyculture Amynthas gracilis, Pontoscolex corethrurus 2 0/2 Huerta et al. (2007)
Tabasco, Teapa (site 5) Conventional Polyculture Dichogaster saliens, Polypheretima elongata, Pontoscolex corethrurus 3 0/3 Huerta et al. (2013)
Tabasco, Teapa (site 6) Conventional NA Dichogaster saliens, Pontoscolex corethrurus 2 0/2 Huerta et al. (2007)
Tabasco, Pablo L. Sidar NA Monoculture Lavellodrilus bonampakensis, Pontoscolex corethrurus 2 1/1 Huerta et al. (2013)
Tamaulipas (Biosphere Reserve “El Cielo”) NA NA Amynthas gracilis ND 0/1 Barois (1992)
Actopan, Ejido Buenavista NA NA Balanteodrilus psammophilus ND 1/0 Fragoso and Rojas (2007)
Nicaragua Managua NA NA Dichogaster bolaui, Periscolex brachycystis 2 1/1 Sherlock et al. (2011)
Peru Sarita Colonia NA Monoculture Pontoscolex corethrurus and two native spp. 3 2/1 Pashanasi (2007)
Philippines Davao (Sumitomo Fruits Corporation, 15% site) Conventional Monoculture Metaphire sp., Pithemera bicincta, Pontoscolex corethrurus 3 1/2 Fusilero et al. (2013)
Davao (Sumitomo Fruits Corporation, 25% site) Conventional Monoculture Metaphire cai, Metapheretima sp., Perionyx excavatus 3 2/1 Fusilero et al. (2013)
Portugal Madeira Island (Ribeira Brava) NA NA Aporrectodea moebii, Eisenia eisensi, Metaphire californica 3 0/3 Talavera (1996)
Madeira Island (Funchal) NA NA Amynthas gracilis, Metaphire californica, Ocnerodrilus occidentalis 3 0/3 Talavera (1996)
Portugal Madeira Island (Santa Cruz) NA NA Amynthas gracilis 1 0/1 Talavera (1996)
Madeira Island (Terceira Lombada) NA NA Aporrectodea moebii, Eiseniella tetraedra 2 0/2 Talavera (1996)
Madeira Island (Porto Moniz) NA NA Amynthas gracilis, Aporrectodea rosea, Aporrectodea trapezoides, Dendrobaena pseudohortensis 4 0/4 Talavera (2011)
Madeira Island (Terceira Lombada) NA NA Aporrectodea caliginosa, Aporrectodea rosea, Eiseniella tetraedra 3 0/3 Talavera (2011)
Seychelles Cousine Island NA Monoculture Pontoscolex corethrurus ND 0/1 Plisko (2001)
South Africa KwaZulu-Natal (Fairfield Farm) NA Monoculture Pontoscolex corethrurus ND 0/1 Plisko (2001)
KwaZulu-Natal (Benhurst Farm) NA Monoculture Pontoscolex corethrurus ND 0/1 Plisko (2001)
KwaZulu-Natal (6 sites in Eshowe) NA Monoculture Amynthas corticis, Amynthas minimus, Amynthas rodericensis, Dichogaster bolaui, Pontoscolex corethrurus, and one other sp. ND 0/5 Dlamini and Haynes (2004)
Spain Gomera Island (Agulo) NA NA Amynthas rodericensis, Allolobophora chlorotica, Eiseniella tetraedra, Ocnerodrilus occidentalis 4 0/4 Talavera (1990a, 2007)
Gomera Island (Barranco de la Villa) NA NA Bimastos rubidus, Ocnerodrilus occidentalis, Pithemera bicincta 3 0/3 Talavera (2007)
Gomera Island (Barranco del Valle) NA NA Allolobophora chlorotica, Metaphire californica 2 0/2 Talavera (1990b, 2007)
Gomera Island (Casas de Aluce) NA NA Aporrectodea rosea, Microscolex phosphoreus 2 0/2 Talavera (2007)
Gomera Island (Cabo Verde) NA NA Amynthas gracilis, Bimastos rubidus 2 0/2 Talavera (1990b, 2007)
Gomera Island (Costa Agulo) NA NA Aporrectodea trapezoides, Amynthas rodericensis, Bimastos rubidus, Ocnerodrilus occidentalis 4 0/4 Talavera (2007)
Gomera Island (El Molinito) NA NA Amynthas morrisi, Microscolex phosphoreus 2 0/2 Talavera (2007)
Gomera Island (Hermigua) NA NA Aporrectodea rosea, Bimastos rubidus, Eisenia fetida, Ocnerodrilus occidentalis 4 0/4 Talavera (1990a, 2007)
Gomera Island (Laguna de Santiago) NA NA Amynthas morrisi, Aporrectodea rosea, Aporrectodea trapezoides, Bimastos rubidus, Dendrobaena hortensis, Dichogaster affinis, Metaphire californica, Pithemera bicincta 9 0/9 Talavera (2007)
Gomera Island (Playa de Santiago) NA NA Ocnerodrilus occidentalis 1 0/1 Talavera (1990a)
Gomera Island (Seimal) NA NA Eiseniella tetraedra, Metaphire californica, Microscolex phosphoreus 3 0/3 Talavera (2007)
Gomera Island (Taguluche) NA NA Amynthas morrisi, Allolobophora chlorotica, Octalasion lacteum 3 0/3 Talavera (2007)
Gomera Island (Valle Gran Rey) NA NA Allolobophora chlorotica, Aporrectodea trapezoides, Dendrobaena hortensis, Eisenia fetida, Microscolex dubius, Pithemera bicincta 5 0/5 Talavera (2007)
Gran Canaria (Lomo del Galeón) NA NA Ocnerodrilus occidentalis 1 0/1 Talavera (1990a)
Gran Canaria (Los Llanos) NA NA Ocnerodrilus occidentalis, Pithemera bicincta 2 0/2 Talavera (1990a)
Gran Canaria Island (Bañaderos) NA NA Metaphire californica 1 0/1 Talavera (1990b)
Gran Canaria Island (Barranco Guiniguada) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
Gran Canaria Island (Frontón) NA NA Amynthas gracilis 1 0/1 Talavera (1990b)
Gran Canaria Island (Galdar) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
Spain Gran Canaria Island (Hoya Mondondo) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
Gran Canaria Island (La Aldea) NA NA Dichogaster affinis 1 0/1 Talavera (1992b)
Gran Canaria Island (Pedrazo) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
Gran Canaria Island (Tenoya) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
Hierro Island (Los Mocanes) NA NA Ocnerodrilus occidentalis 1 0/1 Talavera (1990a)
Hierra Island (NE tip) NA NA Microscolex phosphoreus ND 0/1 Talavera and Pérez (2009)
La Palma Island (Barranco de las Angustias) NA NA Amynthas gracilis 1 0/1 Talavera (1990b)
La Palma Island (Barranco Nogales) NA NA Amynthas gracilis 1 0/1 Talavera (1990b)
La Palma Island (El Socorro) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
La Palma Island (La Caldereta) NA NA Amynthas morrisi, Metaphire californica 2 0/2 Talavera (1990b)
La Palma Island (Los Cancajos) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
La Palma Island (Los Llanos de Aridane) NA NA Amynthas morrisi, Metaphire californica 2 0/2 Talavera (1990b)
La Palma Island (Tazacorte) NA NA Amynthas gracilis, Amynthas morrisi, Metaphire californica 3 0/3 Talavera (1990b)
Tenerife Island (Abama) NA Monoculture Aporrectodea rosea, Dendrobaena hortensis, Eisenia andrei, Microscolex dubius 4 0/4 Talavera (1992a)
Tenerife Island (Adeje) NA NA Ocnerodrilus occidentalis 1 0/1 Talavera (1990a)
Tenerife Island (Bajamar) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Microscolex phosphoreus, Ocnerodrilus occidentalis 6 0/6 Talavera (1990a, 1992a, 1992b)
Tenerife Island (Barranco de Santos) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Bimastos rubidus, Eisenia andrei, Microscolex dubius, Pithemera bicincta 6 0/6 Talavera (1990b, 1992a)
Tenerife Island (Barranco del Inglés) NA Monoculture Aporrectodea rosea, Aporrectodea trapezoides, Eisenia andrei, Microscolex dubius 4 0/4 Talavera (1992a)
Tenerife Island (Barranco la Atalaya) NA Monoculture Aporrectodea rosea, Pithemera bicincta 2 0/2 Talavera (1992a)
Tenerife Island (Barranco las Galletas) NA Monoculture Aporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis 3 0/3 Talavera (1992a)
Tenerife Island (Barranco San Felipe) NA Monoculture Amynthas gracilis, Eisenia andrei, Pithemera bicincta 3 0/3 Talavera (1992a, 1990b)
Tenerife Island (Buenavista del Norte) NA NA Ocnerodrilus occidentalis 1 0/1 Talavera (1990a)
Tenerife Island (Casablanca) NA Monoculture Amynthas corticis, Aporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis 4 0/4 Talavera (1992a)
Tenerife Island (Costa Valle Guerra) NA Monoculture Amynthas gracilis 1 0/1 Talavera (1992a)
Tenerife Island (El Puente) NA Monoculture Amynthas gracilis, Aporrectodea rosea, Eisenia andrei, Microscolex phosphoreus, Ocnerodrilus occidentalis 5 0/5 Talavera (1992a)
Tenerife Island (El Rincón) NA Monoculture Amynthas gracilis, Bimastos rubidus, Dendrobaena cognetti, Microscolex dubius, Microscolex phosphoreus, Octodrilus complanatus 6 0/6 Talavera (1992a)
Spain Tenerife Island (El Socorro) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
Tenerife Island (Fañabé) NA Monoculture Amynthas corticis, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Ocnerodrilus occidentalis 5 0/5 Talavera (1990a, 1992a, 1992b)
Tenerife Island (Güimar) NA NA Dichogaster affinis, Ocnerodrilus occidentalis 2 0/2 Talavera (1990a, 1992b)
Tenerife Island (Iboybo) NA Monoculture Aporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis 3 0/3 Talavera (1992a)
Tenerife Island (Icod de Los Vinos) NA Monoculture Dendrobaena cognetti, Bimastos rubidus, Octodrilus complanatus, Ocnerodrilus occidentalis 4 0/4 Talavera (1992a)
Tenerife Island (Igueste) NA Monoculture Allolobophora chlorotica, Aporrectodea rosea, Aporrectodea trapezoides, Pontoscolex corethrurus, Ocnerodrilus occidentalis 5 0/5 Talavera (1992a)
Tenerife Island (La Hondura) NA Monoculture Amynthas morrisi 1 0/1 Talavera (1992a)
Tenerife Island (La Longuera) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Eisenia fetida, Microscolex dubius, Octodrilus complanatus 5 0/5 Talavera (1992a)
Tenerife Island (La Matanza) NA Monoculture Bimastos rubidus, Eisenia andrei, Microscolex phosphoreus 3 0/3 Talavera (1992a)
Tenerife Island (La Montañeta) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
Tenerife Island (La Vera) NA Monoculture Bimastos rubidus, Eisenia andrei, Microscolex phosphoreus 3 0/3 Talavera (1992a)
Tenerife Island (Las Arenas) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
Tenerife Island (Las Galletas) NA Monoculture Eisenia andrei, Bimastos eiseni, Ocnerodrilus occidentalis 3 0/3 Talavera (1990a, 1992a)
Tenerife Island (Las Madrigueras) NA NA Amynthas morrisi 1 0/1 Talavera (1990b)
Tenerife Island (Los Quintos) NA Monoculture Dendrobaena cognetti, Bimastos rubidus, Microscolex phosphoreus, Pithemera bicincta, Ocnerodrilus occidentalis 5 0/5 Talavera (1992a)
Tenerife Island (Los Realejos) NA NA Pithemera bicincta 1 0/1 Talavera (1990b)
Tenerife Island (Los Rechazos) NA Monoculture Aporrectodea trapezoides, Bimastos rubidus, Eisenia fetida, Octodrilus complanatus, Pithemera bicincta 5 0/5 Talavera (1992a)
Tenerife Island (Los Silos) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Ocnerodrilus occidentalis 5 0/5 Talavera (1992a 1992b)
Tenerife Island (Loss Llanos) NA Monoculture Amynthas morrisi, Bimastos rubidus, Eisenia andrei, Pithemera bicincta 4 0/4 Talavera (1992a)
Tenerife Island (Playa de las Aguas) NA Monoculture Amynthas morrisi, Eisenia andrei, Pithemera bicincta 3 0/3 Talavera (1992a)
Tenerife Island (Playa de San Juan) NA Monoculture Aporrectodea rosea, Dendrobaena hortensis, Bimastos rubidus, Eisenia andrei 4 0/4 Talavera (1992a)
Tenerife Island (Playa San Marcos) NA Monoculture Pithemera bicincta, Bimastos rubidus, Microscolex phosphoreus 3 0/3 Talavera (1992a)
Tenerife Island (Puertito de Gilimar) NA Monoculture Microscolex phosphoreus, Pithemera bicincta, Ocnerodrilus occidentalis 3 0/3 Talavera (1992a)
Tenerife Island (Puerto de Santiago) NA Monoculture Amynthas morrisi 1 0/1 Talavera (1990b, 1992a)
Tenerife Island (Punta del Hidalgo) NA Monoculture Amynthas gracilis, Ocnerodrilus occidentalis 2 0/2 Talavera (1992a)
Tenerife Island (San Andrés) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Microscolex phosphoreus, Ocnerodrilus occidentalis 4 0/4 Talavera (1992a)
Tenerife Island (San Bernardo) NA Monoculture Amynthas corticis, Amynthas morrisi, Aporrectodea rosea, Eisenia andrei 4 0/4 Talavera (1992a)
Spain Tenerife Island (San Juan de la Rambla) NA Monoculture Amynthas gracilis, Bimastos rubidus, Dendrobaena hortensis, Eisenia fetida, Pithemera bicincta 5 0/5 Talavera (1990b, 1992a)
Tenerife Island (San Pedro de Daute) NA Monoculture Amynthas morrisi, Aporrectodea rosea, Ocnerodrilus occidentalis 3 0/3 Talavera (1992a)
Tenerife Island (Santo Domingo) NA Monoculture Dendrobaena cognetti, Microscolex dubius, Microscolex phosphoreus 3 0/3 Talavera (1992a)
Tenerife Island (Taganana) NA Monoculture Amynthas morrisi 1 0/1 Talavera (1992a)
Tenerife Island (Tejina) NA Monoculture Amynthas corticis, Pithemera bicincta 2 0/2 Talavera (1992a)
Taiwan Central region NA NA Pontoscolex corethrurus ND 0/1 Tsai et al. (2000)
Uganda Kabanyolo University Farm NA NA Dichogaster sp. 1, Dichogaster sp. 2, Gordiodrilus sp., Pygmaeodrilus sp., Polytoreutus sp. 1 5 5/0 Block and Banage (1968)

Overall, ≥104 earthworm species from 10 earthworm families were recorded from banana/plantain fields worldwide, of which around 61 (59%) were native and 43 exotic to the sampling sites (Table 5). Estimating these numbers is difficult due to insufficient taxonomic resolution in some samples, as well as the uncertain origin of some widespread anthropochores (peregrines transported by humans), particularly in the Megascolecidae family (Blakemore 2002). Highest species richness (27) was observed overall in India, where most of the species found were native (74%). High proportions of native species were also observed in Ivory Coast, Madagascar, and Uganda (possibly 100%) as well as Cameroon (75%), but were lower in Mexico (58%) and Colombia (53%). In these countries, many of the plantations were managed more traditionally, or using agroforestry, although the low number of sampling sites may also be responsible for these high values, particularly in the former countries. In fact, agroforestry systems had a total of 22 species from nine sites, while conventional production systems had only nine species from 13 sites. Nonetheless, because not enough information was provided in the publications on management practices (not reported in ≥150 sites; Table 4), the role of less intensive banana production systems in maintaining native earthworm populations must still be further evaluated.

High species richness was also detected overall in Spain (25), mainly due to the higher sampling effort involving a large number of sites in the Canary Islands. However, all of the species encountered on the islands offshore of Africa were exotic, their introduction having been stimulated over centuries of human colonization bringing in exotic soils and crops (Talavera 2007, 2011). The Caribbean islands had few species (5), despite a large sampling effort, and many sites were dominated by P. corethrurus (Burac et al. 2018). In Brazil, Costa Rica, Martinique, Jamaica, Bermuda, the Seychelles, Taiwan, Malaysia, and China, all the earthworm species encountered were exotic (Table 5). The continent with the highest number of species recorded was Africa (50), of which 40% were native. In Asia, 35 species were recorded, with a higher proportion of natives (66%). In North and South America, around 50% of the species found were native, but these were mainly due to the higher number of natives observed in Colombian (Feijoo et al. 2018) and Mexican (Geissen et al. 2009; Huerta et al. 2013) plantations.

Table 5.

Number of quantitative (with abundance data) and qualitative (where species were identified) sampling sites and earthworm species (total, native, and exotic) and families found in banana plantations in different countries of the world.

Country No. sites: Quant./Qual.1 Total No. species Native Exotic Families
Asia 6/≥47 35 22 13 5
Bangladesh 0/1 3 1 2 2
China 0/1 1 0 1 1
India 4/≥20 27 20 7 5
Indonesia 0/23 5 1 4 1
Malaysia 0/1 1 0 1 1
Philippines 2/2 6 3 3 2
Taiwan 0/1 1 0 1 1
Africa 33/97 50 20 30 7
Cameroon 10/2 12 9 3 3
Canary Islands (Spain)2
Gomera 0/13 18 0 18 4
Gran Canaria 0/10 6 0 6 3
Hierro 0/2 2 0 2 2
La Palma 0/7 3 0 3 1
Tenerife 0/45 19 0 19 5
Ivory Coast 1/1 4 4 0 3
Madagascar 0/1 2 2 0 1
Madeira (Portugal)2 0/6 10 0 10 3
Seychelles 0/1 1 0 1 1
South Africa 6/8 5 0 5 3
Uganda 6/1 5 5 0 3
North America 12/16 14 7 7 4
Bermuda 0/2 2 0 2 1
Mexico 12/14 12 5 7 4
Central America/Caribbean 53/≥17 10 4 6 4
Costa Rica ≥5/1 1 0 1 1
Cuba 1/1 5 2 3 3
Dominica 1/0 2 1? 1 2
Guadeloupe (France) 40/7 4? ? ≥1 ≥1
Martinique (France) 6/6 1 0 1 1
Jamaica 0/1 2 0 2 2
Nicaragua 0/1 2 1 1 2
South America 49/33 20 10 10 6
Brazil 16/16 7 0 7 5
Colombia 32/15 15 8 7 4
Peru 1/1 3 2 1 ≥1
Total 153/210 104 61 43 10

Species richness in individual banana/plantain fields was measured in 166 of the 210 sites, and was generally very low, with an overall mean of 2.7 species per site worldwide, of which less than one (0.5) was native and 2.1 were exotic (full dataset in Cremonesi et al. 2020). Absolute richness in an individual plantation was highest in the banana plantations in Cameroon (Norgrove et al. 2011), where 8 and 10 species were found (Table 4), most of them native. The only other place with such high richness was a plantation in Gomera Island (Laguna de Santiago), where 9 species were found (Talavera 2007), although all of them were exotic. In West Tripura, up to 7 species were found in a banana plantation (Dhar and Chaudhuri 2018), but most plantations in the world had less than 3 species (~70% of sites), and the highest proportion was of sites with only 1 species (~30% of sites).

There was a clear positive relationship between the number of sites sampled in each country and the total number of species encountered (r = 0.7, p< 0.01), particularly for exotic (r = 0.78, p < 0.01) species (Fig. 3A). Although also positive, this relationship was not significant for native species. Nonetheless, the species accumulation curve for native species for all sampling sites in the world revealed a steep slope, that contrasts with the flattened-out accumulation curves for total and exotic species (Fig. 3B). This indicates that greater sampling efforts, particularly in more low-input production systems, especially in tropical countries with high earthworm biodiversity such as Ecuador (no studies with earthworms identified yet), Brazil and Colombia (Brown and James 2007; Feijoo 2007; Zicsi 2007) will certainly increase the number of species known from banana/plantain fields. Greater sampling efforts are also needed in other tropical countries with important plantain/banana production (FAO 2018), particularly when intercropped or in agroforestry systems (Norgrove et al. 2011; Norgrove and Hauser 2014), and where mostly native earthworm species may inhabit these fields, such as seen for Cameroon, Uganda and Ivory Coast. This phenomenon may likely also be applicable to other Western, Central and Eastern African countries, as well as many other Asian and Pacific countries, but the paucity of available data impedes further speculation.

Figure 3. 

A Relationship between species richness (total, native, and exotic species) and the number of sampling sites in each world country (data from Table 5) and B Species accumulation curves for total, native and exotic species, depending on the number of sampling sites across the world. Linear regression equations and the value and significance (p value, with ** indicating p< 0.01) of the Pearson correlation coefficient (r) are provided in (A).

Of the over 100 species found in banana and plantain fields worldwide, most belonged to the Megascolecidae (22%), Lumbricidae (17%) and Acanthodrilidae (16%) families (Cremonesi et al. 2020). These widespread exotic and often invasive species are found throughout the tropics and subtropics, and include several Amynthas and Metaphire spp. (Blakemore 2002). The most consistently recorded megascolecids were A. gracilis (6% of all records), Amynthas morrisi (Beddard, 1892) (5%), Pithemera bicincta (Perrier, 1875) (4%) and Metaphire californica (Kingerg, 1867), Perionyx excavatus Perrier, 1872 and Polypheretima elongata (Perrier, 1872) (all with 2% each) (Cremonesi et al. 2020). These megascolecids were found in over 15 countries, and were especially frequent in the Canary Islands. All of the lumbricids reported were exotic, and mainly found in the Canary and Madeira Islands (Spain, Portugal), with Aporrectodea rosea (Savigny, 1826) and Eisenia andrei Bouché, 1972 (both with ~4%) and Bimastos rubidus (Savigny, 1826) (3%) being the most frequently reported. Various octochaetid Dichogaster spp. of the Benhamiinae subfamily, i.e., Dichogaster (Diplothecodrilus) affinis (Michaelsen, 1890), D. (D.) bolaui (Michaelsen, 1891) and D. (D.) saliens (Beddard, 1893) (all with around 2% each) and the acanthodrilinae Microscolex spp., i.e., Microscolex phosphoreus (Dugés, 1837) with 3% and M. dubius (Fletcher, 1887) with 2% of records, were the most reported acanthodrilids. The Dichogaster spp. were found in 11 countries, mainly in Latin America and the Canary Islands, while the Microscolex spp. were found only in the Canary Island banana plantations. Similarly, the ocnerodrilid Ocnerodrilus occidentalis Eisen, 1878 with 6% of all records, was found in three countries (Brazil, Portugal, Spain), but most frequently in the Canary Islands.

The most commonly encountered earthworm species in banana plantations was P. corethrurus (11%), found in 15 countries, mainly in Latin America, but also in places as far away as South Africa, India, Bangladesh, Malaysia, Philippines and Taiwan. Interestingly, 37 out of 54 sites (69%) that identified earthworm species reported P. corethrurus as dominant in the banana plantations (Table 3).

Although P. corethrurus may affect soil physical properties negatively by increasing soil compaction under some conditions, it can also positively affect biogeochemical processes, microbial activity, plant production, and soil recovery (see review in Taheri et al. 2018). Furthermore, this species is known to reduce plant-parasitic nematode incidence in banana plants (Loranger-Merciris et al. 2012), and has also been known to promote beneficial plant growth-promoting bacteria in the rhizosphere (Braga et al. 2015). Hence, further work is warranted on the potential beneficial impacts of the presence and populations of P. corethrurus on banana plants, particularly considering its widespread distribution and high abundance in some locations (e.g., Costa Rica, Brazil, Guadeloupe, Martinique, Mexico). Several megascolecids such as A. gracilis are also known to affect soil physical and chemical properties in annual cropping systems (e.g., Peixoto and Marochi 1996; Bartz et al. 2010) as well as crop production (Brown et al. 1999), but little is known of their effects on banana plants. The latter statement is also valid for all of the other species most commonly found in banana plantations.

A total of 31 studies performed in 153 sites and 15 countries (Table 5) had quantitative earthworm data (on abundance and/or biomass) taken mainly by hand sorting soil monoliths of variable size (mostly 25 x 25 cm but sometimes larger, e.g., 50 × 50 cm) and occasionally using liquid extraction (e.g., formalin expulsion). Most of the study sites were in Guadeloupe (N = 40, of which 34 were by Clermont-Dauphin et al. (2004) and Colombia (N = 32; Molina and Feijoo 2017).

Overall earthworm abundance ranged from a minimum of 0 (Figueroa 2019) in an Ecuadorian plantation, to a maximum mean of over 1500 indiv. m-2 in banana plantations in Kwazulu-Natal, South Africa (Dlamini and Haynes 2004). Maximum biomass attained was 453.6 g m-2 for a site in West Tripura, India (Dhar and Chaudhuri 2018). Interestingly, a large number of sites (>50) had abundance values over 100 indiv. m-2, which could be considered quite high for earthworm density in annual agricultural crops (Bartz et al. 2013). Nonetheless, bananas are perennials often cultivated over several cropping cycles, allowing for reduced negative effects of soil preparation, and the soils are also often limed to correct pH and fertilized with inorganic fertilizers (mainly N, P and K) to promote soil fertility and banana production. In these conditions, earthworms present find a soil protected from rainfall impact, as well as frequent organic matter additions through the management of the banana trees, particularly where the residues are left on the soil surface. Consequently, their populations can increase rather rapidly over time, as observed by Okwakol (1994) in Uganda (Table 3).

These high earthworm abundances and biomasses may be contributing significantly to soil processes (bioturbation, nutrient cycling) in banana/plantain fields, as biomasses over 17 g m-2 and above 32 g m-2 are known to lead to moderate (20–40%) and important (>40%) grain production increases, respectively (Brown et al. 1999). Earthworm-induced improvement of plant health and production includes, e.g., plant-parasitic nematode population control (Lafont et al. 2007; Loranger-Merciris et al. 2012), high stable bioaggregate formation, creation of many galleries in the soil and enhanced nutrient mineralization (Lavelle 1997), all factors that deserve future attention. On the other hand, low earthworm abundance may be an indicator of soil degradation, or the use of inappropriate management practices, such as soil inversion or toxic pesticide use (Demetrio et al. 2019). This type of information could be used to help farmers with their management decisions, such as reduction in nematicide applications that reduce earthworm populations (Clermont-Dauphin et al. 2004).

Finally, 18 of the major banana-producing countries in the world (34 countries with >30,000 ha in production, or >1 Million T bananas produced yr-1; FAO 2018) were not examined in the present review due to lack of data. Hence, further sampling efforts are needed in order to provide adequate information on earthworm abundance and biodiversity in banana plantations in these countries, and to complement those reported here but with low sample intensity, particularly focusing on the presence of native species and/or large earthworm abundances, and to identify the reasons for these phenomena and their consequences for banana production and biodiversity conservation.

Conclusions

Earthworms are an important component of banana and plantain fields worldwide and deserve further attention by taxonomists, ecologists and agronomists. Under some conditions, especially in lower-input polycultures, their abundance and biomass may reach high values and contribute significantly to soil processes and plant production. More than 70 studies performed in over 200 banana plantations of 28 countries found >100 species (around 60% of them native) from 10 families, although species richness in each sited tended to be low (generally <3 species) and exotic species predominated (particularly P. corethrurus). However, as many important banana-producing countries have not yet been evaluated, further work is warranted in order to better understand the earthworm communities and their functional roles in plantain/banana fields, and the role of management practices in affecting their populations and diversity worldwide.

Acknowledgements

This study was part of the PhD of the first author at the Federal University of Paraná, where both he and AS received CAPES scholarships. We also gratefully acknowledge financial support from the Fundo Estadual de Recursos Hídricos (Proc. FEHIDRO 102/2016), the CNPq for Profix support (441930/2020-4) and a fellowship to GGB (310690/2017-0), Embrapa Forestry and UFPR for laboratorial and logistical support, and the farmers for permission to sample on their properties.

References

  • Agüero R, Rojas S, Pérez L (2002) Poblaciones de lombrices bajo seis estrategias de manejo de malezas en una plantación de banano. Agronomía Mesoamericana 13(1): 25–29. https://doi.org/10.15517/am.v13i1.13234
  • Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility: a handbook of methods (2nd Edn.). CAB International, Wallingford, 171 pp.
  • Avilés DFV (2017) Biodiversidad intraespecífica varietal para mejorar ambientes degradados por monocultivos en Musáceas, como medida de control de plagas y enfermedades. PhD thesis, Universitat Autònoma de Barcelona, Spain.
  • Baretta D, Santos JCP, Segat JC, Geremia EV, Oliveira Filho LD, Alves MV (2011) Fauna edáfica e qualidade do solo. Tópicos em Ciência do Solo 7: 119–170.
  • Barois I (1992) Mucus production and microbial activity in the gut of two species of Amynthas (Megascolecidae) from cold and warm tropical climates. Soil Biology and Biochemistry 24(12): 1507–1510. https://doi.org/10.1016/0038-0717(92)90141-J
  • Barois I, Cadet P, Albrecht A, Lavelle P (1988) Système de culture et faune des sols: quelques données. In: Feller C (Ed.) Fertilité des sols dans les agricultures paysannes caribéennes: effet des restitutions organiques. ORSTOM, Martinique, 85–96.
  • Bartz MLC, Costa AC, Tormena CA, Souza Júnior IG, Brown GG (2010) Sobrevivência, produção e atributos químicos de coprólitos de duas espécies de minhocas (Pontoscolex corethrurus: Glossoscolecidae e Amynthas gracilis: Megascolecidae) em solos sob diferentes sistemas de manejo. Acta Zoológica Mexicana (nueva série) 26: 261–280.
  • Blakemore RJ (2002) Cosmopolitan Earthworms – An Eco-Taxonomic Guide to the Peregrine Species of the World. VermEcology, Kippax, 426 pp.
  • Block W, Banage WB (1968) Population density and biomass of earthworms in some Uganda soils. Revue d’Écologie et Biologie du Sol 3: 515–521.
  • Braga LPP, Yoshiura CA, Borges CD, Horn MA, Brown GG, Drake HL, Tsai SM (2015) Disentangling the influence of earthworms in sugarcane rhizosphere. Scientific Reports 6: e38923. https://doi.org/10.1038/srep38923
  • Brown GG, James SW (2007) Ecologia, biodiversidade e biogeografia das minhocas no Brasil. In: Brown GG, Fragoso C (Eds) Minhocas na América Latina: Biodiversidade e ecologia. Embrapa Soja, Londrina, 297–381.
  • Brown GG, Domínguez J (2010) Uso das minhocas como bioindicadoras ambientais: princípios e práticas – o 3° encontro latino americano de ecologia e taxonomia de oligoquetas (ELAETAO3). Acta Zoológica Mexicana (nueva série) 26: 1–18. https://doi.org/10.21829/azm.2010.262874
  • Brown GG, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S, Barois I, Lavelle P, Blanchart E, Blakemore RJ, Spain AV, Boyer J (1999) Effects of earthworms on plant production in the tropics. In: Lavelle P, Brussaard L, Hendrix P (Eds) Earthworm management in tropical agroecosystems. CABI, Wallingford, 87–147.
  • Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. European Journal of Soil Biology 36(1): 177–198. https://doi.org/10.1016/S1164-5563(00)01062-1
  • Brown GG, Maschio W, Froufe LCM (2009) Macrofauna do solo em sistemas agroflorestais e Mata Atlântica em regeneração nos Municípios de Barra do Turvo, SP, e Adrianópolis, PR. Embrapa Florestas, Documentos No. 184, Colombo, 51 pp.
  • Brown GG, James SW, Pasini A, Nunes DH, Benito NP, Martins PT, Sautter KD (2006) Exotic, peregrine, and invasive earthworms in Brazil: diversity, distribution and effects on soils and plants. Caribbean Journal of Science 42: 111–117.
  • Brown GG, Callaham MA, Niva CC, Feijoo A, Sautter KD, James SW, Fragoso C, Pasini A, Schmelz RM (2013) Terrestrial oligochaete research in Latin America: The importance of the Latin American Meetings on Oligochaete Ecology and Taxonomy. Applied Soil Ecology 69: 2–12. https://doi.org/10.1016/j.apsoil.2012.12.006
  • Bueno E (2003) Brasil: uma História (2nd ed.). Ática, São Paulo, 480 pp.
  • Bünemann EK, Bongiorno G, Bai Z, Creamer RE, De Deyn G, De Goede R, Pulleman M (2018) Soil quality–A critical review. Soil Biology and Biochemistry 120: 105–125.
  • Burac M, Gros-Desormeaux JR, Lalubie G, Lesales T, Angin B, Breuil M, Picard R (2018) Evaluation et Suivi de la Biodiversité dans les Bananeraies: Guadeloupe et Martinique. Cihense, France, 183 pp. https://doi.org/10.1016/j.soilbio.2018.01.030
  • Campbell CW (2018) Tropical fruits and nuts. In: Martin FW (Ed.) Handbook of Tropical Food Crops. CRC Press, Boca Raton, 235–274.
  • Capowiez Y, Samartino S, Cadoux S, Bouchant P, Richard G, Boizard H (2012) Role of earthworms in regenerating soil structure after compaction in reduced tillage systems. Soil Biology and Biochemistry 55: 93–103. https://doi.org/10.1016/j.soilbio.2012.06.013
  • Castillo FX, Vera LO (2000) Comparación de la biodiversidad de la macrofauna de suelos bananeros con manejo convencional y orgánico en EARTH. Dissertation, Guácimo, Costa Rica: EARTH University.
  • Clermont-Dauphin C, Cabidoche YM, Meynard JM (2004) Effects of intensive monocropping of bananas on properties of volcanic soils in the uplands of the French West Indies. Soil Use and Management 2(2): 105–113. https://doi.org/10.1079/SUM2003231
  • Coelho GC (2017) Ecosystem services in Brazilian’s southern agroforestry systems. Tropical and Subtropical Agroecosystems 20(3): 475–492.
  • Cordeiro GPL, Amorim M, Ronquim CC (2017) Mudança de uso e ocupação da terra no município de registro, SP, entre os anos de 1987 e 2017. Embrapa Territorial. 11° Congresso Interinstitucional de Iniciação Científica, Campinas, July 2017, Instituto Agronômico (IAC), Campinas, 10 pp.
  • Cordeiro ZJM, Matos AD, Meissner Filho PE (2004) Doenças e métodos de controle. In: Borges AL, da Silva Souza L (Eds) O cultivo da bananeira. Cruz das Almas: Embrapa Mandioca e Fruticultura, 146–182.
  • Cornwell E (2014) Effects of different agricultural systems on soil quality in Northern Limón province, Costa Rica. Revista de Biologia Tropical 62(3): 887–897. https://doi.org/10.15517/rbt.v62i3.14062
  • Correia MEF, Lima DA, Franco AA, Campello EFC, Tavares SRL (2001) Comunidades da macrofauna do solo em áreas de floresta secundária de mata atlântica no Estado do Rio de Janeiro. in Anais do V Congresso de Ecologia do Brasil Ambiente x Sociedade, 2001. Sociedade de Ecologia do Brasil, Porto Alegre.
  • Cremonesi MV, Santos A, Rozane D, Bartz MLC, Brown GG (2020) Earthworm species in Musa spp. (plantain and banana) plantations worldwide. Mendeley Data, V1. http://dx.doi.org/10.17632/p8ywsnj8c5.1
  • Csuzdi C, Razafindrakoto M, Hong Y (2017) Three new species of Kynotus from the central highlands of Madagascar (Clitellata, Megadrili). European Journal of Taxonomy 336: 1–14. https://doi.org/10.5852/ejt.2017.336
  • da Silva RF, de Aquino AM, Mercante FM, de Fátima Guimarães M (2006) Macrofauna invertebrada do solo sob diferentes sistemas de produção em Latossolo da Região do Cerrado. Pesquisa Agropecuária Brasileira 41(4): 697–704. https://doi.org/10.1590/S0100-204X2006000400022
  • Dale J, James A, Paul JY, Khanna H, Smith M, Peraza-Echeverria S, Harding R (2017) Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nature Communications 8(1): 1–8. https://doi.org/10.1038/s41467-017-01670-6
  • Demetrio WC, Ribeiro RH, Nadolny H, Bartz MLC, Brown GG (2019) Earthworms in Brazilian no-tillage agriculture: Current status and future challenges. European Journal of Soil Science 71: 988–1005. https://doi.org/10.1111/ejss.12918
  • Dhar S, Chaudhuri PS (2018) Earthworm communities in banana (Musa paradisiaca) and paddy (Oryza sativa) plantations of west Tripura, India. In: Solanki GS (Ed.) Biodiversity Conservation: Strategies and Applications. South Eastern Book Agencies, 303–320.
  • Dlamini TC, Haynes RJ (2004) Influence of agricultural land use on the size and composition of earthworm communities in northern KwaZulu-Natal, South Africa. Applied Soil Ecology 27(1): 77–88. https://doi.org/10.1016/j.apsoil.2004.02.003
  • Feijoo A (2007) Registros históricos y listado de las lombrices de tierra de Colombia. In: Brown GG, Fragoso C (Eds) Minhocas na América Latina: biodiversidade e ecologia. Embrapa Soja, Londrina, 141–153.
  • Feijoo A, Zuluaga LF, Molina LJ (2018) New species and records of earthworms (Annelida, Oligochaeta) in plantain cropping systems in Colombia’s coffee-growing region. Zootaxa 4496(1): 448–458. https://doi.org/10.11646/zootaxa.4496.1.34
  • Fernandes JO, Uehara-Prado M, Brown GG (2010) Minhocas exóticas como indicadoras de perturbação antrópica em áreas de floresta atlântica. Acta Zoológica Mexicana (nueva série) 26: 211–217. https://doi.org/10.21829/azm.2010.262889
  • Figueroa DMN (2019) Comparación de la macrofauna del suelo en agro sistemas de plátano en Santo Domingo y El Carmen. PhD thesis, Ecuador: Universidad Tecnológica Equinoccial, Santo Domingo.
  • Fiuza DTF, Kusdra JF, Fiuza SDS (2012) Maize growth in soil with activity of giant earthworms Chibui bari (Oligochaeta: Glossoscolecidae). Revista Brasileira de Ciência do Solo 36(2): 359–366. https://doi.org/10.1590/S0100-06832012000200005
  • Fragoso C, Rojas P (2007) Two new species of the earthworm genus Balanteodrilus (Oligochaeta: Acanthodrilidae) from Eastern Mexico. Megadrilogica 11(10): 107–114.
  • Fusilero MA, Mangubat J, Ragas RE, Baguinon N, Taya H, Rasco-jr E (2013) Weed management systems and other factors affecting the earthworm population in a banana plantation. European Journal of Soil Biology 56(1): 89–94. https://doi.org/10.1016/j.ejsobi.2013.03.002
  • Garcia BNR, Vieira TA, de Assis Oliveira F (2017) Tree and shrub diversity in agroforestry homegardens in rural community in eastern amazon. Floresta 47(4): 543–552. https://doi.org/10.5380/rf.v47i4.48196
  • Gasparotto L, Pereira JCR, Hanada RE, Montarroyos AVV (2006) Sigatoka-negra da bananeira. Manaus: Embrapa Amazônia Ocidental, 18 pp.
  • Geissen V, Peña-Peña K, Huerta E (2009) Effects of different land use on soil chemical properties, decomposition rate and earthworm communities in tropical Mexico. Pedobiologia 53(1): 75–86. https://doi.org/10.1016/j.pedobi.2009.03.004
  • González WV, Hernández IM, Espinales SC (2015) Evaluación de la diversidad de la macrofauna en las fincas plataneras Cuerno Enano (AAB) en los municipios de León y Posoltega en el ciclo agricola 2014. Undergraduate thesis, Nicaragua: Universidad Nacional Autónoma de Nicaragua, León.
  • Guerra RT, Silva EG (1994) Estudo das comunidades de minhocas (Annelida, Oligochaeta) em alguns ambientes terrestres do Estado da Paraíba. Revista Nordestina de Biologia 9: 209–223
  • Harvey CA, Villalobos JAG (2007) Agroforestry systems conserve species-rich but modified assemblages of tropical birds and bats. Biodiversity and Conservation 16(8): 2257–2292. https://doi.org/10.1007/s10531-007-9194-2
  • Huerta E, Rodríguez-Olán J, Evia-Castillo I, Montejo-Meneses E, de la Cruz-Mondragón M, García-Hernández R (2005) La diversidad de lombrices de tierra (Annelida, Oligochaeta) en el estado de Tabasco, México. Ecosistemas y Recursos Agropecuarios 21(42): 73–83.
  • Huerta E, Rodríguez-Olan J, Evia-Castillo I, Montejo-Meneses E, de la Cruz-Mondragón M, García-Hernández R, Uribe S (2007) Earthworms and soil properties in Tabasco, Mexico. European Journal of Soil Biology 43: 190–195. https://doi.org/10.1016/j.ejsobi.2007.08.024
  • Huerta E, Gaspar-Genico JA, Jarquin-Sánchez A (2013) Biodiversity of Oligochaeta in traditional banana plantations of Musa acuminata in Tabasco, Mexico. In: Pavlicek T, Cardet P, Almeida MT, Pascoal C, Cássio F (Eds) Advances in Earthworm Taxonomy VI (Annelida: Oligochaeta). Kasparek Verlag, Germany, 107–133.
  • IUSS/WRB [International Union of Soil Sciences and Word Reference Base] (2015) World Reference Base for Soil Resources 2014, update 2015: International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome, 192 pp.
  • Kanmegne J (2004) Slash and burn agriculture in the humid forest zone of southern Cameroon: soil quality dynamics, improved fallow management and farmers’ perceptions. PhD thesis, Wageningen University, Wageningen.
  • Kumar TSH, Sreepada KS, Narayanan SP, Reynolds JW (2018) Megadrile earthworms (Annelida: Oligochaeta) around Udupi Power Corporation Limited (UPCL), Udupi District, Karnataka, South-West Coast of India. Megadrilogica 23(5): 79–91.
  • Lafont A, Risède JM, Loranger-Merciris G, Clermont-Dauphin C, Dorel M, Rhino B, Lavelle P (2007) Effects of the earthworm Pontoscolex corethrurus on banana plants infected or not with the plant-parasitic nematode Radopholus similis. Pedobiologia 51(4): 311–318. https://doi.org/10.1016/j.pedobi.2007.05.004
  • Lalthanzara H (2007) Ecological studies on earthworm population in agroforestry system of Mizoram. PhD thesis, Mizoram University, Mizoram.
  • Lavelle P (1997) Diversity of Soil fauna and ecosystem function. Biology International 33(1): 3–16.
  • Loranger-Merciris G, Cabidoche YM, Deloné B, Quénéhervné P, Ozier-Lafointaine H (2012) How earthworm activities affect banana plant response to nematodes parasitism. Applied Soil Ecology 52: 1–8. https://doi.org/10.1016/j.apsoil.2011.10.003
  • Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Valantin-Morison M (2009) Mixing plant species in cropping systems: concepts, tools and models: a review. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (Eds) Sustainable agriculture. Springer, Dordrecht, 329–352. https://doi.org/10.1007/978-90-481-2666-8_22
  • Mariappan V, Karthikairaj K, Isaiarasu L (2013) Relationship between earthworm abundance and soil quality of different cultivated lands in Rajapalayam, Tamilnadu. World Applied Sciences Journal 27(10): 1278–1281.
  • Martínez-Leiva MA (2002) Comunidades de oligoquetos (Annelida: Oligochaeta) en tres ecosistemas con diferente grado de perturbación en Cuba. PhD thesis, Instituto de Ecología y Sistemática, La Habana.
  • Maschio W, Brown G, Seoane C, Froufe L (2010) Abundância e diversidade de minhocas em agroecossistemas da Mata Atlântica nos municípios do Litoral Paranaense-Morretes e Antonina. In Anais do 4° Encontro Latino-Americano de Ecologia e Taxonomia de Oligoquetas (ELAETAO4): Minhocas como bioindicadoras ambientais: princípios e práticas. Embrapa Florestas, Série Documentos No. 199, Colombo, 4 pp.
  • Michaelsen W (1900) Das Tierreich Oligochaeta. Friedländer and Sohn, Berlin, 575 pp.
  • Molina JR, Feijoo AM (2017) Uso del suelo y efecto sobre propiedades químicas, macrofauna en cultivo de plátano andes centrales. Suelos Ecuatoriales 47(1, 2): 16–24.
  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities, Nature 403: 853–858. https://doi.org/10.1038/35002501
  • Nair KV, Manazhy J, Manazhy A, Reynolds J (2007) Earthworm Annelida Oligochaeta fauna of Kerala, India: 1. Some species from Thiruvaanthapuram Corporation. Megadrilogica 11(8): 85–90.
  • Norgrove L, Csuzdi C, Hauser S (2011) Effects of cropping and tree density on earthworm community composition and densities in central Cameroon. Applied Soil Ecology 49: 268–271. https://doi.org/10.1016/j.apsoil.2011.05.008
  • Nunes DH, Pasini A, Benito NP, Brown GG (2007) Minhocas como bioindicadoras da qualidade ambiental. Um estudo de caso na região de Jaguapitã, PR, Brasil. In: Brown GG, Fragoso C (Eds) Minhocas na América Latina: biodiversidade e ecologia. Embrapa Soja, Londrina, 467–480.
  • OECD-FAO (2019) OECD-FAO Agricultural Outlook 2019–2028. OECD Publishing, Paris/Food and Agriculture Organization of the United Nations, Rome.
  • Oliveira MAF, Maniesi V, Teixeira W, Daitx EC (2002) Caracterização isotópica de metabasitos e anfibolitos dos grupos Açungui e Setuva na porção sul da faixa Ribeira. Geologia USP Série Científica 2(1): 161–170. https://doi.org/10.5327/S1519-874X2002000100013
  • Pashanasi B (2007) Las lombrices de tierra en diferentes ecosistemas de la Amazonia Peruana. In: Brown GG, Fragoso C (Eds) Minhocas na América Latina: biodiversidade e ecologia. Embrapa Soja, Londrina, 207–214.
  • Paul C, Griess VC, Havardi-Burger N, Weber M (2015) Timber-based agrisilviculture improves financial viability of hardwood plantations: a case study from Panama. Agroforestry Systems 89(2): 217–235. https://doi.org/10.1007/s10457-014-9755-9
  • Peixoto RDG, Marochi AI (1996) A influência da minhoca Pheretima sp. nas propriedades de um latossolo vermelho escuro álico e no desenvolvimento de culturas em sistema de plantio direto, em Arapoti-PR. Revista Plantio Direto 35: 23–25.
  • Plisko JD (2001) Notes on the occurrence of the introduced earthworm Pontoscolex corethrurus (Müller, 1857) in South Africa (Oligochaeta: Glossoscolecidae). African Invertebrates 42(1): 323–334.
  • Quintero EIQ (2010) Insumos e indicadores biológicos em agrossistemas com bananeiras. PhD thesis, Universidade Federal Rural do Rio de Janeiro, Seropédica.
  • Razafindrakoto M, Csuzdi C, James S, Blanchart E (2017) New earthworms from Madagascar with key to the Kynotus species (Oligochaeta: Kynotidae). Zoologischer Anzeiger 268: 126–135. https://doi.org/10.1016/j.jcz.2016.08.001
  • Reynolds JW, Fragoso C (2004) The earthworms (Oligochaeta: Acanthodrilidae, Eudrilidae, Glossoscolecidae, Lumbricidae, Megascolecidae and Ocnerodrilidae) of Bermuda. Megadrilogica 10(4): 17–26.
  • Reynolds JW, Julka JM, Khan MN (1995) Additional earthworm records from Bangladesh (Oligochaeta: Glossoscolecidae, Megascolecidae, Moniligastridae, Ocnerodrilidae and Octochaetidae). Megadrilogica 6(6): 51–64.
  • Ribeiro M, Metzger J, Martensen A, Ponzoni F, Hirota M (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
  • Righi G (1988) Uma coleção de Oligochaeta da Amazônia Brasileira. Papéis Avulsos de Zoologia (São Paulo) 36(30): 337–351.
  • Righi G (1990) Minhocas de Mato Grosso e Rondônia. Relatório de Pesquisa No. 12. Programa Polonoroeste. CNPq/AED, Brasília, 157 pp.
  • Römbke J, Schmidt P, Höfer H (2009) The earthworm fauna of regenerating forests and anthropogenic habitats in the coastal region of Paraná. Pesquisa Agropecuária Brasileira 44(8): 1040–1049. https://doi.org/10.1590/S0100-204X2009000800037
  • Salazar-Díaz R, Tixier P (2017) Effect of plant diversity on income generated by agroforestry systems in Talamanca, Costa Rica. Agroforestry Systems 93(2): 571–580. https://doi.org/10.1007/s10457-017-0151-0
  • Sherlock E, Lee S, Mcphee S, Steer M, Maes JM, Csuzdi C (2011) The first earthworm collections from Nicaragua with description of two new species (Oligochaeta). Zootaxa 2732(1): 49–58. https://doi.org/10.11646/zootaxa.2732.1.4
  • Siddaraju M, Sreepada KS, Krishna MP (2013) Recorded distribution of earthworms of the family Octochaetidae in Dakshina Kannada district, south west coast, Karnataka. International Journal of Scientific and Research Publications 3(6): 1–8.
  • Siddaraju M, Sreepada KS, Reynolds JW (2010) Checklist of earthworms (Annelida: Oligochaeta) from Dakshina Kannada, Karnataka South West India. Megadrilogica 15(5): 65–76.
  • Sims RW (1987) New species and records of earthworms from Jamaica with notes on the genus Eutrigaster Cognetti, 1904 (Octochaetidae: Oligochaeta). Journal of Natural History 21(2): 429–441. https://doi.org/10.1080/00222938700771101
  • Sun J, Jiang JB, Qiu JP (2012) Four new species of the Amynthas corticis-group (Oligochaeta: Megascolecidae) from Hainan Island, China. Zootaxa 3458(1): 149–158. https://doi.org/10.11646/zootaxa.3458.1.8
  • Taheri S, Pelosi C, Dupont L (2018) Harmful or useful? A case study of the exotic peregrine earthworm morphospecies Pontoscolex corethrurus. Soil Biology and Biochemistry 116(1): 277–289. https://doi.org/10.1016/j.soilbio.2017.10.030
  • Talavera JA (1990a) Considerations about Ocnerodrilus occidentalis (Oligochaeta: Ocnerodrilidae) in the Canary Islands. Bonner Zoologische Beitrage 41: 81–87.
  • Talavera JA (1992b) Octochaetid earthworms of the Canary Islands. Bonner Zoologische Beiträge 43(2): 339–348.
  • Talavera JA (2011) New earthworm records for Macaronesia with observations on the species, ecological characteristics and colonization history. Pedobiologia 54(5–6): 301–308. https://doi.org/10.1016/j.pedobi.2011.06.001
  • Talavera JA, Pérez DI (2009) Occurrence of the Genus Microscolex (Oligochaeta, Acanthodrilidae) at Western Canary Islands. Bonner Zoologische Beiträge 56(1/2): 37–41.
  • Teng SK, Aziz NAA, Mustafa M, Laboh R, Ismail IS, Devi S (2016) Potential role of endogeic earthworm Pontoscolex corethrurus in remediating banana blood disease: a preliminary observation. European Journal of Plant Pathology 145(2): 321–330. https://doi.org/10.1007/s10658-015-0846-x
  • Timm ES, Pardo LH, Coello RP, Navarrete TC, Villegas ON, Ordonez ES (2016) Identification of differentially-expressed genes in response to Mycosphaerella fijiensis in the resistant Musa accession ‘Calcutta-4’using suppression subtractive hybridization. PLoS ONE 11(8): 32–41. https://doi.org/10.1371/journal.pone.0160083
  • Tondoh JE (1994) Effet des divers modes d’utilisation sur le peuplement animal des sols dans la région de Lamto (Côte d’Ivoire). Gestion des systèmes agro-sylvo-pastoraux tropicaux. Thesis DESS, France: Université Paris XII.
  • Tondoh JE (2007) Effet de la mise en culture des forêts secondaires sur les peuplements de macroinvertébrés du sol dans la zone de contact forêt-savane de Côte d’Ivoire. Sciences & Nature 4(2): 197–204. https://doi.org/10.4314/scinat.v4i2.42144
  • Tsai CF, Shen HP, Tsai SC (2000) Occurrence of the exotic earthworm Pontoscolex corethrurus (Müller) (Glossoscolecidae: Oligochaeta) in Taiwan. Endemic Species Research 2: 68–73.
  • Zicsi A (2007) An annotated checklist of the earthworms of Ecuador (Oligochaeta). Earthworms from South Amerca 42. In: Brown GG, Fragoso C (Eds) Minhocas na América Latina: biodiversidade e ecologia. Embrapa Soja, Londrina, 175–199.