Pontoscolex corethrurus: A homeless invasive tropical earthworm?

Authors: Angel I. Ortíz-Ceballos aff001;  Diana Ortiz-Gamino aff001;  Antonio Andrade-Torres aff001;  Paulino Pérez-Rodríguez aff002;  Maurilio López-Ortega aff001
Authors place of work: Instituto de Biotecnología y Ecología Aplicada (INBIOTECA), Universidad Veracruzana, Col. Emiliano Zapata, Xalapa, Veracruz, México aff001;  Programa de Estadística, Campus Montecillo, Colegio de Postgraduados, Montecillo, Estado de México, México aff002
Published in the journal: PLoS ONE 14(9)
Category: Research Article
doi: 10.1371/journal.pone.0222337


The presence of earthworm species in crop fields is as old as agriculture itself. The earthworms Pontoscolex corethrurus (invasive) and Balanteodrilus pearsei (native) are associated with the emergence of agriculture and sedentism in the region Amazon and Maya, respectively. Both species have shifted their preference from their natural habitat to the cropland niche. They contrast in terms of intensification of agricultural land use (anthropic impact to the symbiotic soil microbiome). P. corethrurus inhabits conventional agroecosystems, while B. pearsei thrives in traditional agroecosystems, i.e., P. corethrurus has not yet been recorded in soils where B. pearsei dwells. The demographic behavior of these two earthworm species was assessed in the laboratory over 100 days, according to their origin (OE; P. corethrurus and B. pearsei) food quality (FQ; soil only, maize stubble, Mucuna pruriens), and soil moisture (SM; 25, 33, 42%). The results showed that OE, FQ, SM, and the OE x FQ interaction were highly significant for the survival, growth, and reproduction of earthworms. P. corethrurus showed a lower survival rate (> mortality). P. corethrurus survivors fed a diet of low-to-intermediate nutritional quality (soil and stubble maize, respectively) showed a greater capacity to grow and reproduce; however, it was surpassed by the native earthworm when fed a high-quality diet (M. pruriens). Besides, P. corethrurus displayed a low cocoon hatching (emergence of juveniles). These results suggest that the presence of the invasive species was associated with a negative interaction with the soil microbiota where the native species dwells, and with the absence of natural mutualistic bacteria (gut, nephridia, and cocoons). These results are consistent with the absence of P. corethrurus in milpa and pasture-type agricultural niches managed by peasants (agroecologists) to grow food regularly through biological soil management. Results reported here suggest that P. corethrurus is an invasive species that is neither wild nor domesticated, that is, its eco-evolutionary phylogeny needs to be derived based on its symbionts.


Biology and life sciences – Organisms – Eukaryota – Animals – Invertebrates – Annelids – Earthworms – Plants – Grasses – Maize – Agriculture – Agricultural soil science – Nutrition – Diet – Microbiology – Medical microbiology – Microbiome – Microbial genomics – Genetics – Genomics – Population biology – Population metrics – Death rates – Ecology and environmental sciences – Species colonization – Invasive species – Soil science – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Plant and algal models – Medicine and health sciences


Although humans have produced novel niches prior to the advent of agriculture, the innovation of domestication led to changes in the life cycle of one or a few species, and the local microenvironments were manipulated, especially soil biota [14]. The artificial landscapes that resulted from these practices (anthropocentric ecology) were exported as agricultural packages from the centers of origin [1, 2, 4]. Thus, over a relatively short period in the history of mankind, the expansion of agriculture has brought about the remodeling of biodiversity as one of the most significant anthropogenic impacts on terrestrial ecosystems [1, 2, 5].

Agriculture has given rise to uniform and predictable disturbed ecological niches (invasible habitats), which have proven highly beneficial for non-domesticated species or weeds [1, 2, 6], and some earthworm species. Blakemore [7] has suggested that the origins of cosmopolitan (invasive) earthworms at family level are associated with domestication centers of plants and animals; that is, the presence of earthworms in crop fields is as old as agriculture itself [79]. The terms of the Millennium Ecosystem Assessment highlight the catalytic role of earthworms regarding two environmental services [10], namely the formation of soil and biogeochemical cycles, both of which are prerequisites for other environmental services [1011].

Most of the studies focused on earthworms have used species adapted to crops, and most of them are currently considered as invasive [11]. It has been documented that 3% of the diversity of earthworms are invasive species [12]. As an example, European earthworms are frequently mentioned as the main cause of an irreversible change in the diversity and functioning of ecosystems in North America (Wisconsin glaciation areas) that were previously free from earthworms 12 thousand years ago [1315]. However, there is a deeply rooted positive attitude toward earthworms in human populations in North America, acknowledging their beneficial effects on agricultural soils and urban gardens [10, 16].

Among the invasive tropical earthworms, the endogeic species Pontoscolex corethrurus was collected and described in crop fields in Blumenau, Brazil 160 years ago [1718]; it has a broad distribution range and is the most studied tropical species [1920]. Native species also move across a region in a similar way to invasive species, in addition to natural displacements [5, 7, 21]. The native endogeic earthworm Balanteodrilus pearsei was first collected and described from Gongora cave in Okcutzcab, Yucatan 81 years ago [22]; it is distributed in the east and southeast of Mexico and Belize [19]; it dwells in natural and agricultural environments and is the most studied species native to Mexico. Most studies conducted with both species point to a positive influence of their biological activity on soil [20, 23], i.e., they do not meet the definition of pest [24]. For this reason, we use the term invasive with reference to the biogeographical status of the species, regardless of its impact on soil [2425].

Similar to weeds [6, 8, 9, 26], it can be suggested that P. corethrurus and B. pearsei have shifted their preference from their natural habitat to agricultural environments, spreading geographically beyond their place of origin, and are currently key elements of agricultural environments. The presence of P. corethrurus and B. pearsei is associated with the development of pre-Columbian cultivation techniques in the Amazon [2, 27, 28, 29] and Maya [2, 30, 31] regions, respectively. For example, it is believed that P. corethrurus facilitated the formation of fertile soils in the Amazon area named "Terra Preta do Indo" [32, 33, 34, 35, 36, 37]. Both species have adapted to niches that emerged from agriculture [38], but contrast regarding the intensification of agricultural land use and/or the diversion of each from natural habitats (anthropic manipulation of soil). P. corethrurus is commonly found in conventional agrecosystems (use of fertilizers, herbicides, pesticides, and tillage), as well as in industrial (polluted with heavy metals, petroleum hydrocarbons, and others) and urban areas [20, 39, 40, 41]. B. pearsei inhabits soils managed under an agroecological approach (little human impact of the soil microbiome), such as traditional agroecosystems (no use of industrial inputs) and in natural ecosystems [40, 42, 43]. P. corethrurus has been found coexisting with native species in some agroecosystems [41, 44, 45], but there are no records of its coexistence with B. pearsei so far [40, 42, 43].

A previous study of coexistence under controlled conditions showed no competitive interaction between P. corethrurus and B. pearsei, i.e., both can coexist [23]. However, the question to address is, why P. corethrurus has not invaded the agroecological niche of B. pearsei? Therefore, this work compared the demographic behavior of P. corethrurus vs. B. pearsei assuming that the survival rate of the invasive species decreases in soil populated by the native species.

Materials and methods

Ethics statement

No permits were required for the collection and laboratory trials. Soil and earthworms were provided by farmers with free of charge. The experimental procedure used in this study is detailed elsewhere [23].


Soil was collected from a maize field (MM) rotated with the tropical legume velvet bean (Mucuna prurien var. utilis) located near the village Tamulté de las Sabanas (18°08´N, 92°47´W), 30 km east of Villahermosa, Tabasco, Mexico. The silty clay loam soil (41.5% sand; 26.8% clay; 31.6% silt) was air-dried in the shade at room temperature and sieved through a 2 mm mesh. The main chemical characteristics of this soil were: 2.7% organic matter; 0.14% total N; 11.4 C/N; pH (H2O) of 6.3.


Two tropical endogeic earthworm species were used in this study: B. pearsei (native) and P. corethrurus (invasive). B. pearsei was collected from the MM field, whereas P. corethrurus was collected from pastures at Huimanguillo (79 km southwest Villahermosa, 17°48´N, 93°28´W), given its absence in the former site. All earthworms (120 for each species) were collected two weeks prior to the beginning of the experiment.

Food quality

The effects of foof quality were assessed by using two different types of plant litter of contrasting nutritional quality: M. pruriens (52.4% C, 2.25% N, 23.3 C/N, and 9.67% ash) and maize stubble (52% C, 0.84% N, 61.9% C/N, and 10.3% ash). Both materials were obtained from the MM field, oven-dried at 60°C for 48 h, and sieved (1 mm).


Growth, sexual maturity, reproduction (cocoons and juveniles), and mortality of B. pearsei and P. corethrurus were investigated during 100 days using a factorial design with three factors: origin of earthworms (OE), soil moisture (SM), and food quality (FQ). SM involved 3 levels, corresponding to the permanent wilt point (25%), field capacity (42%), and an intermediate level (33%). FQ included three levels: 300 g soil only (S), 294 g soil + 6 g maize stubble (MS), and 294 g soil + 6g M. pruriens (MP); the amounts added correspond to those commonly found in both maize monocultures and cultures rotating maize and M. pruriens. The earthworm species used belong to two different classes based on origin: Native (B. pearsei) and Invasive (P. corethrurus).

The combination of the three factors and three levels produced nine treatments with five replicates per treatment. Each replicate consisted of a plastic container (12×12×8 cm) containing 300 g dried soil of the corresponding food-soil mixture and soil moisture; two individuals of B. pearsei and two of P. corethrurus were transferred to each container (Table 1).

Tab. 1.

F-values and significance levels (ANOVA) of the interaction of three factors on growth and reproduction of the tropical endogeic earthworm Pontoscolex corethrurus and Balanteodrilus pearsei at 100 days of culture in soil with low anthropic impact.

<h2><i>F</i>-values and significance levels (ANOVA) of the interaction of three factors on growth and reproduction of the tropical endogeic earthworm <i>Pontoscolex corethrurus</i> and <i>Balanteodrilus pearsei</i> at 100 days of culture in soil with low anthropic impact.</h2>

Earthworms were washed, dried on paper towels, weighed, and assigned randomly to each treatment. The baseline weight of the 45 replicates from the nine treatments was statistically similar in B. pearsei and P. corethrurus (76.06 ± 26.1 mg, n = 90 and 66.04 ± 31.1 mg, n = 90, respectively). Containers were incubated at 26 ± 1 ºC. Body weight, mortality, clitellum appearance (sexual maturity), and number and biomass of cocoons and juveniles of B. pearsei and P. corethrurus were recorded at 10-day intervals, and soil was replaced. Before use, fresh soil (including the corresponding food-soil mixture and moisture) was preincubated for 8 days at 26°C in order to trigger litter substrate decomposition. Each cocoon produced was incubated in a petri dish at 26°C; incubation time as well as number and weight of all juveniles hatched were recorded.

Statistical analysis

Cocoon and juvenile weight, and growth were evaluated through Analysis of Varienace (ANOVA). Mortality, sexual maturity, number of cocoons, and number of juveniles were analyzed using generalized linear models, specifically the Poisson distribution wich is widely used for modelling count data. Differences between means were evaluated with Tukey's HSD. All statistical analyses were perfomed using the Statistica software.


At 100 days of culture, significant effects were observed between the origin of earthworms (OE), food quality (FQ) and soil moisture (SM), and the interaction between these three factors on sexual maturity, number of cocoons, and number and biomass of juveniles (Table 1).


At the end of the culture, the invasive earthworm (P. corethrurus) had a 21.1% mortality rate in the soil treatment (33% and 25% SM), while that of the native earthworm (B. pearsei) had only a 1.1% mortality rate in the soil treatment (only 42% SM). In the M. pruriens and maize stubble treatments (25%, 33% and 42% SM) no mortality was observed in both earthworm species.


Growth of the endogeic earthworms clearly varied in response to EO, FQ, SM, and the EO⊆CF and SM⊆CF interactions (Table 1). At 100 days of culture, the growth of the invasive and native species (P. corethrurus and B. pearsei, respectively) was higher when food quality increased (Fig 1). In the three FQ levels (soil, maize stubble, and M. pruriens) the exotic species showed a faster growth (1.6, 9.4, and 12.3 mg/day, respectively) relative to the native species (0.34, 4.8, and 10.4 mg/day).

<h2>Biomass of the tropical endogeic earthworms <i>Pontoscolex corethrurus</i> (invasive) and <i>Balanteodrilus pearsei</i> (native) at 100 days of culture using three diets of different nutritional quality in soil with low anthropic impact.</h2>
Fig. 1.

Biomass of the tropical endogeic earthworms Pontoscolex corethrurus (invasive) and Balanteodrilus pearsei (native) at 100 days of culture using three diets of different nutritional quality in soil with low anthropic impact.

Vertical lines represent standard error.


Sexual maturity (clitellum)

When fed M. pruriens, the onset of sexual maturity in P. corethrurus and B. pearsei occurred at 30 days; when fed maize stubble, sexual maturity was obseved at 30 and 70 days in P. corethrurus and B. pearsei, respectively.

At 100 days of culture, OE, FQ, SM, and the OE ⊆ CF ⊆ SM interaction significantly affected clitellum development (Table 1). The invasive and native earthworms reached sexual maturity in the treatments with M. pruriens (100% and 86.6%) and maize stubble (96.7% and 70.0%), respectively (Fig 2). No individuals reached sexual maturity after 100 days in the soil treatments; however, in the soil treatment with 33% SM, one earthworm of P. corethrurus (6.7%) reached sexual maturity at 80 days.

<h2>Sexual maturity (formation of the clitellum) in the tropical endogeic earthworms <i>Pontoscolex corethrurus</i> (invasive) and <i>Balanteodrilus pearsei</i> (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.</h2>
Fig. 2.

Sexual maturity (formation of the clitellum) in the tropical endogeic earthworms Pontoscolex corethrurus (invasive) and Balanteodrilus pearsei (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.

Vertical lines represent standard error.

Cocoon production

B. pearsei and P. corethrurus displayed biparental and uniparental sexual reproduction, respectively. On M. pruriens treatments (25%, 33% and 42% SM), cocoon production started when B. pearsei and P. corethrurus reached a mean biomass of 773.5 ± 146.8 mg and 644.7 ± 71.1 mg (average of 25%, 33% and 42% SM), respectively. On maize stubble treatments, it started when B. pearsei and P. corethrurus reached a mean body weight of 593.0 ± 80.9 mg and 598.5 ± 95.2 mg (average of 25%, 33% and 42% SM), respectively. Cocoon production in P. corethrurus was observed in soil (6.7%), maize stubble (53.3%), and M. pruriens (86.7%) treatments, but in B. pearsei it was observed only in maize stubble (33.3%) and M. pruriens (86.7%) treatments.

Mean cocoon production was significantly influenced by EO, CF, SM, and the interaction between these three factors (Table 1). After 100 days of culture, peak mean cocoon production in B. pearsei and P. corethrurus was observed in M. pruriens treatments, with 59.7 ± 40.8 and 35.5 ± 21.5 cocoons (average of 25%, 33% and 42% SM treatments), respectively (Fig 3). When fed maize stubble, B. pearsei and P. corethrhrus produced 7.9 ± 3.2 and 14.4 ± 9.2 cocoons (average of 25%, 33% and 42% SM treatments), respectivelly. Finally, when fed soil only (33% SM), P. corethrurus (448 mg body weight) produced only two cocoons.

<h2>Number of cocoons produced by the tropical endogeic earthworms <i>Pontoscolex corethrurus</i> (invasive) and <i>Balanteodrilus pearsei</i> (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.</h2>
Fig. 3.

Number of cocoons produced by the tropical endogeic earthworms Pontoscolex corethrurus (invasive) and Balanteodrilus pearsei (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.

Vertical lines represent standard error.

Cocoon biomass varied significantly in response to EO, FQ, SM and the OE x SM and FQ x SM interactions (Table 1). Average cocoon biomass produced by B. pearsei and P. corethrurus with SM treatments (25%, 33% and 42%) was 10.2 ± 1.4 mg and 27.7 ± 3.7 mg, respectively.

Juvenile production

The mean cocoon incubation time was similar among treatments (P > 0.05). In general, mean cocoon incubation time was 20.4 ± 5.2 days (B. perasei) and 30.3 ± 2.2 days (P. corethrhrus), with one individual hatching per cocoon in all cases. Of the total number of cocoons produced by B. pearsei and P. corethrurus in M. pruriens and corn stubble treatments, the average number of hatched juveniles was 64.7 ± 16.6% and 29.5 ± 7.0% (average of 25%, 33% and 42% SM treatments) and 59.5 ± 24.7 and 24.0 ± 10.6 (average of 25%, 33% and 42% SM treatments), respectively.

The number of hatched juveniles of B. pearsei and P. corethrurus varied significantly with OE, CF, SM, and the interaction between these three factors (Table 1; Fig 4). The mean number of hatched juveniles of B. pearsei and P. corethrurus increased in adults fed M. pruriens, as well as with increasing soil moisture (mean 59.7±40.8 and 35.5±21.5 individuals, respectively), and corn stubble (mean 7.9 ± 3.3 and 14.6 ± 9.2 individuals).

<h2>Number of juveniles hatched from cocoons produced by the tropical endogeic earthworms <i>Pontoscolex corethrurus</i> (invasive) and <i>Balanteodrilus pearsei</i> (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.</h2>
Fig. 4.

Number of juveniles hatched from cocoons produced by the tropical endogeic earthworms Pontoscolex corethrurus (invasive) and Balanteodrilus pearsei (native) at 100 days of culture under the interaction of three diets of different nutritional quality and three moisture content levels in soil with low anthropic impact.

Vertical lines represent standard error.

At hatching, in the M. pruriens and corn stubble treatments, mean biomass of P. corethrurus juveniles (21.2 ± 1.0 and 18.6 ± 7.4 mg, respectively) was higher vs. B. pearsei juveniles (8.5 ± 0.7 and 8.5 ± 1.3 mg, respectively).


Domesticated, wild populations respond to changing selective pressures, which are reflected in their adaptation to agricultural niches [2, 46]. From an ecological perspective, the endogeic earthworm P. corethrurus resembles non-domesticated species or weeds given its strong profile (invading species) regarding growth rate, fertility, plasticity, interspecific competition, and environmental tolerance [7, 8, 9, 26, ]. This suggests that the four P. corethrurus ecotypes described by Taheri et al. [47] are likely the result of the selective forces imposed by cultivation, agricultural practices, and industrial and urban activities [20]. In the present study, soil in the habitat for B. pearsei was observed to restrain the presence of P. corethrurus.

The conversion of the Amazon forest to pastures led to the homogenization of soil biota [3, 48]. The potential resistance of soil (i.e., predators, low species richness, etc.) to earthworms has been documented [15, 49, 50]. For instance, the endogeic tropical earthworm Millsonia anomala from the savannah was unable to prosper in forest soil [49], similar findings have been reported with P. corethrurus from fallow (slash-and-burn) to mature forest [35]. Also, the shift in vegetation from grass to woody plants decreaced in the density and biomass of P. corethrurus [51]. Our results showed that the survival of P. corethrurus was lower in the environment where B. pearsei thrives, maybe due to a negative interaction with a more diverse edaphic microbiome [49, 50, 52], because it has been suggested that P. corethrhrus has a high ability to utilize soil organic resources as an energy source [39].

Earthworms harbor symbiotic microbiomes that are essential for their life history in the nephridia (excretory organs), and cocoons in tropical species such as P. corethrurus is poorly studied [5358]. The microbiome is known to improve the nutritional status of low-quality diets [5758]. For example, Topoliantz and Ponge [35] observed that the behaviour of two populations of P. corethrurus separated along the Maroni river (French Guiana, South America) differed significantly: fallow populations produced more cast on charcoal in the presence of forest soil, while the casting activity of the forest population was higher on soil regardless of the soil origin. Our findings show that P. corethrurus and B. pearsei differ in their diet preference (M. pruriens, corn stubble, and control), i.e., the invasive species displayed faster growth than the native species when nutritional quality improved. This suggests that P. corethrurus consumes and degrades a greater variety of organic materials given its greater ability (efficiency), evidenced by: a) producing endogenous cellulases [5962]; b) its association with the gut microbiota [6366]; c) gene expression (transcriptome) that contribute to the adaptation of its digestive system [65]; d) improving its digestion efficiency according to the type of cecum [59, 67]; and e) its association with nephridial bacteria [50, 68, 69].

It is known that in diets of low nutritional quality, mutualistic bacteria residing in earthworm nephridia (in 19 of 23 species studied) provide vitamins to its host, stimulate earlier sexual maturity, and contribute to pesticide detoxification [56, 57, 58, 60, 70, 71]. The results reported here showed that the invasive species of smaller size (biomass) fed on a lower nutritional diet (M. pruriens > corn stubble > soil) reached sexual maturity earlier than the native earthworm. This suggests that the nephridial symbionts of P. corethrurus are generalists, while those of B. pearsei are specialists.

Earthworms produce external cocoons that are colonized by bacteria from parents and soil [vertical and horizontal transmission, respectively 53, 58] and coul be used as biovectors for the introduction of benefical bateria [55]. In a new habitat, cocoons of invasive earthworms may be affected by the native microbiota, but they can survive if they carry a parental microbial inoculum. Our results show that P. corethrurus produced cocoons when fed either of the three diets, while B. pearsei fed the control diet (only soil) failed to produce cocoons. In contrast, cocoons of P. corethrurus had a low hatching rate (births), which was lower (diet with M. pruriens) compared to B. pearsei. These results suggest the absence and/or loss of parental symbionts bacteria, i.e., the loss of a parental care strategy to control predators, detoxify nitrogenous wastes, conserve nitrogen, and supply vitamins and essential cofactors to the offspring [55, 56, 57, 68, 69, 70, 72]. Thus, the likely symbiotic evolution of P. corethrurus with the microbiome (gut, nephridia and cocoons) should be explored as a source of biogeography and phylogenetic information [11, 57, 68, 70, 71, 73, 74]. That is, we could “…explain why P. corethrurus is rare or absent in undisturbed lands” [39].

The human-mediated translocation of species dates back to the Late Pleistocene [2, 5, 75]. Invasive plant species are usually divided in two groups according their residence time: archaeophytes were found from 1500 AD, and neophytes are found after this date [76]. This approach can contribute to elucidate the history of the invasion of P. corethrurus in Mexico. Until now, only two ecotypes have been recorded [47] and the criptic linage used in this study corresponds to L1 (the most widespread). The origin of P. corethrurus may be related to anthropogenic soil formation (“terras mulatas” and “terras pretas”). The domestication of manioc (bitter and sweet) and peach palm staple food that facilitated sedentary lifestyles in the Amazon region [5, 27, 28, 29, 32] has evolved to the point that we cannot recognize the predecessors of P. corethrurus, as evidenced by the recent designation of the P. corethrurus neotype from an anthropogenic environment [18] and temperate climate [77], and by the ambiguity used for assigning its place of origin [12, 78].

Based on the results reported here, we conclude that the invasive tropical earthworm P. corethrurus had lower survival and cocoons hatching rates (offspring) in the agro-ecological niche of the native endogeic earthworm, i.e., a finding consistent with the absence of P. corethrurus in parcels where maize- and M. pruriens crop rotation is practiced, as well as in pastures and other traditional tropical agroecosystems [40, 41, 42, 43, 44, 45]. This suggests that P. corethrurus is an invasive species that thrives far from its natural status, i.e., has no wild ancestry in the study area. Therefore, it is important to determine the preference of the four P. corethrurus ecotypes [47] in terms of soil type, cultivation, response to stressors and climate change.

Supporting information

S1 Table [pdf]
Results fitting linear model of the earthworm biomass.

S2 Table [pdf]
Results fitting logistic model of sexual maturity of the earthworms.

S3 Table [pdf]
Results fitting zero inflated poisson of the earthworms cocoons.


1. Bender SF, Wagg C, van der Heijden MGA. An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability. Trends in Ecology and Evolution 2016;31(6):440–452. doi: 10.1016/j.tree.2016.02.016 26993667

2. Boivin NL, Zeder MA, Fuller DQ, Crowther A, Larson G, Erlandson JM, et al. Ecological consequences of human niche construction: Examining long-term anthropogenic shaping of global species distributions. Proceedings of the National Academy of Sciences. 2016;113(23):6388–6396. doi: 10.1073/pnas.1525200113 27274046

3. Pérez-Jaramillo JE, Mendes R, Raaijmakers JM. Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Molecular Biology. 2016; 90(6):635–644. doi: 10.1007/s11103-015-0337-7 26085172

4. Fuller DQ, Lucas L. Adapting crops, landscapes, and food choices: Patterns in the dispersal of domesticated plants across Eurasia. In: Boivin N, Crassard R, Petraglia M, editors. Human Dispersal and Species Movement: From Prehistory to the Present. Cambridge: Cambridge University Press; 2017. pp. 304–331.

5. Lodge DM. Biological invasions: lessons for ecology. Trends in Ecology & Evolution. 1993;8(4):133–137

6. Fuller DQ, Stevens CJ. Open for Competition: Domesticates, Parasitic Domesticoids and the Agricultural Niche. Archaeology International. 2017;20:110–121. doi: 10.5334/ai.359

7. Blakemore RJ. Cosmopolitan Earthworms—A Global and Historical Perspective. In Shain DH, editor. Annelids in Modern Biology. New York: John Wiley & Sons, Inc.; 2009. pp. 257–283.

8. Vigueira CC, Olsen KM, Caicedo AL. The red queen in the corn: Agricultural weeds as models of rapid adaptive evolution. Heredity. 2013;119:303–311. doi: 10.1038/hdy.2012.104 23188175

9. Mercuri AM, Fornaciari R, Gallinaro M, Vanin S, Di Lernia S. Plant behaviour from human imprints and the cultivation of wild cereals in Holocene Sahara. Nature Plants. 2018;4(2):71–81. doi: 10.1038/s41477-017-0098-1 29379157

10. Plaas E, Meyer-Wolfarth F, Banse M, Bengtsson J, Bergmann H, Faber J, et al. Towards valuation of biodiversity in agricultural soils: A case for earthworms. Ecological Economics. 2019;159:291–300. doi: 10.1016/j.ecolecon.2019.02.003

11. Brussaard L, Aanen DK, Briones MJI, Decaëns T, Deyn GBD, Fayle TM, et al. Biogeography and Phylogenetic Community Structure of Soil Invertebrate Ecosystem Engineers: Global to Local Patterns, Implications for Ecosystem Functioning and Services and Global Environmental Change Impacts. In: Soil Ecology and Ecosystem Services. Wall DH, Bardgett RD, Behan-Pelletier V, Henrrick J, Jones H, Ritz K, et al. editors. Oxford: University Press; 2013. pp. 201–232.

12. Dupont L, Decaëns T, Lapied E, Chassany V, Marichal R, Dubs F, et al. Genetic signature of accidental transfer of the peregrine earthworm Pontoscolex corethrurus (Clitellata, Glossoscolecidae) in French Guiana. European Journal of Soil Biology. 2012;53:70–75. doi: 10.1016/j.ejsobi.2012.09.001

13. Uvarov AV. (Inter- and intraspecific interactions in lumbricid earthworms: Their role for earthworm performance and ecosystem functioning. Pedobiologi 2009;53(1):1–27. doi: 10.1016/j.pedobi.2009.05.001

14. Lobe JW, Callaham MA, Hendrix PF, Hanula JL. Removal of an invasive shrub (Chinese privet: Ligustrum sinense Lour) reduces exotic earthworm abundance and promotes recovery of native North American earthworms. Applied Soil Ecology. 2014;83:133–139. doi: 10.1016/j.apsoil.2014.03.020

15. Vestergård M, Rønn R, Ekelund F. Above-belowground interactions govern the course and impact of biological invasions. AoB PLANTS. 2015;7:plv025. doi: 10.1093/aobpla/plv025 25854693

16. Simmons W, Dávalos A, Blossey B. Forest successional history and earthworm legacy affect earthworm survival and performance. Pedobiologia. 2015;58(4):153–164. doi: 10.1016/j.pedobi.2015.05.001

17. Müller F. II.—Description of a new species of Earthworm (Lumbricus corethrurus). Annals and Magazine of Natural History. 1857;20(115):13–15. https://doi.org/10.1080/00222935709487865

18. James SW, Bartz MLC, Stanton DWG, Conrado AC, Dupont L, Taheri S., et al. A neotype for Pontoscolex corethrurus (Müller, 1857) (Clitellata). Zootaxa. 2019;4545(1):124–132. doi: 10.11646/zootaxa.4545.1.7 30647239

19. Fragoso GC. Importancia de las lombrices de tierra (Oligochaeta) en el monitoreo de áreas prioritarias de conservación del centro, este y sureste de México. CONABIO. 2018. Available from: https://doi/10.15468/omvnpi accessed via GBIF.org on 2019-05-01

20. Taheri S, Pelosi C, Dupont L. Harmful or useful? A case study of the exotic peregrine earthworm morphospecies Pontoscolex corethrurus. Soil Biology and Biochemistry. 2018b;116:277–289. doi: 10.1016/j.soilbio.2017.10.030

21. Nackley LL, West AG, Skowno AL, Bond WJ. The Nebulous Ecology of Native Invasions. Trends in Ecology and Evolution. 2017;32(11):814–824. doi: 10.1016/j.tree.2017.08.003 28890126

22. Orell T. NMNH Extant Specimen Records. Version 1.2. National Museum of Natural History, Smithsonian Institution. 2019. Available from: 10.15468/hnhrg3 accessed via GBI.org on 2019-05-01. https://www.gbif.org/occurrence/1318951655

23. Ortiz-Ceballos AI, Fragoso C, Equihua M, Brown GG. Influence of food quality, soil moisture and the earthworm Pontoscolex corethrurus on growth and reproduction of the tropical earthworm Balanteodrilus pearsei. Pedobiologia. 2005;49(1):89–98. doi: 10.1016/j.pedobi.2004.08.006

24. Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions. 2000;6(2):93–107. doi: 10.1046/j.1472-4642.2000.00083.x

25. Ricciardi A, Cohen J. The invasiveness of an introduced species does not predict its impact. Biological Invasions. 2007;9(3):309–315. doi: 10.1007/s10530-006-9034-4

26. Willcox G. The Beginnings of Cereal Cultivation and Domestication in Southwest Asia. In: Potts DT, editor. A Companion to the Archaeology of the Ancient Near East. London: Blackwell Publishing Ltd. 2012; pp. 161–180. doi: 10.1002/9781444360790.ch9

27. Clement CR, Denevan WM, Heckenberger MJ, Junqueira AB, Neves EG, Teixeira WG, et al. The domestication of amazonia before european conquest. Proceedings of the Royal Society B: Biological Sciences 2015;282:20150813. doi: 10.1098/rspb.2015.0813 26202998

28. Levis C, Flores BM, Moreira PA, Luize BG, Alves RP, Franco-Moraes J, et al. How People Domesticated Amazonian Forests. Frontiers in Ecology and Evolution. 2018 Jan 17. Available from: https://doi.org/10.3389/fevo.2017.00171

29. Watling J, Shock MP, Mongeló GZ, Almeida FO, Kater T, De Oliveira PE, et al. Direct archaeological evidence for Southwestern Amazonia as an early plant domestication and food production centre. Plos One. 2018;13(7):e0199868. doi: 10.1371/journal.pone.0199868 30044799

30. Ford A, Nigh R. Origins of the Maya Forest Garden: Maya Resource Management. Journal of Ethnobiology. 2009;29(2):213–236. doi: 10.2993/0278-0771-29.2.213

31. McNeil CL. Deforestation, agroforestry, and sustainable land management practices among the Classic period Maya. Quaternary International. 2012;249:19–30. doi: 10.1016/j.quaint.2011.06.055

32. Glaser B, Balashov E, Haumaier L, Guggenberger G, Zech W. Black carbon in density fractions of anthropogenic soils of the Brazilian Amazon region. Organic Geochemistry. 2000;31:669–678. doi: 10.1016/S0146-6380(00)00044-9

33. Lima HN, Schaefer ER, Mello JWV, Gilkes RJ, Ker JC. Pedogenesis and pre-Colombian land use of “Terra Preta Anthrosols” (“Indian black earth”) of Western Amazonia. Geoderma. 2002;110:1–17.

34. Schaefer CEGR Lima HN, Gilkes RJ Mello JWV. Micromorphology and electron microprobe analysis of phosphorus and potassium forms of an Indian Black Earth (IBE) Anthrosol form Western Amazonia. Australian Journal of Soil Research. 2004;24(4):401–409.

35. Topoliantz S, Ponge JF. Charcoal consumption and casting activity by Pontoscolex corethrurus (Glossoscolecidae). Applied Soil Ecology. 2005;28:217–224.

36. Ponge JF, Topoliantz S, Ballof S, Rossi JP, Lavelle P, Betsch JM, et al. Ingestion of charcoal by the Amazonian earthworm Pontoscolex corethrurus: A potential for tropical soil fertility. Soil Biology and Biochemistry. 2006;38(7):2008–2009. doi: 10.1016/j.soilbio.2005.12.024

37. Kim JS, Sparovek G, Longo RM, de Melo WJ, Crowley D. Bacterial diversity of terra and pristine forest soil from Western Amazon. Soil Biology & Biochemistry. 2007;39:684–690.

38. Laland KN, Odling-Smee FJ, Feldman MW. Evolutionary consequences of niche construction and their implications for ecology. Proceedings of the National Academy of Sciences. 1999;96(18):10242–10247.

39. Lavelle P, Barois I, Cruz I, Fragoso C, Hernandez A, Pineda A, Rangel P. Adaptive strategies of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta), a peregrine geophagous earthworm of the humid tropics. Biology and Fertility of Soils. 1987;5(3):188–194. doi: 10.1007/BF00256899

40. Fragoso C, Leyequién E, García-Robles M, Montero-Muñoz J, Rojas P. Dominance of native earthworms in secondary tropical forests derived from slash-and-burn Mayan agricultural practices (Yucatán, Mexico). Applied Soil Ecology. 2016;104:116–124. doi: 10.1016/j.apsoil.2015.12.005

41. Marichal R, Martinez AF, Praxedes C, Ruiz D, Carvajal AF, Oszwald J, et al. Invasion of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta) in landscapes of the Amazonian deforestation arc. Applied Soil Ecology. 2010;64(3):443–449. doi: 10.1016/j.apsoil.2010.09.001

42. Ortiz-Ceballos AI, Fragoso C. Earthworm populations under tropical maize cultivation: the effect of mulching with Velvetbean. Biol. Fert. Soils. 2004;39:438–445

43. Huerta E, Fragoso C, Rodriguez-Olan J, Evia-Castillo I, Montejo-Meneses E, Cruz-Mondragon M, García-Hernández R. Presence of exotic and native earthworms in principal agro- and natural systems in Central and Southeastern Tabasco, Mexico. Caribbean Journal of Science. 2006;42(3):359–365.

44. Lavelle P, Maury ME, Serrano V. Estudio cuantitativo de la fauna del suelo en la región de Laguna Verde, Veracruz. Publicaciones Instituto de Ecología (México). 1981;6:75–105.

45. Ortiz-Gamino D, Pérez-Rodríguez P, Ortiz-Ceballos AI. Invasion of the tropical earthworm Pontoscolex corethrurus (Rhinodrilidae, Oligochaeta) in temperate grasslands. PeerJ. 2016;4:e2572. doi: 10.7717/peerj.2572 27761348

46. Stitzer MC, Ross-Ibarra J. Maize domestication and gene interaction. New Phytologist. 2018;220:395–408. doi: 10.1111/nph.15350 30035321

47. Taheri S, James S, Roy V, Decaëns T, Willians BW, Anderson F, et al. Complex taxonomy of the ‘brush tail’ peregrine earthworm Pontoscolex corethrurus. Molecular Phylogenetics and Evolution. 2018a;124:60–70. doi: 10.1016/j.ympev.2018.02.021 29501375

48. Rodrigues JLM, Pellizari VH, Mueller R, Baek K, da C. Jesus E, Paula FS, et al. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. PNAS. 2013;110(3):988–993. doi: 10.1073/pnas.1220608110 23271810

49. Gilot-Villenave C. Determination of the origin of the different growing abilities of two populations of Millsonia anomala (Omodeo and Vaillaud), a tropical geophageous earthworm. European Journal of Soil Biology. 1994;39(3):125–131.

50. De Menezes AB, Prendergast-Miller MT, Macdonald LM, Toscas P, Baker G, Farrell M, et al. Earthworm-induce shofts in microbial diversity in soils with rare versus established invasive earthworm populations. FEMS Microbiology Ecology. 2018;94(5):fiy051. doi: 10.1093/femsec/fiy051 29579181

51. Sánchez-De León Y, Zou X. Plant influences on native and exotic earthworms during secondary succession in old tropical pastures. Pedobiologia. 2004;48(3):215–226. doi: 10.1016/j.pedobi.2003.12.006

52. Philippot L, Raaijmakers JM, Lemanceau P & Van Der Putten WH. Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews Microbiology. 2013;11:789–799. doi: 10.1038/nrmicro3109 24056930

53. Zachmann JE, Molina JAE. Presence of culturable bacteria in cocoons of the earthworm Eisenia fetida. Applied and Environmental Microbiology. 1993;59(6):1904–1910. 16348968

54. Schramm A, Davidson SK, Dodsworth JA, Drake HL, Stahl DA, Dubilier N. Acidovorax-like symbionts in the nephridia of earthworms. Environmental Microbiology. 2003;5(9):804–809. 12919416

55. Daane LL, Häggblom MM. Earthworm egg capsules as vectors for the environmental introduction of biodegradative bacteria. Applied and Environmental Microbiology. 1999;65:2376–2381. 10347016

56. Lund MB, Davidson SK, Holmstrup M, James S, Kjeldsen KU, Stahl DA, et al. Diversity and host specificity of the Verminephrobacter-earthworm symbiosis. Environmental Microbiology. 2010a;12(8):2142–2151. doi: 10.1111/j.1462-2920.2009.02084.x 21966909

57. Lund MB, Holmstrup M, Lomstein BA, Damgaard C, Schramm A. Beneficial effect of Verminephrobacter nephridial symbionts on the fitness of the earthworm Aporrectodea tuberculata. Applied and Environmental Microbiology. 2010b;76(14):4738–4743. doi: 10.1128/AEM.00108-10 20511426

58. Aira M, Pérez-Losada M, Domínguez J. Diversity, structure and sources of bacterial communities in earthworm cocoons. Scientific Reports. 2018;8:6632. doi: 10.1038/s41598-018-25081-9 29700426

59. Nozaki M, Miura C, Tozawa Y, Miura T. The contribution of endogenous cellulase to the cellulose digestion in the gut of earthworm (Pheretima hilgendorfi: Megascolecidae). Soil Biology and Biochemistry. 2009;41(4):762–769. doi: 10.1016/j.soilbio.2009.01.016

60. Shweta M. Cellulolysis. A transient property of earthworm or symbiotic/ingested microorganisms? International Journal of Scientific and Research Publications. 2012;2(11):1–8.

61. Ueda M, Ito A, Nakazawa M, Miyatake K, Sakaguchi M, Inouye K. Cloning and expression of the cold-adapted endo-1,4-β-glucanase gene from Eisenia fetida. Carbohydrate Polymers. 2014;101:511–516. doi: 10.1016/j.carbpol.2013.09.057 24299806

62. Park IY, Cha JR, Ok SM, Shin C, Kim JS, Kwak HJ, et al. A new earthworm cellulase and its possible role in the innate immunity. Developmental and Comparative Immunology. 2017;67:476–480. doi: 10.1016/j.dci.2016.09.003 27614272

63. Thakuria D, Schmidt O, Finan D., Egan D., & Doohan F.M. (2010). Gut wall bacteria of earthworms: A natural selection process. ISME Journal 4, 357–366. doi: 10.1038/ismej.2009.124 19924156

64. Liu D, Lian B, Wu C, Guo P. Earthworms’ Transcriptome and Gut Microbiota Response to Mineral Weathering. Acta Geologica Sinica—English Edition. 2017;91(1):1–2. doi: 10.1111/1755-6724.13232

65. Liu D, Lian B, Wu C, Guo P. A comparative study of gut microbiota profiles of earthworms fed in three different substrates. Symbiosis 2018;74(1):21–29. doi: 10.1007/s13199-017-0491-6

66. Gong X, Jiang Y, Zheng Y, Chen X, Li H, Hu F, Liu M, Scheu S. Earthworms differentially modify the microbiome of arable soils varying in residue management. Soil Biology and Biochemistry. 2018;121:120–129. doi: 10.1016/j.soilbio.2018.03.011

67. Ikeda H, Fukumori K, Shoda-Kagaya E, Takahashi M, Ito MT, Sakai Y, Matsumoto K. Evolution of a key trait greatly affects underground community assembly process through habitat adaptation in earthworms. Ecology and Evolution. 2018;8(3):1726–1735. doi: 10.1002/ece3.3777 29435247

68. Davidson SK, Powell R, James S. (A global survey of the bacteria within earthworm nephridia. Molecular Phylogenetics and Evolution 2013;67:188–200. doi: 10.1016/j.ympev.2012.12.005 23268186

69. Davidson S, Stahl DA. Transmission of nephridial bacteria of the earthworm Eisenia fetida. Applied and Environmental Microbiology. 2006;72(1):769–775. doi: 10.1128/AEM.72.1.769-775.2006 16391117

70. Møller P, Lund MB, Schramm A. Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria. Frontiers in Microbiology. 2015;6:529. doi: 10.3389/fmicb.2015.00529 26074907

71. Ponesakki V, Paul S, Mani DK S, Rajendiran V, Kanniah P, Sivasubramaniam S. Annotation of nerve cord transcriptome in earthworm Eisenia fetida. Genomics Data. 2017;14:91–105. doi: 10.1016/j.gdata.2017.10.002 29204349

72. Ortiz-Ceballos AI, Pérez-Staples D, Pérez-Rodríguez P. Nest site selection and nutritional provision through excreta: a form of parental care in a tropical endogeic earthworm. PeerJ. 2016;4:e2032. doi: 10.7717/peerj.2032 27231655

73. Schult N, Pittenger K, Davalos S, McHugh D. Phylogeographic analysis of invasive Asian earthworms (Amynthas) in the northeast United States. Invertebrate Biology. 2016;135(4):314–327. doi: 10.1111/ivb.12145

74. Fernández-Marchán DF, Díaz-Cosín DJ, Novo M. Why are we blind to cryptic species? Lessons from the eyeless. European Journal of Soil Biology. 2018;86:49–51. doi: 10.1016/j.ejsobi.2018.03.004

75. Denevan WM. The Pristine Myth: The Landscape of the Americas in 1492. Annals of the Association of American Geographers. 1992;82(3):369–385. doi: 10.1111/j.1467-8306.1992.tb01965.x

76. Kowarik I. On the role of alien species in urban flora and vegetation. In: Marzluff JM, Shulenberger E, Endlicher w, Alberti M, Bradley G, Ryan C, et al. editors. Urban Ecology: An International Perspective on the Interaction Between Humans and Nature. USA: Spinger Us; 1995. pp. 321–338. doi: 10.1007/978-0-387-73412-5_20

77. Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences. 2007;11(5):1633–1644. doi: 10.5194/hess-11-1633-2007

78. Righi G. Pontoscolex (Oligochaeta, Glossoscolecidae), a New Evaluation. Studies on Neotropical Fauna and Environment. 1984;19(3):159–177. doi: 10.1080/01650528409360653

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