Pontoscolex corethrurus: A homeless invasive tropical earthworm?


Autoři: Angel I. Ortíz-Ceballos aff001;  Diana Ortiz-Gamino aff001;  Antonio Andrade-Torres aff001;  Paulino Pérez-Rodríguez aff002;  Maurilio López-Ortega aff001
Působiště autorů: 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
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222337

Souhrn

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.

Klíčová slova:

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


Zdroje

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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