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Earthworm species in spp. plantations in Brazil and worldwide
DOI 10.3897/zookeys.1033.54331 , Volume: 1033 , Issue: null , Pages: 1-33
Article Type: research-article, Article History
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 (, ) belonging to two families (, ) 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 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 , and 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
Cremonesi, Santos, Rozane, Bartz, and Brown: Earthworm species in Musa spp. plantations in Brazil and worldwide

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.
SiteCountySystemWN1Age (yrs)Latitude, LongitudeSoil types
1EldoradoBanana34450 24°29'35"S, 48°02'10"W Cambisols
2EldoradoAtlantic forest344> 50 24°30'09"S, 48°02'30"W Cambisols
3Sete BarrasBanana42215 24°23'34"S, 47°53'51"W Cambisols
4Sete BarrasAtlantic forest422> 50 24°23'30"S, 47°53'22"W Cambisols
5RegistroBanana37940 24°26'56"S, 47°49'41"W Cambisols / Histosols
6RegistroAtlantic forest38945 24°26'47"S, 47°49'23"W Cambisols / Histosols
1Official cartographic number for the watershed.

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 speciesEldoradoSete BarrasRegistro
BananaAtlantic ForestBananaAtlantic ForestBananaAtlantic Forest
Megascolecidae
Amynthas gracilis +++
Megascolecidae juveniles++++
Rhinodrilidae
Pontoscolex corethrurus ++++++
Rhinodrilidae juveniles+
Species Richness 222≥222

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).
CountryLocationAbundance (indiv. m–2)Biomass (g m–2)Predominant speciesReferences
BrazilAntonina (Monoculture)7135.1 P. corethrurus Römbke et al. (2009)
22195.7 P. corethrurus
8623.8 P. corethrurus
Antonina (Agroforestry)17377.1 P. corethrurus
33869.6 P. corethrurus
11743.5 P. corethrurus
21a3.1b P. corethrurus Maschio et al. (2010)
293a34.9b P. corethrurus
Adrianópolis (Agroforestry)211–413c37–71.2c P. corethrurus Brown et al. (2009)
Barra do Turvo (Agroforestry)99–176c11.2–17.3c P. corethrurus
229–459c48.3–117.4c P. corethrurus
Casimiro de Abreu~205–440cNA Quintero (2010)
Paraty167NA Correia et al. (2001)
Eldorado83.9 P. corethrurus This study
Sete Barras139.0 P. corethrurus
Registro62.5 P. corethrurus
CameroonMbalmayo Forest Reserve70Legonodrilus sp. nov. 1, Eminoscolex lamani Norgrove et al. (2011)
121Legonodrilus sp. nov. 1, Eminoscolex lamani
Campo Ma’an16–92dNA Kanmegne (2004)
ColombiaQuindío (Armenia)9–16e1.2–3.0eNAfMolina and Feijoo (2016)
Costa RicaLimón Province (Finca San Pablo)83–812gNA Agüero et al. (2002)
Pueblo Nuevo de Villa Franca de Guácimo, Limón296.2NA Cornwell (2014)
Cahuita350144.6 P. corethrurus Lapied and Lavelle (2003)
Guadeloupe (France)Basse-Terre Andosols (mean of 23 sites)8823NA Clermont-Dauphin et al. (2004)
Basse Terre Nitisols (mean of 11 sites)5417.5NA
Capesterre-Belle-Eau (Gloria Bas)16827.6 P. corethrurus Burac et al. (2018)
Capesterre-Belle-Eau (Source)28842.2 P. corethrurus
Capesterre-Belle-Eau (Bergerie)18833.6 P. corethrurus
Baillif (Sextius)336112 P. corethrurus
Baillif (Grand Canon)19270.8 P. corethrurus
Saint-Claude (Saut d’Eau)36446 P. corethrurus
EcuadorLatacunga (La Maná)168NA Avilés (2017)
111NA
Manabí (El Carmen)78NA
37NA
El Carmen (Cijádi)0–145hNA Figueroa (2019)
El Carmen (Nápoles)34–144hNA
Santo Domingo de los Tsáchilas (Santa Patrícia)83–548hNA
Santo Domingo de los Tsáchilas (La Floresta)22–150hNA
IndiaWest Tripura16–656i4.8–453.6i P. corethrurus Dhar and Chaudhuri (2018)
Rajapalayam11648.8Lampito mauritii, Perionyx excavatus Mariappan et al. (2013)
Ivory CoastTaabo (Lamto reservation)1868.5 Reginaldia anomala Tondoh (1994, 2007)
Martinique (France)Le Lorrain (Feugère)24467.6 P. corethrurus Burac et al. (2018)
Le Lorrain (Bellevue)15243.6 P. corethrurus
Le Lorrain (Limite)5226 P. corethrurus
L’Ajoupa-Bouillon (Allée Domergue 3)14849.6 P. corethrurus
Basse-Pointe (Fromager Rivière)8026 P. corethrurus
Basse-Pointe (Dantu Bas)409 P. corethrurus
MexicoTabasco, Pablo L. Sidar2510P. corethrurus, Lavellodrilus bonampakensis Huerta et al. (2005)
Tabasco, Teapa11620.8P. corethrurus, Drawida barwelli, Polypheretima elongata Geissen et al. (2009)
11711.8Balanteodrilus pearsei, Drawida barwelli
9440.4Balanteodrilus pearsei, Polypheretima elongata
12535.6P. corethrurus, Drawida barwelli
258.8P. corethrurus, Lavellodrilus bonampakensis Huerta et al. (2007)
~3502.5 Diplotrema murchiei Huerta et al. (2013)
~3509.3 P. corethrurus
~47016.2 P. corethrurus
~10011 P. corethrurus
~802.8 P. corethrurus
~1250.8Dichogaster sp.
NicaraguaLeón (Finca Cony)150NAHernández et al. (2015)
León (Finca San Martín)325NA
León (Finca Santa Isabel)50NA
León (Finca El verdon)65NA
Possoltega (Finca San Joaquin)150NA
Possoltega (Finca Los Ángeles)225NA
Possoltega (Finca Maria de los Ángeles)100NA
Possoltega (Finca Montes Verdes)125NA
PhilippinesDavao (Sumitomo Fruits Corporation)~85–175jNA Fusilero et al. (2013)
~75–215j Metaphire cai
South AfricaKwazulu-Natal (Eshowe)1500k180Amynthas rodericensis, Amynthas minimus, P. corethrurus Dlamini and Haynes (2004)
UgandaKabanyolo University Farm18–207l0.1–9.4lDichogaster sp. 2, Gordiodrilus sp. 1 Block and Banage (1968)
Mabira Forest reserve (1 yr old)130.4NA Okwakol (1994)
(2 yr old)1252.2NA
(3 yr old)1311.3NA
(5 yr old)540.5NA
(20 yr old)1544.2NA
a Earthworm abundance values were corrected from Maschio et al. (2010) that reported earthworm numbers per sample and not per m2. bBiomass values in g m-2 are now included for this study. cMean of dry and wet season samplings, respectively. dMean abundance from eight sites, with four sampled in one year and the other four the subsequent year. eRange of abundance taken from eight replicate farms under four different management practices (totaling 32 plantations) in the Armenia region. f The identification of the earthworm species collected overall in this study (not by plantation type) is published in Feijoo et al. (2018). gRange of abundance found under six weed control treatments (performed on same banana plantation) on five sampling dates; hRange of abundance found on six sampling dates in same plantation. iRange of abundance and biomass found in three banana plantations. jRange of abundance and biomass found on sixteen sampling dates in same plantation. kMean of six banana plantations. lRange of abundance and biomass found on eight sampling dates in same plantation.

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.
CountryLocationManagementCulture typeEarthworm speciesRichnessNative (N) /Exotic (E)References
Bangladesh Lalmonirhat DistrictNANALampito mauritii, Metaphire posthuma, Pontoscolex corethrurus32/1 Reynolds et al. (1995)
Bermuda Paget ParishNANA Amynthas rodericensis 10/1 Reynolds and Fragoso (2004)
Southampton ParishNANA Amynthas hupeiensis 10/1 Reynolds and Fragoso (2004)
Brazil Antonina, PRAgroforestryMonocultureAmynthas corticis, Pontoscolex corethrurus, two other spp.40/4 Römbke et al. (2009)
Antonina, PRAgroforestryMonocultureAmynthas gracilis, Pontoscolex corethrurus, two other spp.40/4 Römbke et al. (2009)
Antonina, PRAgroforestryMonocultureDichogaster spp., Pontoscolex corethrurus40/4 Römbke et al. (2009)
Antonina, PRAgroforestryMonocultureOcnerodrilus occidentalis, Pontoscolex corethrurus, two other spp.40/4 Römbke et al. (2009)
Antonina, PRAgroforestryMonoculturePontoscolex corethrurus, one other sp.20/2 Römbke et al. (2009)
Antonina, PRNAPolyculturePontoscolex corethrurus, one other sp.20/2 Römbke et al. (2009)
Antonina, PRAgroforestryPolycultureDichogaster sp., Pontoscolex corethrurus, and one unidentified sp.3?/2 Maschio et al. (2010)
Antonina, PRAgroforestryPolyculture Pontoscolex corethrurus 10/1 Maschio et al. (2010)
Adrianópolis, PRAgroforestryPolycultureAmynthas gracilis, Pontoscolex corethrurus20/2 Brown et al. (2009)
Barra do Turvo, SPAgroforestryPolycultureAmynthas gracilis, Pontoscolex corethrurus20/2 Brown et al. (2009)
Barra do Turvo, SPAgroforestryPolycultureAmynthas gracilis, Dichogaster sp., Pontoscolex corethrurus30/3 Brown et al. (2009)
Areia, PBNAPolycultureAmynthas gracilis, Dichogaster affinis, Eudrilus eugeniae, Pontoscolex corethrurus40/4 Guerra and Silva (1994)
Eldorado, SPConventionalMonocultureAmynthas gracilis, Pontoscolex corethrurus20/2This study
Jutaí River margin, AMNANA Pontoscolex corethrurus ND0/1 Righi (1990)
Registro, SPConventionalMonocultureAmynthas gracilis, Pontoscolex corethrurus20/2This study
Sete Barras, SPConventionalMonocultureAmynthas gracilis, Pontoscolex corethrurus20/2This study
Cameroon Mbalmayo Forest Reserve (low density cover)Organic AgroforestryMonocultureDichogaster hauseri, Eminoscolex lamani, Eudrilidae gen. et sp. nov.1 & 2, Legonodrilus sp. nov.1, Malodrilus kamerunensis, Nematogenia panamaensis, Rosadrilus camerunensis87/1 Norgrove et al. (2011)
Mbalmayo Forest Reserve (high density cover)Organic AgroforestryMonocultureDichogaster 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 tantillus107/3 Norgrove et al. (2011)
China Hainan ProvinceNANA Pheretima montana ND0/1 Sun et al. (2012)
Colombia Quindío, Circasia, Barcelona (La Sofe farm)NAMonocultureAptodrilus fuhrmanni, Amynthas minimus, Glossodrilus chaguala, Glossodrilus panikita, Martiodrilus quimbayaensis54/1 Feijoo et al. (2018)
Quindío, Circasia, Barcelona (La Sofe farm)NAPolycultureAptodrilus fuhrmanni, Amynthas minimus, Glossodrilus chaguala, Glossodrilus panikita, Martiodrilus quimbayaensis54/1 Feijoo et al. (2018)
Quindío, Circasia, Barcelona (La Sofe farm)NANAAmynthas gracilis, Periscolex columbianus21/1 Feijoo et al. (2018)
Colombia Armenia, Niagara (La Catalina)NANAAmynthas gracilis, Glossodrilus griseus, Pontoscolex corethrurus31/2 Feijoo et al. (2018)
Quindio, Calarcá, Quebrada NegraNANA Glossodrilus griseus 11/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm)NAMonoculture Glossodrilus lacteus 11/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm)NAPolyculture Glossodrilus lacteus 11/0 Feijoo et al. (2018)
Quindío, Marmato (La Cristalina farm)NANA Dichogaster affinis 10/1 Feijoo et al. (2018)
Armenia, La Revancha (Villa Sofia farm)NANAAmynthas gracilis, Dichogaster affinis, Dichogaster bolaui, Glossodrilus griseus, Perionyx excavatus51/4 Feijoo et al. (2018)
Armenia, La Revancha (Bella Marina farm)NANADichogaster saliens, Periscolex columbianus21/1 Feijoo et al. (2018)
Quindío, Armenia, El RhinNANA Periscolex columbianus 11/0 Feijoo et al. (2018)
Quindío, Armenia, La India (La Ermita farm)NANA Periscolex coreguaje 11/0 Feijoo et al. (2018)
Circasia, Barcelona Baja rural (Buenos Aires farm)NANAAmynthas gracilis, Dichogaster saliens, Pontoscolex corethrurus30/3 Feijoo et al. (2018)
Quindío, Armenia, La India (La Miranda farm)NANA Dichogaster saliens 10/1 Feijoo et al. (2018)
Quindío, Armenia, La PatriaNANA Dichogaster saliens 10/1 Feijoo et al. (2018)
Costa Rica CahuitaNANA Pontoscolex corethrurus ND?/1 Lapied and Lavelle (2003)
Cuba BoyerosOrganicMonocultureDichogaster affinis, Dichogaster bolaui, Onychochaeta elegans, Polypheretima elongata, Protozapotecia angelesae52/3 Martínez-Leiva (2002)
Guadeloupe (France) Capesterre-Belle-EauNAMonoculture Pontoscolex corethrurus ND?/1 Lafont et al. (2007)
Capesterre-Belle-Eau (Gloria Bas)ConventionalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Capesterre-Belle-Eau (Source)ConventionalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Capesterre-Belle-Eau (Bergerie)AgroecologicalMonoculturePontoscolex corethrurus, unknown sp. 22? Burac et al. (2018)
Baillilf (Sextius)AgroecologicalMonoculturePontoscolex corethrurus, unknown sp.2? Burac et al. (2018)
Baillilf (Grand Canon)AgroecologicalMonoculturePontoscolex corethrurus, unknown sp. 32? Burac et al. (2018)
Saint-Claude (Saut d’Eau)AgroecologicalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
India Dakshina Kannada District (Belthangady)NANA Hoplochaetella kempi ND1/0 Siddaraju et al. (2013)
Dakshina Kannada District (Mangalore)NANA Konkadrilus bahli ND1/0 Siddaraju et al. (2013)
Dakshina Kannada District (Mangalore)NANA Dichogaster affinis ND0/1 Siddaraju et al. (2013)
India Dakshina Kannada District (Bantwal)NANA Octochaetona parva ND1/0 Siddaraju et al. (2010)
Dakshina Kannada District (sites not detailed)NANAAmynthas corticis, Hoplochaetella kempi, Hoplochaetella stuarti, Hoplochaetella suctoria, Megascolex konkanensis, Metaphire posthuma, Octochaetona paliensis, Octochaetona parvaND7/1Siddaraju et al. (2010, 2013)
Kerala (Vellayambalam)NANAPerionyx excavatus, Pontoscolex corethrurus20/2 Nair et al. (2007)
MizoramNAMonocultureDrawida nepalensis, Drawida rangamatiana, Drawida sp., Metaphire houlleti, Perionyx excavatus53/2 Lalthanzara (2007)
MizoramNAPolycultureDrawida nagana, Drawida sp., Metaphire houlleti, Perionyx excavatus42/2 Lalthanzara (2007)
RajapalayamNANALampito mauritii, Perionyx excavatus21/1 Mariappan et al. (2013)
Udupi District (Adve)NANA Megascolex konkanensis 11/0 Kumar et al. (2018)
Udupi District (Adve)NANA Metaphire houlleti 10/1 Kumar et al. (2018)
Udupi District (Bellibetu)NANAMetaphire houlleti, Pontoscolex corethrurus20/2 Kumar et al. (2018)
Udupi District (Mudarangadi)NANA Pontoscolex corethrurus 10/1 Kumar et al. (2018)
Udupi District (Nandikur)NANADrawida ampullacea, Drawida sulcata, Metaphire peguana33/0 Kumar et al. (2018)
Udupi District (Nandikur)NANA Drawida ampullacea 11/0 Kumar et al. (2018)
Udupi District (Padabettu)NANA Perionyx excavatus 10/1 Kumar et al. (2018)
Udupi District (Yellur)NANAMallehulla indica, Megascolex konkanensis22/0 Kumar et al. (2018)
West Tripura (Mohanpur, Maheshkhola, Rastermatha)OrganicMonocultureAmynthas alexandri, Drawida assamensis, Drawida papillifer, Eutyphoeus comillahnus, Lampito mauritii, Lennogaster sp., Metaphire houlleti, Metaphire posthuma, Octochaetona beatrix, Perionyx excavatus, Pontoscolex corethrurus3–74/7 Dhar and Chaudhuri (2018)
Indonesia Bangkalan (Kamal, Burneh, Socah, Bypass)NANAAmynthas robustus, Metaphire californica, Metaphire javanicaND1/2 Budijastuti (2019)
Bangkalan (Tanah Merah)NANA Metaphire posthuma 10/1 Budijastuti (2019)
Bangkalan (Labang)NANAAmynthas robustus, Metaphire javanica, Metaphire californica, Pheretima racemosa42/2 Budijastuti (2019)
Gresik (Driyorejo, Kedamean, Ngipik, SumengkoLegundi)NANAAmynthas robustus, Metaphire javanicaND1/1 Budijastuti (2019)
Gresik (Wringinanamon)NANAAmynthas robustus, Metaphire javanica, Metaphire posthuma31/2 Budijastuti (2019)
Sidoarjo (Waru, Taman, Sidoarjo, Tulangan, Tanggulangin, Candi)NANAAmynthas robustus, Metaphire javanica, Metaphire posthumaND1/2 Budijastuti (2019)
Surubaya (Pakal, Benowo, Tandes, Sukolilo, Gubeng, Gununganyar)NANAAmynthas robustus, Metaphire javanica, Metaphire posthumaND1/2 Budijastuti (2019)
Ivory Coast Lamto regionNANADichogaster wenkei, Reginaldia anomala, Stuhlmannia palustris, Stuhlmannia zielaeND4/0 Tondoh (1994)
Jamaica Clarendon, Crofts MountainNANADrawida barwelli, Polypheretima elongata20/2 Sims (1987)
Madagascar Ambatosoratra AmbatondrazakaNANAKynotus sihanakus, Kynotus sp.222/0Razafindrakoto et al. (2016), Csuzdi et al. (2017)
Malaysia Serdang, Sengalor (Universiti Putra Malaysia)NANA Pontoscolex corethrurus ND0/1Teng et al. (2006)
Martinique (France) Le Lorrain (Feugère)ConventionalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Le Lorrain (Limite)AgroecologicalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Le Lorrain (Bellevue)ConventionalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
L’Ajoupa-Bouillon (Allée Domergue 3)AgroecologicalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Basse-Pointe (Fromager Rivière)ConventionalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Basse-Pointe (Dantu Bas)AgroecologicalMonoculture Pontoscolex corethrurus 10/1 Burac et al. (2018)
Mexico TabascoNAMonocultureLavellodrilus bonampakensis, Pontoscolex corethrurus21/1 Huerta et al. (2005)
Tabasco, Teapa B1NAMonocultureBalanteodrilus pearsei, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus, Pontoscolex sp.51/4 Geissen et al. (2009)
Tabasco, Teapa B2NAMonocultureBalanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Periscolex brachycystis, Polypheretima elongata, Pontoscolex sp.62/4 Geissen et al. (2009)
Tabasco, Teapa AF1AgroforestryPolycultureBalanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus, Pontoscolex sp.62/4 Geissen et al. (2009)
Tabasco, Teapa AF2AgroforestryPolycultureBalanteodrilus pearsei, Dichogaster bolaui, Drawida barwelli, Polypheretima elongata, Pontoscolex corethrurus51/4 Geissen et al. (2009)
Tabasco, Teapa (site 1)ConventionalNADichogaster saliens, Diplotrema murchiei, Pontoscolex corethrurus3½ Huerta et al. (2013)
Tabasco, Teapa (site 2)ConventionalNADichogaster saliens, Pontoscolex corethrurus20/2 Huerta et al. (2013)
Tabasco, Teapa (site 3)ConventionalNADiplotrema murchiei, Polypheretima elongata, Pontoscolex corethrurus31/2 Huerta et al. (2013)
Tabasco, Teapa (site 4)ConventionalPolycultureAmynthas gracilis, Pontoscolex corethrurus20/2 Huerta et al. (2007)
Tabasco, Teapa (site 5)ConventionalPolycultureDichogaster saliens, Polypheretima elongata, Pontoscolex corethrurus30/3 Huerta et al. (2013)
Tabasco, Teapa (site 6)ConventionalNADichogaster saliens, Pontoscolex corethrurus20/2 Huerta et al. (2007)
Tabasco, Pablo L. SidarNAMonocultureLavellodrilus bonampakensis, Pontoscolex corethrurus21/1 Huerta et al. (2013)
Tamaulipas (Biosphere Reserve “El Cielo”)NANA Amynthas gracilis ND0/1 Barois (1992)
Actopan, Ejido BuenavistaNANA Balanteodrilus psammophilus ND1/0 Fragoso and Rojas (2007)
Nicaragua ManaguaNANADichogaster bolaui, Periscolex brachycystis21/1 Sherlock et al. (2011)
Peru Sarita ColoniaNAMonoculturePontoscolex corethrurus and two native spp.32/1 Pashanasi (2007)
Philippines Davao (Sumitomo Fruits Corporation, 15% site)ConventionalMonocultureMetaphire sp., Pithemera bicincta, Pontoscolex corethrurus31/2 Fusilero et al. (2013)
Davao (Sumitomo Fruits Corporation, 25% site)ConventionalMonocultureMetaphire cai, Metapheretima sp., Perionyx excavatus32/1 Fusilero et al. (2013)
Portugal Madeira Island (Ribeira Brava)NANAAporrectodea moebii, Eisenia eisensi, Metaphire californica30/3 Talavera (1996)
Madeira Island (Funchal)NANAAmynthas gracilis, Metaphire californica, Ocnerodrilus occidentalis30/3 Talavera (1996)
Portugal Madeira Island (Santa Cruz)NANA Amynthas gracilis 10/1 Talavera (1996)
Madeira Island (Terceira Lombada)NANAAporrectodea moebii, Eiseniella tetraedra20/2 Talavera (1996)
Madeira Island (Porto Moniz)NANAAmynthas gracilis, Aporrectodea rosea, Aporrectodea trapezoides, Dendrobaena pseudohortensis40/4 Talavera (2011)
Madeira Island (Terceira Lombada)NANAAporrectodea caliginosa, Aporrectodea rosea, Eiseniella tetraedra30/3 Talavera (2011)
Seychelles Cousine IslandNAMonoculture Pontoscolex corethrurus ND0/1 Plisko (2001)
South Africa KwaZulu-Natal (Fairfield Farm)NAMonoculture Pontoscolex corethrurus ND0/1 Plisko (2001)
KwaZulu-Natal (Benhurst Farm)NAMonoculture Pontoscolex corethrurus ND0/1 Plisko (2001)
KwaZulu-Natal (6 sites in Eshowe)NAMonocultureAmynthas corticis, Amynthas minimus, Amynthas rodericensis, Dichogaster bolaui, Pontoscolex corethrurus, and one other sp.ND0/5 Dlamini and Haynes (2004)
Spain Gomera Island (Agulo)NANAAmynthas rodericensis, Allolobophora chlorotica, Eiseniella tetraedra, Ocnerodrilus occidentalis40/4Talavera (1990a, 2007)
Gomera Island (Barranco de la Villa)NANABimastos rubidus, Ocnerodrilus occidentalis, Pithemera bicincta30/3 Talavera (2007)
Gomera Island (Barranco del Valle)NANAAllolobophora chlorotica, Metaphire californica20/2Talavera (1990b, 2007)
Gomera Island (Casas de Aluce)NANAAporrectodea rosea, Microscolex phosphoreus20/2 Talavera (2007)
Gomera Island (Cabo Verde)NANAAmynthas gracilis, Bimastos rubidus20/2Talavera (1990b, 2007)
Gomera Island (Costa Agulo)NANAAporrectodea trapezoides, Amynthas rodericensis, Bimastos rubidus, Ocnerodrilus occidentalis40/4 Talavera (2007)
Gomera Island (El Molinito)NANAAmynthas morrisi, Microscolex phosphoreus20/2 Talavera (2007)
Gomera Island (Hermigua)NANAAporrectodea rosea, Bimastos rubidus, Eisenia fetida, Ocnerodrilus occidentalis40/4Talavera (1990a, 2007)
Gomera Island (Laguna de Santiago)NANAAmynthas morrisi, Aporrectodea rosea, Aporrectodea trapezoides, Bimastos rubidus, Dendrobaena hortensis, Dichogaster affinis, Metaphire californica, Pithemera bicincta90/9 Talavera (2007)
Gomera Island (Playa de Santiago)NANA Ocnerodrilus occidentalis 10/1 Talavera (1990a)
Gomera Island (Seimal)NANAEiseniella tetraedra, Metaphire californica, Microscolex phosphoreus30/3 Talavera (2007)
Gomera Island (Taguluche)NANAAmynthas morrisi, Allolobophora chlorotica, Octalasion lacteum30/3 Talavera (2007)
Gomera Island (Valle Gran Rey)NANAAllolobophora chlorotica, Aporrectodea trapezoides, Dendrobaena hortensis, Eisenia fetida, Microscolex dubius, Pithemera bicincta50/5 Talavera (2007)
Gran Canaria (Lomo del Galeón)NANA Ocnerodrilus occidentalis 10/1 Talavera (1990a)
Gran Canaria (Los Llanos)NANAOcnerodrilus occidentalis, Pithemera bicincta20/2 Talavera (1990a)
Gran Canaria Island (Bañaderos)NANA Metaphire californica 10/1 Talavera (1990b)
Gran Canaria Island (Barranco Guiniguada)NANA Amynthas morrisi 10/1 Talavera (1990b)
Gran Canaria Island (Frontón)NANA Amynthas gracilis 10/1 Talavera (1990b)
Gran Canaria Island (Galdar)NANA Amynthas morrisi 10/1 Talavera (1990b)
Spain Gran Canaria Island (Hoya Mondondo)NANA Pithemera bicincta 10/1 Talavera (1990b)
Gran Canaria Island (La Aldea)NANA Dichogaster affinis 10/1 Talavera (1992b)
Gran Canaria Island (Pedrazo)NANA Pithemera bicincta 10/1 Talavera (1990b)
Gran Canaria Island (Tenoya)NANA Amynthas morrisi 10/1 Talavera (1990b)
Hierro Island (Los Mocanes)NANA Ocnerodrilus occidentalis 10/1 Talavera (1990a)
Hierra Island (NE tip)NANA Microscolex phosphoreus ND0/1 Talavera and Pérez (2009)
La Palma Island (Barranco de las Angustias)NANA Amynthas gracilis 10/1 Talavera (1990b)
La Palma Island (Barranco Nogales)NANA Amynthas gracilis 10/1 Talavera (1990b)
La Palma Island (El Socorro)NANA Pithemera bicincta 10/1 Talavera (1990b)
La Palma Island (La Caldereta)NANAAmynthas morrisi, Metaphire californica20/2 Talavera (1990b)
La Palma Island (Los Cancajos)NANA Amynthas morrisi 10/1 Talavera (1990b)
La Palma Island (Los Llanos de Aridane)NANAAmynthas morrisi, Metaphire californica20/2 Talavera (1990b)
La Palma Island (Tazacorte)NANAAmynthas gracilis, Amynthas morrisi, Metaphire californica30/3 Talavera (1990b)
Tenerife Island (Abama)NAMonocultureAporrectodea rosea, Dendrobaena hortensis, Eisenia andrei, Microscolex dubius40/4 Talavera (1992a)
Tenerife Island (Adeje)NANA Ocnerodrilus occidentalis 10/1 Talavera (1990a)
Tenerife Island (Bajamar)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Microscolex phosphoreus, Ocnerodrilus occidentalis60/6Talavera (1990a, 1992a, 1992b)
Tenerife Island (Barranco de Santos)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Bimastos rubidus, Eisenia andrei, Microscolex dubius, Pithemera bicincta60/6Talavera (1990b, 1992a)
Tenerife Island (Barranco del Inglés)NAMonocultureAporrectodea rosea, Aporrectodea trapezoides, Eisenia andrei, Microscolex dubius40/4 Talavera (1992a)
Tenerife Island (Barranco la Atalaya)NAMonocultureAporrectodea rosea, Pithemera bicincta20/2 Talavera (1992a)
Tenerife Island (Barranco las Galletas)NAMonocultureAporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis30/3 Talavera (1992a)
Tenerife Island (Barranco San Felipe)NAMonocultureAmynthas gracilis, Eisenia andrei, Pithemera bicincta30/3Talavera (1992a, 1990b)
Tenerife Island (Buenavista del Norte)NANA Ocnerodrilus occidentalis 10/1 Talavera (1990a)
Tenerife Island (Casablanca)NAMonocultureAmynthas corticis, Aporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis40/4 Talavera (1992a)
Tenerife Island (Costa Valle Guerra)NAMonoculture Amynthas gracilis 10/1 Talavera (1992a)
Tenerife Island (El Puente)NAMonocultureAmynthas gracilis, Aporrectodea rosea, Eisenia andrei, Microscolex phosphoreus, Ocnerodrilus occidentalis50/5 Talavera (1992a)
Tenerife Island (El Rincón)NAMonocultureAmynthas gracilis, Bimastos rubidus, Dendrobaena cognetti, Microscolex dubius, Microscolex phosphoreus, Octodrilus complanatus60/6 Talavera (1992a)
Spain Tenerife Island (El Socorro)NANA Pithemera bicincta 10/1 Talavera (1990b)
Tenerife Island (Fañabé)NAMonocultureAmynthas corticis, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Ocnerodrilus occidentalis50/5Talavera (1990a, 1992a, 1992b)
Tenerife Island (Güimar)NANADichogaster affinis, Ocnerodrilus occidentalis20/2Talavera (1990a, 1992b)
Tenerife Island (Iboybo)NAMonocultureAporrectodea rosea, Eisenia andrei, Ocnerodrilus occidentalis30/3 Talavera (1992a)
Tenerife Island (Icod de Los Vinos)NAMonocultureDendrobaena cognetti, Bimastos rubidus, Octodrilus complanatus, Ocnerodrilus occidentalis40/4 Talavera (1992a)
Tenerife Island (Igueste)NAMonocultureAllolobophora chlorotica, Aporrectodea rosea, Aporrectodea trapezoides, Pontoscolex corethrurus, Ocnerodrilus occidentalis50/5 Talavera (1992a)
Tenerife Island (La Hondura)NAMonoculture Amynthas morrisi 10/1 Talavera (1992a)
Tenerife Island (La Longuera)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Eisenia fetida, Microscolex dubius, Octodrilus complanatus50/5 Talavera (1992a)
Tenerife Island (La Matanza)NAMonocultureBimastos rubidus, Eisenia andrei, Microscolex phosphoreus30/3 Talavera (1992a)
Tenerife Island (La Montañeta)NANA Pithemera bicincta 10/1 Talavera (1990b)
Tenerife Island (La Vera)NAMonocultureBimastos rubidus, Eisenia andrei, Microscolex phosphoreus30/3 Talavera (1992a)
Tenerife Island (Las Arenas)NANA Amynthas morrisi 10/1 Talavera (1990b)
Tenerife Island (Las Galletas)NAMonocultureEisenia andrei, Bimastos eiseni, Ocnerodrilus occidentalis30/3Talavera (1990a, 1992a)
Tenerife Island (Las Madrigueras)NANA Amynthas morrisi 10/1 Talavera (1990b)
Tenerife Island (Los Quintos)NAMonocultureDendrobaena cognetti, Bimastos rubidus, Microscolex phosphoreus, Pithemera bicincta, Ocnerodrilus occidentalis50/5 Talavera (1992a)
Tenerife Island (Los Realejos)NANA Pithemera bicincta 10/1 Talavera (1990b)
Tenerife Island (Los Rechazos)NAMonocultureAporrectodea trapezoides, Bimastos rubidus, Eisenia fetida, Octodrilus complanatus, Pithemera bicincta50/5 Talavera (1992a)
Tenerife Island (Los Silos)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Dichogaster affinis, Eisenia andrei, Ocnerodrilus occidentalis50/5Talavera (1992a1992b)
Tenerife Island (Loss Llanos)NAMonocultureAmynthas morrisi, Bimastos rubidus, Eisenia andrei, Pithemera bicincta40/4 Talavera (1992a)
Tenerife Island (Playa de las Aguas)NAMonocultureAmynthas morrisi, Eisenia andrei, Pithemera bicincta30/3 Talavera (1992a)
Tenerife Island (Playa de San Juan)NAMonocultureAporrectodea rosea, Dendrobaena hortensis, Bimastos rubidus, Eisenia andrei40/4 Talavera (1992a)
Tenerife Island (Playa San Marcos)NAMonoculturePithemera bicincta, Bimastos rubidus, Microscolex phosphoreus30/3 Talavera (1992a)
Tenerife Island (Puertito de Gilimar)NAMonocultureMicroscolex phosphoreus, Pithemera bicincta, Ocnerodrilus occidentalis30/3 Talavera (1992a)
Tenerife Island (Puerto de Santiago)NAMonoculture Amynthas morrisi 10/1Talavera (1990b, 1992a)
Tenerife Island (Punta del Hidalgo)NAMonocultureAmynthas gracilis, Ocnerodrilus occidentalis20/2 Talavera (1992a)
Tenerife Island (San Andrés)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Microscolex phosphoreus, Ocnerodrilus occidentalis40/4 Talavera (1992a)
Tenerife Island (San Bernardo)NAMonocultureAmynthas corticis, Amynthas morrisi, Aporrectodea rosea, Eisenia andrei40/4 Talavera (1992a)
Spain Tenerife Island (San Juan de la Rambla)NAMonocultureAmynthas gracilis, Bimastos rubidus, Dendrobaena hortensis, Eisenia fetida, Pithemera bicincta50/5Talavera (1990b, 1992a)
Tenerife Island (San Pedro de Daute)NAMonocultureAmynthas morrisi, Aporrectodea rosea, Ocnerodrilus occidentalis30/3 Talavera (1992a)
Tenerife Island (Santo Domingo)NAMonocultureDendrobaena cognetti, Microscolex dubius, Microscolex phosphoreus30/3 Talavera (1992a)
Tenerife Island (Taganana)NAMonoculture Amynthas morrisi 10/1 Talavera (1992a)
Tenerife Island (Tejina)NAMonocultureAmynthas corticis, Pithemera bicincta20/2 Talavera (1992a)
Taiwan Central regionNANA Pontoscolex corethrurus ND0/1 Tsai et al. (2000)
Uganda Kabanyolo University FarmNANADichogaster sp. 1, Dichogaster sp. 2, Gordiodrilus sp., Pygmaeodrilus sp., Polytoreutus sp. 155/0 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.
CountryNo. sites: Quant./Qual.1Total No. speciesNativeExoticFamilies
Asia 6/≥47 35 22 13 5
Bangladesh0/13122
China0/11011
India4/≥20272075
Indonesia0/235141
Malaysia0/11011
Philippines2/26332
Taiwan0/11011
Africa 33/97 50 20 30 7
Cameroon10/212933
Canary Islands (Spain)2
Gomera 0/13180184
Gran Canaria 0/106063
Hierro 0/22022
La Palma 0/73031
Tenerife 0/45190195
Ivory Coast1/14403
Madagascar0/12201
Madeira (Portugal)20/6100103
Seychelles0/11011
South Africa6/85053
Uganda6/15503
North America 12/16 14 7 7 4
Bermuda0/22021
Mexico12/1412574
Central America/Caribbean 53/≥17 10 4 6 4
Costa Rica≥5/11011
Cuba1/15233
Dominica1/021?12
Guadeloupe (France)40/74??≥1≥1
Martinique (France)6/61011
Jamaica0/12022
Nicaragua0/12112
South America 49/33 20 10 10 6
Brazil16/167075
Colombia32/1515874
Peru1/1321≥1
Total 153/210 1046143 10
1Quant.=quantitative samples, taken using various sampling methods (mostly hand sorting of soil monoliths); Qual.=qualitative samples, usually performed for biodiversity studies (species presence) and normally without specifying volume of soil sampled; 2Although politically these islands belong to Europe, biogeographically they belong to Africa.

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.

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https://www.researchpad.co/tools/openurl?pubtype=article&doi=10.3897/zookeys.1033.54331&title=Earthworm species in <i/> spp. plantations in Brazil and worldwide&author=&keyword= Annelida ,banana,biodiversity, Oligochaeta ,plantain,Pontoscolex corethrurus,&subject=Research Article,Animalia,Annelida,Clitellata,Haplotaxida,Invertebrata,Agriculture and Forestry,Ecology &amp; Environmental sciences,Habitats,ecosystems &amp; natural spaces,Soils and Soil Ecology,Cenozoic,Brazil,World,