Abstract

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.

Highlights

  • 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 [1,2,3,4]

  • In the M. pruriens and maize stubble treatments (25%, 33% and 42% soil moisture (SM)) no mortality was observed in both earthworm species

  • The endogeic earthworm P. corethrurus resembles non-domesticated species or weeds given its strong profile regarding growth rate, fertility, plasticity, interspecific competition, and Homeless invasive tropical earthworm 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]

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Summary

Introduction

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 [1,2,3,4]. The artificial landscapes that resulted from these practices (anthropocentric ecology) were exported as agricultural packages from the centers of origin [1, 2, 4]. 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 [7,8,9]. 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 [10,11]

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