Abstract
Agroecological productivity of the Arganeraie Biosphere Reserve of Morocco is limited by the wide spread and dynamics of plant parasitic nematodes (PPN). Ecological studies of nematode communities are required to develop effective biological management of these bioagressors as conventional control methods of PPN are inadequate and have persistent harmful effects. Fifty-nine organic vegetable soils in Souss-Massa were nematologically sampled, and assessment of taxonomic proliferation was made in relation to host species, geographical origin, and climatic and microclimatic factors. Twenty-four nematode genera were identified as obligate and facultative plant feeders. Taxonomic diversity increased from Chtouka to Taroudant and Tiznit provinces. Soil texture, organic matter, pH, nitrogen, zinc, magnesium, copper, altitude, and humidity and temperature were seen to effect driving roles in the abundance, distribution, and community structures of nematodes. The most prevalent taxa posing a high risk to organic agriculture of Souss Massa were needle nematodes (Longidorus spp.) and root-knot nematodes (Meloidogyne spp.). Edaphic and climatic variables effected nematode populations greatly. A combination of biological treatments and appropriate agroecological practices restricting important economic PPN growth and enhancing soil quality are required to achieve sustainable management in the area.









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Afouda L, Baimey H, Fanou H (2008) Evaluation of Amaranthus sp. and Vernonia amygdalina, and soil amendments with poultry manure for the management of root-knot nematodes on eggplant. Phytoparasitica 36(4):368–376
Agence du Bassin Hydraulique Souss Massa (2019) Modeling study of climate change in Souss Massa; mission 1 (study in progress). Unpublished internal data provided by the agency ABHSM.
Aït Hamza M, Ferji Z, Ali N, Tavoillot J, Chapuis E, El Oualkadi A et al (2015) Plant-parasitic nematodes associated with olive tree in Southern Morocco. Int J Agric Biol 17(4):719–726
Aït Hamza M, Moukhli A, Ferji Z, Fossati-Gaschignard O, Tavoillot J, Ali N, Boubaker H, el Mousadik A, Mateille T (2018) Diversity of plant-parasitic nematode communities associated with olive nurseries in Morocco: origin and environmental impacts. Appl Soil Ecol 124:7–16
Al-Hazmi AS, Dawabah AA, Al-Nadhary SN, Al-Yahya FA, Lafi HA (2017) Influence of soil texture and moisture on the interaction of Meloidogyne javanica and Macrophomina phaseolina on green beans. J Exp Biol Agric Sci 5(1):148–154
Allison LE (1960) Wet-combustion apparatus and procedure for organic and inorganic carbon in soil 1. Soil Sci Soc Am J 24(1):36–40
Ali N, Tavoilot J, Besnard G et al (2017) How anthropogenic changes may affect soil-borne parasite diversity? Plant-parasitic nematode communities associated with olive trees in Morocco as a case study. BMC Ecol 17:4. https://doi.org/10.1186/s12898-016-0113-9
Amosu JO, Taylor DP (1974) Interaction of Meloidogyne hapla, Pratylenchus penetrans, and Tylenchorhynchus agri on Kenland red clover, Trifolium pratense. Indian J Nematol 4:124–131
Anwar SA, Mahdi MM, McKenry MV, Qadir A (2013) Survey of plant-parasitic nematodes associated with four vegetable crops cultivated within tunnels. Pak J Zool 45(3):595–603
Anwar SA, McKenry MV (2012) Incidence and population density of plant-parasitic nematodes infecting vegetable crops and associated yield losses. Pak J Zool 44:327–333
Ashley R, Bishop A, Dennis J (2007) Intensive organic vegetable production integrated development. A report for the Rural Industries Research and Development Corporation. RIRDC Publication No 04/121 RIRDC Project No: DAT-37A, 46 pp Google Scholar
Audebert A, Coyne DL, Dingkuhn M, Plowright RA (2000) The influence of cyst nematodes (Heterodera sacchari) and drought on water relations and growth of upland rice in Cote d'Ivoire. Plant Soil 220(1-2):235–242
Badra T, Yousif GM (1979) Comparative effects of potassium levels on growth and mineral composition of intact and nematized cowpea and sour orange seedlings. Nematol Mediterr 7:21–27
Baimey H, Coyne D, Dagbenonbakin G, James B (2009) Plant-parasitic nematodes associated with vegetable crops in Benin: relationship with soil physico-chemical properties. Nematol Mediterr 37(2):227–236
Bakonyi G, Nagy P, Kovacs-Lang E, Kovacs E, Barabás S, Répási V, Seres A (2007) Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Appl Soil Ecol 37(1-2):31–40
Barbano DM, Clark JL, Dunham CE, Flemin RJ (1990) Kjeldahl method for determination of total nitrogen content of milk: collaborative study. J Assoc Off Anal Chem 73(6):849–859
Barker KR, Koenning SR (1998) Developing sustainable systems for nematode management. Annu Rev Phytopathol 36(1):165–205
Barker KR, Pederson GA, Windham GL (eds) (1998) Plant nematode interactions. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison
Benjlil H, Elkassemi K, Hamza MA, Mateille T, Furze JN, Cherifi K, Ferji Z (2020) Plant-parasitic nematodes parasitizing saffron in Morocco: structuring drivers and biological risk identification. Appl Soil Ecol 147:103362. https://doi.org/10.1016/j.apsoil.2019.103362
Blok VC, Jones JT, Phillips MS, Trudgill DL (2008) Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. BioEssays 30:249–259
Boag B, Crawford JW, Neilson R (1991) The effect of potential climatic changes on the geographical distribution of the plant-parasitic nematodes Xiphinema and Longidorus in Europe. Nematologica 37(1-4):312–323
Bongers T (1988) De Nematoden van Nederland. Stichting Uitgeverij Koninklijke Nederlandse NatuurhistorischeVereniging, Utrecht, 408 p
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19
Bougeard S, Qannari EM, Lupo C, Hanafi M (2011) From multiblock partial least squares to multiblock redundancy analysis. A continuum approach. Informatica 22(1):11–26
Cadet P, Thioulouse J (1998) Identification of soil factors that relate to plant-parasitic nematode communities on tomato and yam in the French West Indies. Appl Soil Ecol 8(1-3):35–49
Castillo P, Nico AI, Navas-Cortés JA, Landa BB, Jiménez-Díaz RM, Vovlas N (2010) Plant-parasitic nematodes attacking olive trees and their management. Plant Dis 94(2):148–162
Chessel D, Dufour AB, Thioulouse J (2004) The ADE 4 package-1. One-table methods. R News 4:5–10
Choshali AH, Seraji A, Rezaee S, Shirinfekr A, Mirghasemi SN (2015) The effects of soil organic matter content and soil texture on the population number of Pratylenchus loosi, in tea plantation of Iran. International Journal of Agronomy and Agricultural Research 6(2):54–62
Chowdhury IA, Yan G, Friskop A (2019) Occurrence of vermiform plant-parasitic nematodes in North Dakota corn fields and impact of environmental and soil factors. Can J Plant Pathol 42:429–444. https://doi.org/10.1080/07060661.2019.1674384
Coakley SM, Scherm H, Chakraborty S (1999) Climate change and plant disease management. Annu Rev Phytopathol 37(1):399–426
Colagiero M, Ciancio A (2011) Climate changes and nematodes: expected effects and perspectives for plant protection. Redia 94:113–118
De Guiran GL, Bonnel M, Abirached M (1980) Landspreading of pig manures IV. Effect on soil nematodes. In: Gasser JE (ed) Effluents from Livestock. Appl, Sci. London, pp 109–119
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20
Duyck PF, Dortel E, Tixier P, Vinatier F, Loubana PM, Chabrier C, Quénéhervé P (2012) Niche partitioning based on soil type and climate at the landscape scale in a community of plant-feeding nematodes. Soil Biol Biochem 44(1):49–55
EFSA PLH Panel (EFSA Panel on Plant Health) (2014) Scientific Opinion on the pest categorisation of Radopholus similis (Cobb) Thorne and Radopholus citrophilus Huettel, Dickson and Kaplan. EFSA J 12(10):3852. doi:https://doi.org/10.2903/j.efsa.2014.3852
Eisenback JD (1993) Interactions between nematodes in cohabitance. In: Khan MW (ed) Nematode interactions. Springer, Dordrecht, pp 134–174
Evans AA, Perry RN (2009) Survival mechanisms. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CABI, Wallingford, pp 201–222
Falissard B (2012) psy: Various procedures used in psychometry. R package version 1.1. https://CRAN.R-project.org/package=psy
Fortuner R, Merny G (1973) Nematode root-parasites associated with rice in lower Casamance (Senegal) and Gambia. Cahiers ORSTOM Série Biologie 21:4–43
Francl LJ (1993) Multivariate analysis of selected edaphic factors and their relationship to Heterodera glycines population density. J Nematol 25(2):270–276
Georgieva SS, McGrath SP, Hooper DJ, Chambers BS (2002) Nematode communities under stress: the long-term effects of heavy metals in soil treated with sewage sludge. Appl Soil Ecol 20(1):27–42
Grandison GS, Wallace HR (1974) The distribution and abundance of Pratylenchus thornei in fields of strawberry clover (Trifolium fragiferum). Nematologica 20(3):283–290
Haegeman A, Elsen A, De Waele D, Gheysen G (2010) Emerging molecular knowledge on Radopholus similis, an important nematode pest of banana. Mol Plant Pathol 11(3):315–323
Hedges JI, Oades JM (1997) Comparative organic geochemistries of soils and marine sediments. Org Geochem 27(7-8):319–361
Hominick B (1999) Nematodes. In: Proceeding of the International Workshop Tropical Soil Biology: Opportunities and Challenges for African Agriculture. March, Nairobi, pp 16–19
ISO 23611-4 (2007) Soil quality – sampling of soil invertebrates– part 4: sampling, extraction and identification of soil-inhabiting nematodes. International Organization for Standardization, Geneva
Jones FGW, Perry JN (1978) Modelling populations of cyst-nematodes (Nematoda: Heteroderidae). J Appl Ecol:349–371
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14(9):946–961
Kandji ST, Ogol CK, Albrecht A (2001) Diversity of plant-parasitic nematodes and their relationships with some soil physico-chemical characteristics in improved fallows in western Kenya. Appl Soil Ecol 18(2):143–157
Khalil MS (2013) Alternative approaches to manage plant-parasitic nematodes. J Plant Pathol Microbiol 04. https://doi.org/10.4172/2157-7471.1000e105
Kincaid RR, Martin FG, Gammon N, Breland HL, Pritchett WL (1970) Multiple regression of tobacco black shank, root-knot and coarse root indexes on soil pH, potassium, calcium and magnesium. Phytopathology 60(10):1513–1516
Koenning SR, Overstreet C, Noling JW, Donald PA, Becker JO, Fortnum BA (1999) Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J Nematol 31:587–618
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25(1):1–18
Lindsay WL, Norvell W (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper 1. Soil Sci Soc Am J 42(3):421–428
Loof PAA (1991) The family Pratylenchidae Thorne, 1949. In: Nickle WR (ed) Manual of Agricultural Nematology. Marcel Dekker, Inc., New York, pp 363–421
Luc M, Bridge J, Sikora RA (2005) Reflections on nematology in subtropical and tropical agriculture. Plant-parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford
Mai WF, Mullin PG (1996) Plant-Parasitic Nematodes. A Pictorial Key to Genera, 5th edn. Comstock Publishing Associates, New-York
MAPMDREF : Ministère de l'agriculture, de la pêche maritime, du développement rural et des eaux et forêts (2018). Agriculture in figures 2018 edition 2019. http://www.agriculture.gov.ma/pages/publications/agriculture-en-chiffres-2018-edition-2019 (in French)
Maqbool MA (1992) Distribution and host association of plant-parasitic nematodes in Pakistan. National Nematological Research Centre, Karachi
Mateille T, Tavoillot J, Martiny B, Dmowska E, Winiszewska G, Ferji Z, Msanda F, Mousadik AE (2016) Aridity or low temperatures: What affects the diversity of plant-parasitic nematode communities in the Moroccan argan relic forest? Appl Soil Ecol 101:64–71
McSorley R, Frederick JJ (2002) Effect of subsurface clay on nematode communities in a sandy soil. Appl Soil Ecol 19(1):1–11
Neilson R, Boag B (1996) The predicted impact of possible climatic change on virus-vector nematodes in Great Britain. Eur J Plant Pathol 102(2):193–199
Nico AI, Rapoport HF, Jiménez-Díaz RM, Castillo P (2002) Incidence and population density of plant-parasitic nematodes associated with olive planting stocks at nurseries in Southern Spain. Plant Dis 86(10):1075–1079
Nicol JM (2002) Important nematode pests. FAO plant production and protection series. http://www.fao.org/3/y4011e/y4011e00.htm#Contents
Noling JW (1986) Partitioning crop losses among pest groups. J Nematol 18:594–594
Olle M, Williams IH (2012) Organic farming of vegetables. In: Lichtfouse E (ed) Sustainable Agriculture Reviews. Springer, Dordrecht, pp 63–76
Oostenbrink M (1960) Estimating nematode populations by some selected methods. Nematology 85-102
Oostenbrink M (1966) Major characteristics of the relation between nematodes and plants. Wageningen, Veenman
Ornat C, Sorribas FJ (2008) Integrated management of root-knot nematodes in Mediterranean horticultural crops. In: Ornat C, Sorribas FJ (eds) Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes. Springer, Dordrecht, pp 295–319
Plowright R, Coyne D (2002) Assessment of the importance of individual plant-parasitic nematode species in a community dominated by Heterodera sacchari on upland rice in Cote d’Ivoire. Nematology 4(6):661–669
Popovici I, Ciobanu M (2010) Diversity and distribution of nematode communities in grasslands from Romania in relation to vegetation and soil characteristics. Appl Soil Ecol 14(1):27–36
Powell NT (1971) Interactions between nematodes and fungi in disease complexes. Annu Rev Phytopathol 9(1):253–274
Qi Y, Hu C (2007) Soil nematode abundance in relation to diversity in different farming management system. World J Agric Sci 3:587–592
Regnault RC, Philogène BJR, Vincent C (2008) Biopesticides of Plant Origin. Lavoisier, Paris (in French)
Richards LA (1954) Diagnosis and Improvement of Saline and Alkali Soils. USDA Handbook 60:84–156
Roberts PA, Ulloa M (2010) Introgression of root-knot nematode resistance into tetraploid cottons. Crop Sci 50(3):940–951
Robinson AF, Heald CM, Flanagan SL, Thames WH, Amador J (1987) Geographical distributions of Rotylenchulus reniformis, Meloidogyne incognita, and Tylenchulus semipenetrans in the Lower Rio Grande Valley as related to soil texture and land use. J Nematol 19(1):20–25
Rodriguez-Kabana R (1986) Organic and inorganic nitrogen amendments to soil as nematode suppressants. J Nematol 18(2):129–134
Ross J (1964) Interaction of Heterodera glycines and Meloidogyne incognita on soybeans. Phytopathology 54(3):304–307
Sasser JN (1989) Plant-parasitic nematodes: the farmer's hidden enemy. A cooperative publication of the Department of Plant Pathology and the Consortium for International Crop Protection, Raleigh, USA
Sehgal HL, Gaur HS (1999) Important nematode problems of India. Technical Bulletin NCIMP, New Delhi
Seinhorst JW (1982) The relationship in field experiments between population density of Globodera rostochiensis before planting potatoes and yield of potato tubers. Nematologica 28(3):277–284
Sims JT, Johnson GV (1991) Micronutrient soil tests. Micronutrients in Agriculture 4:427–476
Starr JL, Moresco ER, Smith CW, Nichols RL, Roberts PA, Chee P (2010) Inheritance of resistance to Meloidogyne incognita in primitive cotton accessions from Mexico. J Nematol 42(4):352–358
Starr JL, Roberts PA (2004) Resistance to plant-parasitic nematodes. Nematology, Advances and Perspectives 2:879–907
Taylor CE (1971) Nematodes as vector of plant viruses. Plant-Parasitic Nematodes 2:185–211
Thompson JP, Clewett TG, Sheedy JG, Reen RA, O’reilly MM, Bell KL (2010) Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia. Australas Plant Pathol 39(3):254–264
Treonis AM, Unangst SK, Kepler RM, Buyer JS, Cavigelli MA, Mirsky SB, Maul JE (2018) Characterization of soil nematode communities in three cropping systems through morphological and DNA metabarcoding approaches. Sci Rep 8(1):1–12
Tzortzakakis EA, Trudgill DL (2005) A comparative study of the thermal time requirements for embryogenesis in Meloidogyne javanica and M. incognita. Nematology 7(2):313–315
van Den Hoogen J, Geisen S, Routh D, Ferris H, Traunspurger W, Wardle DA et al (2019) Soil nematode abundance and functional group composition at a global scale. Nature 572(7768):194–198
van Den Hoogen J, Geisen S, Wall DH, Wardle DA, Traunspurger W, de Goede RG et al (2020) A global database of soil nematode abundance and functional group composition. Scientific Data 7(1):1–8
Walkley AJ, Black IA (1934) Estimation of soil organic carbon by the chromic acid titration method. Soil Sci 37:29–38
Wallace HR (1962) Observations on the behaviour of Ditylenchus dipsaci in soil. Nematologica 7(1):91–101
Wang C, Bruening G, Williamson VM (2009) Determination of preferred pH for root-knot nematode aggregation using pluronic F-127 gel. J Chem Ecol 35(10):1242–1251
Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. Springer Verlag, New York
Widmer TL, Mitkowski NA, Abawi GS (2002) Soil organic matter and management of plant-parasitic nematodes. J Nematol 34(4):289
Willer H, Schlatter B, Travnick J, Kemper L, Lernoud J (2020) The World of Organic Agriculture. Statistics and Emerging Trends 2020. Research Institute of Organic Agriculture (FiBL), Frick, and IFOAM Organic International, Bonn
Yavuzaslanoglu E, Elekcioglu HI, Nicol JM, Yorgancilar O, Hodson D, Yildirim AF, Yorgancilar A, Bolat N (2012) Distribution, frequency and occurrence of cereal nematodes on the Central Anatolian Plateau in Turkey and their relationship with soil physicochemical properties. Nematology 14(7):839–854
Yeates GW (2007) Abundance, diversity, and resilience of nematode assemblages in forest soils. Can J For Res 37(2):216–225
Zhong W, Gu T, Wang W, Zhang B, Lin X, Huang Q, Shen W (2010) The effects of mineral fertilizer and organic manure on soil microbial community and diversity. Plant Soil 326(1-2):511–522
Zirakparvar ME, Norton DC, Cox CP (1980) Population increase of Pratylenchus hexincisus on corn as related to soil temperature and type. J Nematol 12(4):313–318
Zoon FC, Troelstra SR, Maas PT (1993) Ecology of the plant-feeding nematode fauna associated with sea buckthorn (Hippophae rhamnoides L. ssp. rhamnoides) in different stages of dune succession. Fundam Appl Nematol 16(3):247–258
Acknowledgements
The soil samples used in this research were collected with support of organic vegetable producers in Souss-Massa region. We express our gratitude to Mr. Mohamed Doulhousen, operator in the Soil-Plant-Water Laboratory of the Agronomic and Veterinary Institute Hassan II, for assistance during soil physicochemical analyses.
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EH Mayad and I Filali Alaoui conceived the study design. I Filali Alaoui, E. Mzough, A. Idhmida, A Braimi, H Benjlil, K Basaid, and EH Mayad contributed to soil sampling and nematodes extraction. I Filali Alaoui and EH Mayad carried out the nematological analysis. I Filali Alaoui, A. Hallouti, MA Hamza, JN Furze and EH Mayad performed data analysis and interpretation. Authors contributed equally in the writing of the manuscript.
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Filali Alaoui, I., Ait Hamza, M., Benjlil, H. et al. Phytoparasitic nematodes of organic vegetables in the Argan Biosphere of Souss-Massa (Southern Morocco). Environ Sci Pollut Res 28, 64166–64180 (2021). https://doi.org/10.1007/s11356-021-12986-8
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DOI: https://doi.org/10.1007/s11356-021-12986-8


