Plant-parasitic nematodes associated with olive tree (<i>Olea europaea</i> L.) with a focus on the Mediterranean Basin: A review

Nadine Ali; Elodie Chapuis; Johannes Tavoillot; Thierry Mateille

doi:10.1016/j.crvi.2014.05.006

Plant-parasitic nematodes associated with olive tree (Olea europaea L.) with a focus on the Mediterranean Basin: A review

Nadine Ali ^1,² ; Elodie Chapuis ^2,³ ; Johannes Tavoillot ² ; Thierry Mateille ²

¹ Tichreen University, Faculty of Agriculture, Plant Protection Department, PO Box 230, Latakia, Syrian Arab Republic
² IRD, UMR CBGP (Center for Biology and Management of Populations) (INRA/IRD/CIRAD/Montpellier SupAgro), campus de Baillarguet, 755, avenue du Campus-Agropolis, CS30016, 34988 Montferrier-sur-Lez cedex, France
³ IRD, UMR RPB, 911, avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France

Comptes Rendus. Biologies, Volume 337 (2014) no. 7-8, pp. 423-442.

Résumé

The olive tree (Olea europaea ssp. europaea.) is one of the most ancient cultivated trees. It is an emblematic species owing to its ecological, economic and cultural importance, especially in the Mediterranean Basin. Plant-parasitic nematodes are major damaging pests on olive trees, mainly in nurseries. They significantly contribute to economic losses in the top-ten olive-producing countries in the world. However, the damages they induce in orchards and nurseries are specifically documented only in a few countries. This review aims to update knowledge about the olive-nematode pathosystem by: (1) updating the list of plant-parasitic nematodes associated with olive trees; (2) analysing their diversity (taxonomic level, trophic groups, dominance of taxa), which allowed us (i) to assess the richness observed in each country, and (ii) to exhibit and describe the most important taxa able to induce damages on olive trees such as: Meloidogyne, Pratylenchus, Helicotylenchus, Xiphinema, Tylenchulus, Rotylenchulus, Heterodera (distribution especially in the Mediterranean Basin, pathogenicity and reactions of olive trees); (3) describing some management strategies focusing on alternative control methods; (4) suggesting new approaches for controlling plant-parasitic nematodes based on the management of the diversity of their communities, which are structured by several environmental factors such as olive diversity (due to domestication of wild olive in the past, and to breeding now), cropping systems (from traditional to high-density orchards), irrigation, and terroirs.

Métadonnées

Reçu le : 2014-03-04
Accepté le : 2014-05-16
Publié le : 2014-07-01

PMID

DOI : 10.1016/j.crvi.2014.05.006

Mots clés : Communities, Control methods, Diversity, Geographical distribution, Mediterranean Basin, Olive, Pathogenicity, Plant-parasitic nematodes

Affiliations des auteurs :

Nadine Ali ^{1, 2} ; Elodie Chapuis ^{2, 3} ; Johannes Tavoillot ² ; Thierry Mateille ²

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     author = {Nadine Ali and Elodie Chapuis and Johannes Tavoillot and Thierry Mateille},
     title = {Plant-parasitic nematodes associated with olive tree {(\protect\emph{Olea~europaea}} {L.)} with a focus on the {Mediterranean} {Basin:} {A} review},
     journal = {Comptes Rendus. Biologies},
     pages = {423--442},
     publisher = {Elsevier},
     volume = {337},
     number = {7-8},
     year = {2014},
     doi = {10.1016/j.crvi.2014.05.006},
     language = {en},
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Nadine Ali; Elodie Chapuis; Johannes Tavoillot; Thierry Mateille. Plant-parasitic nematodes associated with olive tree (Olea europaea L.) with a focus on the Mediterranean Basin: A review. Comptes Rendus. Biologies, Volume 337 (2014) no. 7-8, pp. 423-442. doi : 10.1016/j.crvi.2014.05.006. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2014.05.006/

Version originale du texte intégral

1 The olive tree: origins, dissemination and cultivation

Six Olea europaea subspecies with distinct geographic areas are distinguished [1,2] (Fig. 1):

• subsp. europaea present in the Mediterranean Basin, with two botanical varieties: O. europaea subsp. europaea var. europaea for the cultivated forms, and O. e. subsp. e. var. sylvestris for wild and spontaneous trees (usually named oleasters) [2];
• subsp. laperrinei in the Saharan mountains;
• subsp. cuspidata from southern Africa to southern Egypt and from Arabia to China;
• subsp. guanchica in the Canary Islands;
• subsp. maroccana in southern Morocco;
• subsp. cerasiformis in Madeira.

Fig. 1
Simplified diagram of the Olea genus (Oleaceae) and biogeography of taxa [11].

The Mediterranean olive (Olea europaea L. subsp. europaea; Oleaceae) is one of the first domesticated tree species [3,4]. Its origins and domestication history are still highly debated, but archaeological and molecular data sustain that the first cultivars originated from the Levant, very likely 6000 years ago, in a region presently located at the border between southwestern Turkey and northwestern Syria [5,6]. Genetic studies indicated also that olive domestication is a long and on-going process and cultivars have originated from multiple source populations, as for grape and figs [7–9]. It is currently established that western wild olives secondarily contributed to the cultivated gene pool, while most of present cultivars remain mainly related to eastern wild olives [10].

The genetic diversity of oleaster is somewhat greater than that of the cultivated olive [6,10,11]. This diversity is highly structured between the East and the West of the Mediterranean Basin [6,12,13]. The analysis of plastid DNA polymorphisms allowed the identification of 48 distinct profiles delineating three diverging lineages. Lineage E1 is currently distributed over the whole Basin, whereas lineages E2 and E3 exclusively occur in western and central Mediterranean areas [6,14].

The olive tree has long been considered as the most typical Mediterranean tree. It has been widely disseminated through conquests and exchanges that accompanied the expansion of the Mediterranean civilizations (Phoenicians, Greeks, Romans, and Arabs) [15]. Populations of wild olives are restricted to a few isolated areas of native Mediterranean forests, where pollen/stones may be spread by natural factors (wind and birds) [13]. Most other wild-looking forms of olive may include feral forms (either cultivated olive abandoned and becoming wild or olive from stones of cultivated olive spread by birds). The olive dissemination was accompanied by a secondary diversification that has led to a high genetic variability that reflects a wide range of morphological (tree vigour, fruit shape, yield, oil content, etc.) and physiological (adaptation traits to environmental stresses, particularly those related to climate and soil constraints) characteristics that can explain its large distribution in the Mediterranean Basin [16,17]. This diversity can also result from a series of events related to human practices made to meet microclimate and terroir requirements and to satisfy consumer taste [12].

More than 2000 Mediterranean varieties have been recognised based on fruit, pit, and leaf shapes and colours, tree architecture and phenology (i.e. flowering time) [18–21]. Olive cultivars are propagated vegetatively by cutting or grafting. Most of the modern varieties display a maternal lineage (E1) that is distributed all around the whole Mediterranean area [6,14,22]. However, the genetic diversity of cultivated populations exhibits a complex patchy pattern [23,24].

For cultural (traditions, landscapes) and economic (oil and olives) reasons, this tree is regarded as one of the most cultivated plant in the world, ranking the 24th among 35 species [25]. It is now distributed in the five continents. It grows extensively in Mediterranean climate regions in Australia, South Africa, North and South America and covers about 11 Mha, with 98% located in the Mediterranean Basin [26,27]. Eighty percent of the cultivated olive surface is located in northern Mediterranean countries (Spain, Italy, Greece, Turkey), 17% in the Middle East (Jordan, Syria, Iraq, Iran) and in North Africa (Morocco, Algeria, Tunisia, Egypt), and only 2% is located in North (USA) and South (Mexico, Argentina, Peru) America [28,29] (Fig. 2).

Fig. 2
World distribution of Olea europaea L. producing areas [26].

Olive diversity may also reflect a significant diversity of associated pests, some of them being specific. Major olive diseases are due to insects (e.g., the fruit fly Bactrocera oleae, the black scale Saissetia oleae, the moth Prays oleae, the borer Palpita unionalis), and to air-borne (e.g., the peacock spot Spilocaea oleaginea, the knot Pseudomonas syringae) or soil-borne (e.g., verticillium wilt Verticillium dahliae and plant-parasitic nematodes) parasites and pathogens.

2 Plant-parasitic nematodes associated with olive trees

2.1 General considerations

Nematodes are roundworms of the phylum Nematoda, Metazoa having unsegmented, cylindrical bodies with a non-ciliated tough outer cuticle. The group includes free-living forms and disease-causing parasites. Plant-parasitic nematodes (PPN) are soil-borne microscopic worms that mainly feed on plant-root cells using a spear-like structure, called a stylet. They introduce it in cells to inject digestion secretions and suck cell contents [30].

Thereby, these parasites cause significant economic damages to many types of crops as cereals, vegetables, tubers, fruit, and floral crops [31]. Annual losses caused by PPN are estimated from 8.8 to 14.6% of the world crop production (100–157 billion USD/year) [32,33]. In Europe, economic losses are estimated to 10% of the grain production and lead to reduce by 20 to 30% Mediterranean citrus production [34].

Olive trees are hosts of these parasites. But very few information is available about PPN communities associated with olive [27]. The first record was from the USA, where root-knot nematodes Meloidogyne spp. were detected [35]. Since then, some researches on olive PPN were developed in several parts of the world, mainly in Italy [36–38], Chile [39], Jordan [40], Libya [41], Spain [27,42], Portugal [43], Egypt [44–46], Iran [47,48], Turkey [49,50], Argentina [51], and Syria [52].

Most of these studies have focused on PPN description without studying their potential effects on the crop [53]. However, studies focused on taxa that represent a real threat to olive tree, particularly in the Mediterranean Basin, such as root-knot nematodes Meloidogyne [54–57], lesion nematodes Pratylenchus [58], spiral nematodes Helicotylenchus [59,60], reniform nematodes Rotylenchulus [61,62], cyst nematodes Heterodera [63,64], and dagger nematodes Xiphinema [60].

Other studies focused on assessing the impact of these parasites in nurseries, especially in Spain [27] and Iran [48].

2.2 Diversity of plant-parasitic nematodes associated with olive trees

Previous reviews updated knowledge about nematode diversity associated with olive tree [53,65–68].

Moreover, the analysis of all literature sources let to record 153 species (some as still unidentified) belonging to 56 genera related to the PPN orders Aphelenchida (4 genera and 3 species), Dorylaimida (5 genera and 36 species) and Tylenchida (48 genera and 114 species) (Table 1). Most of the species have been detected on other crops [28]. They belong to three trophic groups: plant feeders, fungal feeders (this group usually feeds on fungi but may alternatively feeds on plants, e.g. Aphelenchida nematodes) and root-hair feeders. Considering their adaptive strategies defined by colonizer/persister values (= cp-values) ranking from 1 (colonizers/r strategy) to 5 (persisters/K strategy) [69], most of these species show high reproduction rates and rapid adaptation capacities to environmental changes (cp-3).

Order	Family	Species	Country	Reference
Aphelenchida	Aphelenchidae	Aphelenchus avenae Bastian 1865	Greece Iran^a Jordan Spain	[103] [48] [40] [42]
		Aphelenchus sp. Bastian 1865	Iran Italy	[47] [36]
		Paraphelenchus pseudoparietinus Micoletzky 1921	Spain	[42]
	Aphelenchoididae	Aphelenchoides sp. Fischer 1984	Egypt Italy Jordan Spain Syria	[46] [36] [40] [42] [52]
		Aprutides guidettii Scognamiglio 1974	Spain	[42]
Dorylaimida	Longidoridae	Longidorus africanus Merny 1966	Egypt	[108]
		L. belloi Andres and Arias 1988	Portugal	[79]
		L. closelongatus Stoyanov 1964	Greece	[167]
		L. cretensis Tzortzakakis et al., 2001	Greece	[168]
		L. elongatus De Man 1876	Egypt	[46]
		L. macrosoma Hooper 1961	Spain	[42]
		L. siddiqii Aboul-Eid 1970	Jordan	[94]
		L. vinearum Bravo and Roca 1995	Portugal	[79]
		Longidorus sp. Micoletzky 1922	Egypt Italy Spain^a Syria	[60] [36] [27] [52]
		Paralongidorus sp. Siddiqi et al., 1963	Italy	[110]
		Xiphinema aequum [112]	Italy	[112]
		X. barense Lamberti et al., 1986	Italy	[113]
		X. californicum Lamberti and Bleve-Zacheo 1979	USA	[114]
		X. diversicaudatum Micoletzky, 1927	Portugal	[115]
		X. elongatum Schuurmans Stekhoven and Teunissen, 1938	Egypt	[60]
		X. index Thorne and Allen 1950	Greece Italy Jordan	[169] [121] [40]
		X. ingens Luc and Dalmasso 1964	Italy Jordan	[116] [94]
		X. italiae Meyl 1953	Italy	[78]
		X. lusitanicum Sturhan, 1983	Portugal	[79]
		X. macroacanthum Lamberti et al., 1990	Italy	[117]
		X. nuragicum Lamberti et al., 1992	Spain	[17]
		X. pachtaicum Tulaganov 1938	Italy Jordan Portugal Spain Spain^a	[68] [94] [79] [17] [27]
		X. sahelense Dalmasso, 1969	Spain	[118]
		X. turcicum Luc and Dalmasso, 1964	Spain	[42]
		X. vuittenezi Luc et al., 1964	Spain	[118]
		Xiphinema sp. Cobb, 1913	Chile Egypt Iran Israel Italy Jordan Spain	[120] [46] [47] [170] [36] [171] [172]
	Trichodoridae	Paratrichodorus alleni Siddiqi, 1974	Italy	[142]
		P. minor Colbran 1956	Spain^a	[27]
		P. teres Hooper 1962	Spain^a	[27]
		Paratrichodorus sp. Siddiqi 1974	Jordan	[40]
		Trichodorus aequalis Allen 1957	Spain	[42]
		T. andalusicus Decraemer et al., 2012	Spain^b	[140]
		T. iliplaensis Decraemer et al., 2012	Spain	[140]
		T. giennensis Decraemer et al., 1993	Spain^a	[27]
		T. lusitanicus Siddiqi, 1974	Portugal	[143]
		T. parasilvestris Decraemer et al., 2012	Spain	[140]
		T. primitivus De Man 1880	Portugal	[143]
		T. silvestris Decraemer et al., 2012	Spain^b	[140]
		T. taylori Mancine 1980	Italy	[141]
		T. variopapillatus Hooper, 1972	Italy	[142]
		Trichodorus sp. Cobb 1913	Chile Italy	[120] [36]
Tylenchida	Anguinidae	Ditylenchus anchiliposomus Tarjan 1958	Spain	[42]
		D. dipsaci Kuhn 1857	Jordan Spain	[40] [173]
		D. virtudesae Tobar-Jimenez 1964	Spain	[172]
		Ditylenchus sp. Filipjev 1936	Italy Jordan Spain	[36] [171] [42]
	Criconematidae	Criconema annuliferum De Man 1921	Spain	[42]
		C. princeps Andrássy 1962	Portugal	[68]
		Criconema sp. Hofmänner and Menzel 1914	Greece	[169]
		Criconemella informis Micoletzky 1922	Spain	[42]
		C. sphaerocephala Taylor 1936	Spain	[42]
		C. xenoplax Raski 1952	Jordan Spain	[40] [27]
		Criconemella sp. De Grisse and Loof 1965	Spain	[42]
		Criconemoides informis Micoletzky 1922	Jordan Spain^a	[94] [27]
		Criconemoides sp. Taylor 1936	Chile Egypt Greece Italy Jordan	[120] [60] [103] [36] [171]
		Crossonema multisquamatum Kirjanova 1948	Zimbabwe	[174]
		Hemicriconemoides gaddi Loos 1949	Turkey	[49]
		Mesocriconema curvatum Raski 1952	Spain	[68]
		M. onoense Luc 1959	Brazil	[175]
		M. sicula Loof and De Grisse 1989	Italy	[176]
		M. sphaerocephalum Taylor 1936	Spain	[68]
		M. xenoplax Raski 1952	Spain^a	[27]
		Neolobocriconema olearum Hashim 1984	Jordan	[177]
		Nothocriconema princeps De Grisse and Loof 1965	Portugal	[142]
		Ogma civellae Steiner 1949	Zimbabwe	[174]
		O. rhomobosquamatum Mehta and Raski 1971	Spain	[42]
		O. seymouri Wu 1965	Jordan Italy Portugal Spain	[40] [148] [146] [68]
		Ogma sp. Mehta and Raski 1971	Italy	[110]
	Dolichodoridae	Dolichodorus heterocephalus Cobb 1911	Italy	[178]
		Dolichodorus sp. Cobb 1915	Italy	[110]
		Trophurus sp. Loof 1956	Italy	[36]
	Hemicycliophoridae	Hemicycliophora sturhani Loof 1984	Turkey	[49]
		Hemicycliophora sp. De Man 1921	Chile Spain^a	[120] [27]
	Heteroderidae	Heterodera avenae Filipjev 1934	Spain^a	[27]
		H. mediterranea Vovlas et al., 1981	Italy Spain	[63] [64]
		Heterodera sp. Filipjev and Schuurmans Stekhoven 1941	Italy	[36]
		Heteroderinae Filipjev and Schuurmans Stekhoven 1941	Spain	[42]
	Hoplolaimidae	Aorolaimus perscitus Doucet 1980	Spain	[147]
		Helicotylenchus digonicus Perry 1959	Cyprus Greece Jordan Spain Spain^a Turkey	[179] [103] [180] [17] [27] [49]
		H. dihystera Cobb 1893	Brazil Cyprus Egypt Italy Jordan Spain^a Spain Zimbabwe	[181] [179] [108] [111] [180] [27] [182] [109]
		H. erythrinae Zimmermann 1904	Italy	[59]
		H. minzi Sher 1966	Jordan	[40]
		H. neopaxili Inserra et al., 1979	Italy	[70]
		H. oleae Inserra et al., 1979	Italy	[70]
		H. pseudorobustus Steiner 1914	Greece Iran^a Italy Jordan Spain^a Spain	[103] [48] [68] [94] [27] [27]
		H. tunisiensis Siddiqi 1963	Israel Jordan Portugal Spain Turkey	[109] [94] [146] [173] [49]
		H. vulgaris Yuen 1964	Jordan Portugal Spain^a Spain Turkey	[40] [146] [27] [173] [49]
		Helicotylenchus sp. Steiner 1945	Algeria Chile Egypt Greece Iran Italy Jordan Syria	[104] [120] [46] [103] [47] [36] [171] [52]
		Hoplolaimus aorolaimoides Siddiqi 1972	Portugal	[146]
		H. galeatus Cobb 1913	Turkey	[49]
		Hoplolaimus sp. Daday 1905	Egypt Syria	[60] [52]
		Plesiorotylenchus striaticeps Vovlas et al., 1993	Turkey	[49]
		Rotylenchus buxophilus Golden 1956	Turkey	[49]
		R. cypriensis Antoniou 1980	Jordan Turkey	[40] [49]
		R. robustus De Man 1876	Portugal	[142]
		Rotylenchus sp. Filipjev 1936	Cyprus Greece Italy Spain^a	[179] [103] [36] [27]
		Hoplolaiminae Filipjev 1934	Spain	[42]
	Meloidogynidae	Meloidogyne acrita Chitwood 1949	China	[89]
		M. arenaria Neal 1889	Chile China Spain^a	[39] [89] [27]
		M. baetica Castillo et al. 2003	Spain^b	[90]
		M. hapla Chitwood 1949	Chile Israel Portugal	[39] [88] [96]
		M. incognita Kofoid and White 1919	Argentina Brazil Chile China Egypt India Israel Italy Jordan Lebanon Lybia Portugal Spain^a	[68] [181] [39] [89] [45] [183] [88] [184] [185] [186] [41] [187] [27]
		M. javanica Treub 1885	Argentina Chile China Egypt Greece Iran^a Israel Italy Jordan Lybia Pakistan Portugal Spain^a	[51] [39] [89] [60] [103] [48] [87] [184] [94] [41] [68] [68] [27]
		M. lusitanica Abrantes and Santos 1991	Portugal Spain^a	[43] [27]
		Meloidogyne sp. Goeldi 1887	Chile Cyprus Iran Israel Italy Jordan Portugal Syria USA	[120] [179] [47] [87] [59] [171] [188] [52] [35]
	Paratylenchidae	Gracilacus peratica Raski 1962	Italy Portugal Spain	[36] [146] [68]
		G. teres Raski 1976	Spain	[147]
		Gracilacus sp. Raski 1962	Italy Spain	[37] [42]
		Paratylenchus arculatus Luc and de Guiran 1962	Spain^a Turkey	[27] [49]
		P. baldacii Raski1975	Spain	[42]
		P. ciccaronei Raski 1975	Spain	[17]
		P. microdorus Andrassy 1959	Spain	[173]
		P. nanus Cobb 1923	Spain	[173]
		P. sheri Raski 1973	Spain	[173]
		P. vandenbrandei De Grisse 1962	Italy	[95]
		Paratylenchus sp. Filipjev 1936	Italy Jordan Syria	[36] [171] [52]
	Pratylenchidae	Pratylenchoides erzurumensis Yuksel 1977	Turkey	[49]
		P. ritteri Sher 1970	Spain^a Iran	[27] [190]
		Pratylenchoides sp. Winslow 1958	Jordan	[171]
		Pratylenchus coffeae Zimmerman 1898	Australia Jordan	[101] [40]
		P. crenatus Loof 1960	Italy	[190]
		P. fallax Seinhorst 1968	Spain^a	[27]
		P. mediterraneus Corbett 1983	Turkey	[49]
		P. musicola Cobb 1919	USA	[102]
		P. neglectus Rensch 1924	Greece Italy Iran Jordan Spain Spain^a	[103] [95] [189] [40] [173] [27]
		P. penetrans Cobb 1917	Australia Italy Jordan Spain Turkey	[191] [95] [40] [42] [68]
		P. thornei Sher and Allen 1953	Iran^a Jordan Spain^a	[48] [94] [27]
		P. vulnus Allen and Johnson 1951	Algeria Australia Italy Spain^a USA	[104] [191] [58] [27] [102]
		P. zeae Graham 1951	Turkey	[49]
		Pratylenchus sp. Thorne 1949	Algeria Chile Egypt Greece Iran Italy Jordan Spain Syria	[104] [120] [46] [103] [47] [36] [171] [42] [52]
		Radopholus sp. Thorne 1949	Greece	[103]
		Zygotylenchus guevarai Tobar-Jimenez 1963	Spain Spain^a Turkey	[42] [27] [49]
	Psilenchidae	Psilenchus hilarulus De Man 1921	Iran^a	[48]
		P. iranicus Kheiri 1970	Jordan Spain	[40] [42]
		Psilenchus sp. De Man 1921	Greece Iran	[169] [47]
	Rotylenchulidae	Rotylenchulus macrodoratus Dasgupta et al., 1968	Greece Italy	[133] [131]
		R. macrosoma Dasgupta et al., 1968	Israel Jordan Spain^b Turkey	[134] [40] [62] [49]
		R. reniformis Linford and Oliveira 1940	Egypt Greece	[192] [103]
		Rotylenchulus sp. Linford and Oliveira 1940	Algeria Syria	[104] [52]
	Telotylenchidae	Amplimerlinius amplus Siddiqi 1976	Portugal	[193]
		A. dubius Steiner 1914	Turkey	[49]
		A. macrurus Goodey 1932	Jordan	[94]
		A. paraglobigerus Castillo et al., 1990	Spain^a	[27]
		Amplimerlinius sp. Siddiqi 1976	Spain	[42]
		Bitylenchus goffarti Sturhan 1966	Turkey	[49]
		Merlinius brevidens Allen 1955	Cyprus Greece Iran^a Jordan Spain	[179] [103] [48] [94] [42]
		M. microdorus Geraert 1966	Jordan Spain	[40] [173]
		M. nothus Allen 1955	Jordan	[40]
		Quinisulcius acutus Allen 1955	Turkey	[49]
		Paratrophurus loofi Arias 1970	Spain	[42]
		Scutylenchus lenorus Brown 1956	Turkey	[49]
		Telotylenchus sp. Siddiqi 1960	Greece	[103]
		Trophurus sp.	Italy	[36]
		Tylenchorhynchus aduncus De Guiran 1967	Spain^a	[27]
		T. clarus Allen 1955	Jordan Spain^a	[94] [27]
		T. claytoni Steiner 1937	Cyprus Turkey	[68] [49]
		T. cylindricus Cobb 1913	Turkey	[49]
		T. dubius Buetschli 1873	Greece Spain Spain^a	[103] [42] [27]
		T. goffarti Sturhan 1966	Jordan	[94]
		T. huesingi Paetzold 1958	Spain^a	[27]
		T. mamillatus Tobar-Jimenez 1966	Spain^a	[27]
		T. penniseti Gupta and Uma 1980	Turkey	[49]
		T. striatus Allen 1955	Greece	[103]
		T. tenuis Micoletzky 1922	Jordan	[194]
		T. tritici Golden et al., 1987	Turkey	[49]
		Tylenchorhynchus sp. Cobb 1913	Algeria Chile Egypt Greece Iran Italy Jordan Spain^a Syria	[104] [120] [45] [103] [47] [36] [171] [27] [52]
	Tylenchidae	Aglenchus agricola De Man 1884	Spain	[42]
		Basiria duplexa Hagemeyer and Allen 1952	Spain	[42]
		Basiria sp. Siddiqi 1959	Jordan	[40]
		Boleodorus thylactus Thorne 1941	Iran^a	[48]
		Boleodorus sp. Thorne 1941	Iran Jordan Spain	[47] [40] [42]
		Coslenchus cancellatus Cobb 1925	Spain	[42]
		C. costatus De Man 1921	Greece	[103]
		C. lateralis Andrassy 1982	Spain	[42]
		Coslenchus sp. Siddiqi 1978	Spain	[42]
		Discotylenchus discretus Siddiqi 1980	Jordan	[40]
		Filenchus discretus Siddiqi 1979	Spain	[42]
		F. filiformis Buetschli 1873	Greece	[103]
		F. sandneri Wasilewska 1965	Spain	[17]
		Filenchus sp. Andrássy 1954	Jordan Spain	[40] [17]
		Irantylenchus sp. Kheiri 1972	Iran^a	[48]
		Neopsilenchus magnidens Thorne 1949	Spain	[42]
		Tylenchus arcuatus Siddiqi 1963	Spain	[42]
		T. davainei Bastian 1865	Spain	[17]
		Tylenchus sp. Bastian 1865	Chile Greece Iran Italy Jordan Spain	[120] [103] [47] [36] [94] [17]
	Tylenchulidae	Trophotylenchulus saltensis Hashim 1983	Jordan	[40]
		Tylenchulus semipenetrans Cobb 1913	Australia Chile Egypt Greece Italy USA	[101] [68] [60] [169] [38] [195]
		Tylenchulus sp. Cobb 1913	Chile Italy Syria	[120] [110] [52]

^a In nurseries.

^b On wild olive.

While many species such as Helicotylenchus digonicus, Meloidogyne javanica, M. incognita, Pratylenchus vulnus are able to parasite a wide range of cultivated and wild plants, others, such as H. oleae, H. neopaxilli, M. baetica, M. lusitanica, Rotylenchulus macrosoma, are specific to olive tree [28].

Considering the species richness encountered in each genus, the genera Xiphinema, Tylenchorhynchus, Pratylenchus, Helicotylenchus, Longidorus, Meloidogyne and Paratylenchus are the most diversified with 16, 13, 12, 10, 9, and 8 species respectively, while 41.4% of the genera are monospecific (Fig. 3).

Fig. 3
Species diversity in each plant-parasitic nematode genus.

2.3 Distribution of plant-parasitic nematodes

Plant-parasitic nematodes were encountered in most of the olive-producing countries. But 81% of the genera were scattered in less than 25% of the countries (Fig. 4). Twenty-one genera were detected in only one country. The dominant genera (Criconemoides, Helicotylenchus, Longidorus, Meloidogyne, Pratylenchus, Rotylenchulus, Rotylenchus, Tylenchorhynchus, Tylenchulus, Tylenchus, and Xiphinema) are each present in at least six countries (Fig. 5), especially around the Mediterranean Basin. Root-knot nematodes Meloidogyne spp. are distributed in 19 countries. That could explain the economic importance of this group that can represent a real threat for olive.

Fig. 4
Frequency of the plant-parasitic nematode genera detected (% of countries).

Fig. 5
World and Mediterranean distribution of the most frequent plant-parasitic nematode genera associated with olive tree (i.e. present in more than 25% of countries).

Modelling the number of genera recorded in each country (Fig. 6A), the highest diversities were recorded in Spain (38 genera), in Jordan (28), in Italy (24), in Greece (20), and in Turkey (16). Ten to twelve genera were detected in Chile, Egypt, Iran, Portugal, and Syria. Only one to five genera were recorded in the other countries. However, these data can in no way reflect the true diversity of the PPN associated with olive trees in each country. Indeed, modelling the research effort by the number of publications as an indicator (Fig. 6B), the diversity found in each country is close to this indicator. Moreover, considering the Mediterranean Basin only, PPN diversity is totally unknown in France, in Morocco, in Adriatic countries, and in most of the Mediterranean islands.

Fig. 6
Genus richness of plant-parasitic nematode recorded in each Mediterranean country (A) and associated publications (B).

The most common nematode genera detected in Jordan were [40]: Filenchus, Helicotylenchus, Merlinius, Pratylenchus, and Xiphinema. A more recent study conducted in Iran revealed other frequent genera, such as Aphelenchus, Boleodorus, Meloidogyne, Psilenchus, Tylenchus, and Tylenchorhynchus [47].

The spatial distribution of PPN species in different fields sampled in Spain is homogeneous [42]. However, this author noticed seasonal fluctuations according to local climate. High-level PPN populations were observed in autumn, low levels in summer and intermediate levels in winter and spring. He hypothesized that microclimatic soil variations could modify root tissue plasticity, which consequently could change the aptitude of nematodes to penetrate roots [70].

Nematode occurrence usually differs in nurseries: the most common species detected in southern Spain are M. incognita, M. javanica, M. arenaria, Mesocriconema xenoplax, Pratylenchus penetrans, and P. vulnus [27]. In contrast, the most common nematodes detected in nurseries in northern Iran are [48]: Aphelenchus avenae, M. javanica, Irantylenchus sp. (a new genus reported for the first time as associated with olive), Pratylenchus thornei, Helicotylenchus pseudorobustus, Boleodorus thylactus, Psilenchus hilarulus, and Merlinius brevidens. But in nurseries, the occurrence of PPN is directly related to the origin of the cutting substrates that are often not sterilized, and to the susceptibility of olive cultivars (e.g., P. vulnus is more frequent on cv. Manzanilla than on other cultivars [27]).

2.4 Impacts of plant-parasitic nematodes on olive trees

Host–parasite interactions between PPN and olive trees have been scarcely studied. However, controlled experiments showed that root-knot nematodes Meloidogyne (e.g., M. arenaria, M. incognita, and M. javanica) significantly reduce tree growth [55–57,71] and may be responsible for 5 to 10% crop losses [33], while these damages are often difficult to assign to PPN [28]. Indeed, the symptoms due to PPN parasitism are not clear, because

• the hardiness of this plant is able to hide them;
• population levels are usually low in the rhizosphere [68]. In any case, this is commonly observed in traditional olive cropping systems.

Three species of fruit crop infecting nematodes that could damage olive (Longidorus diadecturus, Xiphinema americanum, X. californicum) are absent in Europe [68]. These species have been declared as quarantine pests in Europe (EPPO/OEPP). Heterodera mediterranea and X. italiae are also quarantine pests in Chile.

The nematode parasitism impacts directly the plant growth and yield. Basically, root functions are disturbed by histological alterations of root tissues. Physiological disorders limit water and mineral absorption, leading to major deficits [66]. These phenomena are less prominent on wild olive trees that seems more tolerant to PPN infection [28].

The impact of nematodes is much more significant in nurseries where irrigation conditions favour the development of roots and therefore PPN multiplication [27,28,68]. Humidification of the substrates moderates the temperature, two factors that support the development of nematodes [72]. Moreover, roots of olive seedlings are more susceptible to PPN than older plants [27]. Thus, infestation levels with Meloidogyne arenaria, M. incognita, M. javanica, Mesocriconema xenoplax, Pratylenchus penetrans and P. vulnus are significantly higher in nurseries than in orchards [27,48]. But although the same genera are known for their harmfulness on other fruit trees such as apple and pear, the damaging threshold of PPN is poorly evaluated on olive [55,58,73].

Indirect root damages are also related to nematode infection, whose penetration opens pathways to other soil-borne pathogens (bacteria, fungi) [67,74]. The best example is the association of PPN, such as M. incognita and P. vulnus, with the fungal pathogen Verticillium dahliae (Verticillium wilt). The presence of nematodes enhances the symptoms induced by the fungus [75–77]. Experiments have demonstrated a positive correlation between the number of root galls induced by M. incognita and the extent of root rots and vascular discoloration, and the M. incognita/V. dahliae combination reduced rhyzogenesis [76]. When the three parasites M. incognita/P. vulnus/V. dahliae were associated, the reproduction of each of two nematode species was affected by the presence of the other species and/or by the fungus.

Similarly, damages induced by Heterodera mediterranea could be intensified by the presence of V. dahliae [64]. The M. javanica/Fusarium sp. complex would also be responsible for the “Seca” disease that induces drying of young olive trees in nurseries [51].

Virus transmission by some PPN species is also a major risk to the olive tree. Thus, the olive tree is a natural host to Nepoviruses such as the “Arabis Mosaic Nepovirus” (ArMV), the “Strawberry Latent Ringspot Sadwavirus” (SLRSV) and the “Cherry Leaf Roll Virus” (CLRV) transmitted by Xiphinema diversicaudatum and X. vuittenezi [78,79]. These viruses do not produce symptoms on olive [80], except SLRSV that is responsible for leaf and fruit distortion on the variety Ascolana tenera [81].

Biochemical reactions in olive tree roots are diverse, depending on the nematode species that induce specific physiological mechanisms, as for lesion nematodes as P. vulnus [58,82], for root-knot nematodes as M. javanica [55,56], or for dagger nematodes as Xiphinema index [83]. The secondary metabolism would be involved in plant reactions, which would confer resistance (i.e. lower infestation and reproduction) on some varieties [84].

3 The dominant plant-parasitic nematodes associated with olive trees

3.1 Meloidogyne spp. (root-knot nematodes)

Root-knot nematodes (RKN) are sedentary endoparasites. Ninety-seven species have been described [85]. They have developed reproduction and parasitism strategies that allow them to infect thousands of plant species. Most RKN species induce galls that can invade the whole root system. They are widespread all over the world [66,74,86].

These nematodes have been firstly reported on olive trees in the United States [35]. Thereafter, several Meloidogyne species were detected: M. javanica [87], M. incognita, and M. hapla [88], M. arenaria [89], M. lusitanica [43], and M. baetica [90] recently. These nematodes occur on wild and cultivated olive and also in nurseries (except for M. baetica [27] (Table 1). Among these species, M. baetica was detected on wild olive in southern Spain, and could infect olive orchards. Experiments have shown that this species does not reproduce on tomato (on which it induces small galls without any egg mass) or on legumes. That would confirm its specificity to olive, which led to call it “Mediterranean olive root-knot nematode” [90]. This species was also detected on Pistacia lentiscus and Aristolochia baetica [91].

RKN are very well adapted to a wide range of temperatures, which explains their worldwide distribution (Table 1 and Fig. 7). However, M. incognita and M. javanica are the most widespread species in the world [53,92] especially in the Mediterranean Basin [93].

Fig. 7
World and Mediterranean distribution of root-knot nematode species (Meloidogyne spp.) associated with olive tree.

But RKN are at least the less frequent species in olive orchards: they were detected in less than 4% of the samples in Jordan, mainly in irrigated areas and nurseries [40,94], in 2% of the samples in southern Italy (the main production area of the country) and in less than 1% in the other producing areas of the country [95]. That supports other observations made elsewhere in the world [54,55,60,92].

In spite of their scarce distribution, RKN are considered as major pests on olive [53]. Thus, M. javanica is the main cause of “Seca” syndrome in new olive orchards in Argentina [51]. This species is responsible for olive decay in nurseries [40]. RKN reduce plant growth [27,43,55,56]. Pathogenicity tests showed that M. arenaria, M. incognita and M. javanica grow as well on rootstocks [56,57] and on plants cv. Picual and cv. Arbequina, which are widely distributed in the Mediterranean Basin [71]. Controlled experiments showed that six months after inoculation with 5000 or 10,000 M. javanica juveniles per plant, plant growth was significantly reduced: 28% [60] and 45–52%, according to the cultivar [55], respectively. The stem diameter is the most sensitive parameter to infestation [57,71]. Olive trees infected by Meloidogyne spp. show yellowing of the highest branches, and then defoliation [68]. These symptoms are observed everywhere, as well as in China [89], Portugal [96], and Chile [39].

Histological observations of roots infected with M. incognita [97], with M. baetica [90,91], or with M. javanica and M. lusitanica [92] indicate different sizes and different localisations of the galls they induce. M. javanica galls are usually located on the root tip, but some galls are also distributed along roots. Clusters of several galls were also observed and no secondary roots seen near them [92]. M. lusitanica galls are usually distributed as individual galls along roots. M. baetica induces small galls, frequently located along the taproot and very rarely on secondary roots, without the development of egg masses [90].

3.2 Pratylenchus spp. (lesion nematodes)

Lesion nematodes (LN) are migratory endoparasites. They are worldwide distributed, and are able to infect a wide range of plants. They are involved with other soil-borne pathogens (e.g., fungi) in parasitic complexes. LN are the most damaging nematodes with RKN [98–100].

Several Pratylenchus species have been detected on olive (Table 1 and Fig. 5): P. coffeae [101], P. crenatus [95], P. mediterraneus and P. musicola and P. vulnus [102], P. neglectus [103], P. penetrans [95], P. thornei [104] and P. zeae [49]. Some of them (P. neglectus, P. penetrans, P. thornei, P. vulnus and P. fallax) have been also observed in nurseries [27,48].

Among these species, P. vulnus and P. penetrans are considered the most frequent and pathogenic on olive [58,71].

Infection with LN induces large necrotic areas on roots, which may cover all the root system. This may rot the cortical parenchyma [66,102] and reduce both number and size of infected roots [105]. Other symptoms such as leaf chlorosis, internode shortening and defoliation can be observed [106].

Controlled inoculations revealed that most of the LN species do not reproduce on olive, leading one to minimize the impact of these nematodes on this crop [71]. Field observations pointed that LN reproduce primarily in weeds without injuring olive trees [107]. Nevertheless, P. vulnus is the most pathogenic species [58]. It is responsible for tree decline [53,106]. Significant damages attributed to this species have been recorded in several olive orchards in Italy [38,95,106], in the USA [102], and in Algeria [104]. Inoculations with P. vulnus performed on several olive cultivars (Arbequina, Ascolana, Manzanilla, Picual) confirmed its strong pathogenic potential [58,71]. Competitions between RKN and LN have been recorded on olive. Reproduction of P. vulnus populations was reduced with root-knot nematode co-infection [76].

3.3 Helicotylenchus spp. (spiral nematodes)

Spiral nematodes (SN) are migratory ectoparasites. They are also widely distributed in the world.

Several Helicotylenchus species were detected in the olive rhizosphere such as H. digonicus [103], H. erythrinae [59], H. dihystera [108], H. minzi [40], H. neopaxili and H. oleae [70], H. pseudorobustus [103], H. tunisiensis [109], and H. vulgaris [40]. Some species, such as H. digonicus, H. pseudorobustus and H. vulgaris were also detected in nurseries [27,48]. These species have been observed in different olive-producing areas in the world (Table 1 and Fig. 5).

H. digonicus is dominant in many olive orchards [17,42]. For example, it occurs in more than 45% of the orchards in Jordan [40]. Nevertheless, H. oleae is widely distributed in Italy [70], where H. digonicus was not detected [42]. Other studies also demonstrate the dominance of other spiral nematodes, as Rotylenchus spp. in Italy [37,110,111].

Pathogenicity processes caused by SN are still unclear [53]. However, some few studies indicate that H. dihystera, H. erythrinae or H. oleae induces brown lesions on roots and chlorosis of leaf tips, leading to root-mass and plant-growth reduction [59,60,66,70]. Growth delay was observed on plants infected by H. digonicus [93]. A 78% plant-growth reduction was measured on plants inoculated with 1000 H. dihystera six months before [60]. Some species (e.g., H. digonicus and H. oleae) have a semi-endoparasitic behaviour (i.e. introduction of the anterior body part into roots) [40,70]. H. oleae penetrates up to the root epidermis and to the cortical parenchyma. It induces cell wall necroses, feed from place to place, leaving cavities in the cortex.

3.4 Xiphinema spp. (dagger nematodes)

Dagger nematodes (DN) are ectoparasites, frequently found in the olive rhizosphere [66]. Different species have been recorded (Table 1 and Fig. 5): Xiphinema aequum [112], X. barense [113], X. californicum (X. americanum) [114], X. diversicaudatum [115], X. elongatum [60], X. index [40], X. ingens [116], X. italiae [78], X. lusitanicum [79], X. macroacanthum [117], X. nuragicum [17] and X. pachtaicum [94], X. sahelense and X. vuittenezi [118], and X. turcicum [42]. Despite the low population densities, X. pachtaicum is the most common DN species on olive [40,94].

X. diversicaudatum and X. pachtaicum show different distribution areas [115]. X. diversicaudatum could be considered as an Atlantic species, distributed in both cultivated and uncultivated habitats, but is more abundant in uncultivated ones with weak environmental stresses. X. pachtaicum is rather a Mediterranean species, associated also with other fruit trees (apple and peach). This would explain why X. diversicaudatum has been reported on olive in central and northern Spain [115], but not in the South [119].

These nematodes are considered as major pathogens on olive trees in Chile [120]. In the USA, they are responsible for 5 to 10% of the damages, which corresponds to an estimated $ 38.9 million loss [33]. X. pachtaicum could be a real nuisance in olive orchards [42]. DNs affect plant growth initiated by root necrosis [60,121].

A 65% plant-growth reduction was observed on plants inoculated with 500 X. elongatum six months before [60]. However, significant development of X. californicum populations did not affect plant growth [114]. In fact, DNs are usually difficult to rear in controlled conditions because of their susceptibility to moisture and temperature variations [122]. That could explain failures in pathogenicity experiments [53].

3.5 Tylenchulus spp. (citrus nematodes)

Usually known as citrus parasites, T. semipenetrans was reported on olive in California, Chile and Italy [123] (Table 1 and Fig. 5). Studying several life history traits associated with infection and reproduction on specific host plants, six biotypes were identified: four in California [124], one in Florida [125], and one in Italy [126]. This diversity was revised and reduced to four biotypes [127]:

• the “Poncirus biotype” that reproduces on Poncirus trifoliate and grapevine but not on olive (= California biotype C3);
• the “Citrus biotype” that reproduces on Citrus spp., grapevine and olive (= California biotype C1)—both previous C2 and C4 California biotypes were included in this biotype group, since they cannot reproduce on P. trifoliate; but they were detected on olives in Italy;
• the “Mediterranean biotype” is very close to the “Citrus biotype” for its host range except olive—this biotype has been found in all olive-producing Mediterranean countries, in South Africa and possibly in India;
• the “Grass biotype” was reported in Florida only, where it reproduces only on Andropogon rhizomatus, but this biotype corresponds to the new species T. graminis that only parasites monocots [128].

The limits of these biotypes are rather unclear. C1 and C2 reproduce on grapevine and olive, whereas C3 affects grapevine but not olive, and C4 reproduces only on olive [124]. Furthermore, C1 does not reproduce on P. trifoliate and olive [126], while other studies showed that it is the only biotype able to reproduce on olive [127]. Moreover, T. semipenetrans was found in olive roots in northern Italy where citrus is not cultivated [127]. C1 has not been reported in Spain [129] either in orchards or in nurseries [27].

Histological disturbances induced by these nematodes in olive roots are similar to those observed on citrus [127]. However, life history traits vary from one variety to another. C1 is more aggressive and reproduces faster on cvs. Manzanilla and Ascolana than on other cultivars, and much more than on Citrus sinensis, delaying plant growth [130]. Similarly, C1 populations significantly reduced cv. Frangivento root growth, even no reproduction was observed one year after infection [126].

3.6 Rotylenchulus spp. (reniform nematodes)

Reniform nematodes (RN) are semi-endoparasites that infect herbaceous and woody plants, especially in tropical and subtropical regions. Three RN species were detected on olive (Table 1 and Fig. 5): R. macrodoratus [131], R. macrosoma [62,132] and R. reniformis [103,133]. These species were registered in Algeria [104], Greece [103], Israel [134], and Italy [95,131,135], but their pathogenicity on olive remains poorly documented [53].

Non-mature females penetrate the roots and remain in the epidermis on feeding sites [61,136,137]. Mature female produce a gelatinous matrix, and lays eggs within it [62].

Distribution of R. macrodoratus is restricted to Mediterranean countries, especially to France, Greece, Italy, and Malta. It is the most common RN species in Italy, where it has been detected in about 20% of the samples in the South and 22% somewhere else [38,95].

R. macrosoma is more abundant on wild olive in southern Spain [62], but it has not been detected in nurseries in the same region [27]. It is able to reproduce on common olive cultivars (Picual, Arbequina). Potential damages may occur in irrigated sandy soils for 0.5–1 nematode/cm³ population levels, but infected plants show no symptoms [62].

Feeder cell disturbances are different according to RN species: R. macrodoratus and R. reniformis induce extended mononucleated cells [131], whereas R. macrosoma induces syncytia [62]. High infection with R. reniformis leads to weak tree growth [103].

3.7 Heterodera spp. (cyst nematodes)

Cyst nematodes (CN) are sedentary endoparasites. Females lay eggs inside them which remain as a persistence structure, and/or in a yellow gelatinous matrix. When they die, their cuticle hardens, forming a cyst that may persist in the soil for several years in the absence of host plant [66], and hatch when soil conditions are favourable. CN are widespread and economically important nematodes. Very few species infect woody plants [138]. They were not recorded as olive parasites until H. mediterranea was described on cultivated olive (cv Manzanilla) in Spain [64]. More recently, H. avenae was detected in olive nurseries on grasses associated with substrates [27].

H. mediterranea differs from other CN species by its semi-endoparasitic behaviour which would be explained by the woody structure of olive roots [64]. Identical observations have been reported on pistachio tree [63].

Infected olive trees do not exhibit any symptoms on leaves, even in heavily infested soils. However, necrosis and root distortion were observed near root penetration sites [64], suggesting that H. mediterranea could contribute to plant decline in young orchards and nurseries [64,66,139], where high densities occur [66].

3.8 Other plant-parasitic nematodes

Trichodoridae nematodes are also frequently detected on olive trees. They are polyphagous root ectoparasites and are distributed worldwide. They cause damage to a wide range of crops and natural vegetation by direct feeding on roots, causing stunted roots. Some species (13%) are known as Tobraviruses vectors, resulting in important yield losses [140]. Three species of Paratrichodorus and 10 species of Trichodorus were recorded on olive trees, especially in Italy [141,142], Portugal [143], and Spain [27,42,140] (Table 1).

Nematodes belonging to the Telotylenchidae family are not major crop parasites, although they are mostly associated with several crops. The genus Tylenchorhynchus seems to be the most diverse, with 13 species recorded in different olive-producing areas, mainly in the Mediterranean Basin (Table 1 and Fig. 5).

Gracilacus peratica (family Paratylenchidae) is an ectoparasite detected on olives in Italy [36,95,144,145], Spain [42], and Portugal [146] (Table 1). Juveniles, young females and males were detected only in soil, while mature females were observed in roots. Cell walls become thick and lignified [145]. Pathogenicity processes on olive are not known [53]. G. teres was also detected on olive in Spain [147].

Ogma spp. nematodes are sedentary ectoparasites. O. rhombosquamatum has been reported in different orchards in Spain [42], Italy [38,148], Jordan [40], and Portugal [146] (Table 1). Nematode infection induces cortical cell wall thickening and cortex and epidermis necrosis.

4 Management of plant-parasitic nematodes on olive

4.1 Exclusion of PPN infection

Given that PPN are parasites living in the soil and/or in roots, olive tree protection relies first on the use of healthy plant material transplanted in a soil free of these parasites. That is why the first step in avoiding PPN on olive starts in nurseries where the best conditions for PPN multiplication are met, and from where they could be widely disseminated in orchards [53]. In that way, most infestations by RKN and LN nematodes in olive orchards originate from unsanitized plant material produced in uncertified nurseries [149]. Chemical disinfection of substrates is a suitable approach for production of nematode-free nursery stock [68]. Although laws have been established by the European Union for healthy olive seedlings certification [150], their application is unfortunately still limited [68]. Cultural practices such as fertilization, weed control with herbicides, could lead to increased populations of NPP [17]. On the other hand, intensive production systems (high-yield varieties, high-density plantations, permanent grassing, irrigation, fertilization, etc.) induce environments suitable for the development of soil-borne diseases caused directly or indirectly (e.g., verticillium wilt) by PPN [68]. These cropping systems could lead to PPN communities dominated by the most damaging species to olive tree.

4.2 Plant resistance

The use of resistant cultivars is an effective alternative to chemical control of PPN [151], but their productivity in olive fruits and oil can be a limiting factor to use them [53]. Some cultivars are resistant or tolerant to some species of Meloidogyne, Pratylenchus, and Tylenchulus.

Olive varieties can be distinguished as susceptible (nematode reproduction and plant disturbance), tolerant (nematode reproduction without plant disturbance) and resistant (no nematode reproduction) to RKN. Cvs. Manzanillo and Ascolano are very susceptible to M. javanica [54]. But they are resistant to M. arenaria and M. hapla [55]. In nurseries, Arbequina, Cornicabra, Hojiblanca, Manzanilla and Picual are the most susceptible cultivars to M. arenaria, M. incognita, and M. javanica [27].

Olive cultivars show also various reactions towards P. vulnus. This species does not reproduce on cv. Verdalion [82] while cvs. Ascolana and Manzanilla are very susceptible [55]. However, cv. Ascolana is more tolerant than cv. Manzanilla [53]. The host–parasite interaction would also depend on the diversity of both P. vulnus geographical strains and host plants on which they were detected [152].

Several olive cultivars are susceptible to X. index except cvs. FS17 and DA12I that exhibited resistance [121].

Comparing CN reproduction traits, such as soil (juveniles and cysts) and root (juveniles) infestation levels and reproduction rates on different olive cultivars, cv. Arbequina appeared as the most susceptible cultivar to H. mediterranea [68].

These resistant varieties can be also used as stocks for susceptible cultivars that have yield interests.

In that way, resistance screenings were developed, and in vitro tests have proved to be valid alternatives to traditional resistance screenings trials [151].

4.3 Soil solarisation

This method was successfully used to control soil-borne parasites: fungi [153,154], bacteria [155], and PPN [156]. It can be an efficient method especially in the Mediterranean Basin, where climatic conditions are optimal with high summer temperatures. In nurseries, soil solarisation can therefore be used for controlling RKN in substrates [157], affecting 95% of M. incognita eggs up to a 40-cm depth after a 10-day application. However, the gelatinous egg mass matrix protects them against several environmental stresses. Then, Meloidogyne spp. is sometimes heat-tolerant and difficult to control by soil solarisation [158]. This method may also be useful to control other PPN, e.g., P. vulnus and P. penetrans, and other soil-borne pathogens as Verticillium dahliae [157].

4.4 Biological control

4.4.1 Organic residues

The addition of forest residues provides organic matter that could contribute to PPN suppression, by increasing soil microflora [159]. Composted dry cork, especially in nurseries, may be effective for M. incognita suppression, due to the toxicity of released products (e.g., ammonia, phenolic compounds) [160].

4.4.2 Biofumigation

Some plants (e.g., Brassica oleracea, B. nigera, B. juncea, Raphanus sativum, Crambe abyssinica, Sorghum spp.) are able to release volatile biocides after ploughing in soil that could have toxic effects on PPN. Such soil biofumigations are ecological alternatives to chemical fumigation against PPN and other soil-borne pathogens [161]. Trials to assess the effect of Sorghum sudanense on the suppression of M. incognita showed a significant reduction in final nematode populations 30 to 60 days after treatment [68]. Brassicaceae species showed suppressive effects on M. incognita parasitizing tomato plants by reducing root galls and nematode reproduction [162]. The association of these plants with olive trees could be a way to reduce PPN populations.

4.4.3 Microbial control

Soil inoculation with mycorrhizal fungi can be a useful practice to reduce RKN populations. An early inoculation of olive stocks cvs. Arbequina and Picual with Glomus intraradices, G. mosseae and G. viscosum enhanced plant-growth and controlled M. incognita race 1 and M. javanica populations by inhibiting nematode reproduction and reducing root galling [163]. Other microbial antagonists to PPN (such as nematophagous fungi and Pasteuria penetrans) can be also used for nematode suppression.

5 Prospects: better knowledge on PPN biodiversity for better management

This review clearly shows that the diversity of the PPN communities strongly differ across countries. Considering olive protection, PPN control strategies appear to be developed in each Mediterranean producing country according to its own ecological and agronomical constraints, and the PPN diversity encountered.

As seen above, most of the researches emphasized studies targeting some PPN species. Because resistance and biocontrol are specific to emblematic species and because PPN are everywhere found in communities (i.e. species mixtures), these control strategies may induce changes in nematode communities, but do not necessarily decrease their overall pathogenicity. Consequently, such biological strategies may be unsustainable from an ecological point of view [164], and they must focus on community rearrangements instead of reducing the most pathogenic species.

Considering olive tree history and diversity of associated PPN around the Mediterranean Basin, local PPN communities could be originating from historical mixtures set up with native (before olive introduction) and invasive (with rootstocks from oleasters) communities. Olive domestication in the past, and breeding and cropping now could explain the present distribution of PPN. Consequently, management strategies must take into account the spatial distribution of the PPN diversity all around the Mediterranean Basin (regional scale) and in each olive-producing country (local scale). A special focus on PPN communities associated with wild olive would give information about trade-offs between PPN communities and olive trees in non-disturbed situations. Moreover, investigation about co-adaptation between PPN and olive tree (wild and varieties) would provide new insights into assembling mechanisms between PPN and olive trees. In this way, a large survey with high sampling efforts is initiated [165] in order to evaluate as precisely as possible the diversity of PPN communities parasitizing wild and cultivated olive, and to target the historical (evolution) and environmental (cropping systems, olive varieties, soil factors) filters involved in community patterns. As a confirmation, interesting effects of olive genotypes on PPN community patterns were observed [17]. Such observations could lead to the development of new management strategies in a diversity-conservation approach.

Acknowledgements

This work was part of the PESTOLIVE project: Contribution of olive history for the management of soil-borne parasites in the Mediterranean Basin (KBBE 219262), funded by the ARIMNet action (www.arimnet.net) [166] supported by EU and non-EU Mediterranean countries. The authors thank Dr. G. Besnard (CNRS, Université Paul-Sabatier, Toulouse, France) for his critical reading of this manuscript.

Bibliographie

[1] F. Medail; P. Quezel; G. Besnard; B. Khadari Systematics, ecology and phylogeographic significance of Olea europaea L. ssp. maroccana (Greuter and Burdet) P. Vargas et al., a relictual olive tree in south west Morocco, Bot. J. Linn. Soc., Volume 137 (2001), pp. 249-266

[2] P. Green A revision of Olea L. (Oleaceae), Kew Bull., Volume 57 (2002), pp. 91-140

[3] D. Zohary; P. Spiegel-Roy Beginnings of fruit growing in the Old World, Science, Volume 187 (1975), pp. 319-327

[4] N. Liphschitz; R. Gophna; M. Hartman; G. Biger The beginning of olive (Olea europaea) cultivation in the old world: a reassessment, J. Archaeol. Sci., Volume 18 (1991), pp. 441-453

[5] D. Kaniewski; E. Van Campo; T. Boiy; J.F. Terral; B. Khadari; G. Besnard Primary domestication and early uses of the emblematic olive tree: palaeobotanical, historical and molecular evidence from the Middle East, Biol. Rev., Volume 87 (2012), pp. 885-899

[6] G. Besnard; B. Khadari; M. Navascués; M. Fernández-Mazuecos; A. El Bakkali; N. Arrigo; D. Baali-Cherif; V.B.-B. de Caraffa; S. Santoni; P. Vargas The complex history of the olive tree: from Late Quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant, Proc. R. Soc. B, Volume 280 (2013) no. 1756, p. 20122833

[7] G. Besnard; A. Bervillé Multiple origins for Mediterranean olive (Olea europaea L. ssp. europaea) based upon mitochondrial DNA polymorphisms, C. R. Acad. Sci. Paris, Ser. III, Volume 323 (2000), pp. 173-181

[8] A. Belaj; I. Trujillo; R. De la Rosa; L. Rallo; M. Gimenez Polymorphism and discrimination capacity of randomly amplified polymorphic markers in an olive germplasm bank, J. Am. Soc. Hortic. Sci., Volume 126 (2001), pp. 64-71

[9] C. Breton; J.-F. Terral; C. Pinatel; F. Médail; F. Bonhomme; A. Bervillé The origins of the domestication of the olive tree, C. R. Biologies, Volume 332 (2009), pp. 1059-1064

[10] G. Besnard; J. Dupuy; M. Larter; P. Cuneo; D. Cooke; L. Chikhi History of the invasive African olive tree in Australia and Hawaii: evidence for sequential bottlenecks and hybridization with the Mediterranean olive, Evol. Appl. (2013), pp. 195-211

[11] C. Breton; F. Médail; C. Pinatel; A. Bervillé De l’olivier à l’oléastre: origine et domestication de l’Olea europaea L. dans le Bassin méditerranéen, Cah. Agric., Volume 15 (2006), pp. 329-336

[12] G. Besnard; P. Baradat; C. Breton; B. Khadari; A. Bervillé Olive domestication from structure of oleasters and cultivars using nuclear RAPDs and mitochondrial RFLPs, Genet. Sel. Evol., Volume 33 (2001), pp. 251-268

[13] R. Lumaret; N. Ouazzani; H. Michaud; G. Vivier; M. Deguilloux; F. Di Giusto Allozyme variation of oleaster populations (wild olive tree) (Olea europaea L.) in the Mediterranean Basin, Heredity, Volume 92 (2004), pp. 343-351

[14] G. Besnard; B. Khadari; P. Baradat; A. Bervillé Combination of chloroplast and mitochondrial DNA polymorphisms to study cytoplasm genetic differentiation in the olive complex (Olea europaea L.), Theor. Appl. Genet., Volume 105 (2002), pp. 139-144

[15] D. Zohary; M. Hoph Domestication of plants in the Old World, Clarendon Press, Oxford, 2000 (316 p.)

[16] L. Sebastiani; A. Minnocci; F. Scebba; C. Vitagliano; A. Panicucci; G. Lorenzini Physiological and biochemical reactions of olive genotypes during site-relevant ozone exposure IV, Int. Symp. Olive Grow., Volume 586 (2002), pp. 445-448

[17] J.E. Palomares-Rius; P. Castillo; M. Montes-Borrego; H. Müller; B.B. Landa Nematode community populations in the rhizosphere of cultivated olive differs according to the plant genotype, Soil Biol. Biochem., Volume 45 (2012), pp. 168-171

[18] G. Bartolini; G. Prevost; C. Messeri; G. Carignani Olive germplasm: cultivars and worldwide collections, 1998

[19] N. Moutier; C. Pinatel; A. Martre; J.-P. Roger; B. Khadari; J.-F. Burgevin; D. Ollivier; J. Artaud, Identification des variétés d’oliviers cultivées en France, tome1, Naturalia Publications, 2004 (246 p.)

[20] N. Moutier; B. Khadari; L. Berti; J. Maury; C. Gambotti; J. Giannettini; J. Panighi; V. Bronzini de Caraffa; V. Lorenzi; C. Palmieri; C. Breton; G. Besnard; A. Bervillé L’olivier : les ressources génétiques, INRA Mensuel les Dossiers, Volume 128 (2006), pp. 14-21

[21] N. Moutier; C. Pinatel; A. Martre; J.-P. Roger; B. Khadari; J.-F. Burgevin; D. Ollivier; J. Artaud, Identification et caractérisation des variétés d’oliviers, tome2, Naturalia Publications, 2011 (248 p.)

[22] P. Hatzopoulos; G. Banilas; K. Giannoulia; F. Gazis; N. Nikoloudakis; D. Milioni; K. Haralampidis Breeding, molecular markers and molecular biology of the olive tree, Eur. J. Lipid Sci. Technol., Volume 104 (2002), pp. 574-586

[23] G. Besnard; P. Baradat; D. Chevalier; A. Tagmount; A. Bervillé Genetic differentiation in the olive complex (Olea europaea) revealed by RAPDs and RFLPs in the rRNA genes, Genet. Resour. Crop Evol., Volume 48 (2001), pp. 165-182

[24] C.A. Owen; E.C. Bita; G. Banilas; S.E. Hajjar; V. Sellianakis; U. Aksoy; S. Hepaksoy; R. Chamoun; S.N. Talhook; I. Metzidakis AFLP reveals structural details of genetic diversity within cultivated olive germplasm from the Eastern Mediterranean, Theor. Appl. Genet., Volume 110 (2005), pp. 1169-1176

[25] N.C. Ellstrand Dangerous liaisons?: when cultivated plants mate with their wild relatives, JHU Press, 2003

[26] IOC, Olive nursery production and plant production techniques (www.internationaloliveoil.org/projects/paginas/Section-a.htm), Madrid, Spain. (1991, 2000).

[27] A.I. Nico; H.F. Rapoport; R.M. Jiménez-Díaz; P. Castillo Incidence and population density of plant-parasitic nematodes associated with olive planting stocks at nurseries in southern Spain, Plant Dis., Volume 86 (2002), pp. 1075-1079

[28] F.E. El-Borai; L.W. Duncan; M. Luc; R. Sikora; J. Bridge (2005), pp. 467-492

[29] Food, Agriculture Organization of the United Nations Statistical Database (FAOSTAT), FAOSTAT, Production statistics of crops, Online database, 2010 http://www.faostat.fao.org/

[30] W. Decraemer; D.J. Hunt; R. Perry; M. Moens Structure and classification, Plant Nematol. (2006), pp. 3-32

[31] C. Djian-Caporalino; H. Védie; A. Arrufat Gestion des nématodes à galles : lutte conventionnelle et luttes alternatives, L’atout des plantes pièges, Phytoma, Volume 624 (2009), pp. 21-25

[32] J. Sasser; D. Freckman (1987), pp. 7-14

[33] S. Koenning; C. Overstreet; J. Noling; P. Donald; J. Becker; B. Fortnum Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994, J. Nematol., Volume 31 (1999), pp. 587-618

[34] J.C. Cayrol; C. Djian-Caporalino; E. Panchaud-Mattei, La lutte biologique contre les nématodes phytoparasites, 17, Courrier de la cellule environnement de l’INRA (1992), pp. 31-44

[35] E.M. Buhrer; C. Cooper; G. Steiner A list of plants attacked by the root-knot nematode (Heterodera marioni), Plant Dis. Rep., Volume 17 (1933), pp. 64-96

[36] A. Scognamiglio; M. Talame; N. Giandomenico Indagine sui nematodi viventi nella rizosfera dell’olivo (1 contributo), Boll. Lab. Ent. agr., Volume 26 (1968), pp. 205-226

[37] A. Scognamiglio; M. Talame; F.P. D’Errico Indagine sui nematodi viventi nella rizosfera dell’olivo (2 contributo), Boll. Lab. Ent. agr., Volume 29 (1971), pp. 43-59

[38] R.N. Inserra; N. Vovlas Indagine sulla distribuzione Reproduction of Nematodes on Olive: geografica dei nematodi parassiti dell’olivo in Italia, Informat. fitopat., Volume 1 (1981), pp. 117-119

[39] R.M. Jimenez, Primeras Jornadas Olivícolas Nacionales, 23-27 de Noviembre, 1981, Arica, Chile, Trabajos y resumenes, Universidad de Tarapaca, Departamento de Agricultura (1982), pp. 127-138

[40] Z. Hashim Plant-parasitic nematodes associated with olive in Jordan, Nematologia Mediterranea, Volume 11 (1983), pp. 27-32

[41] E. Edongali Plant-parasitic nematodes associated with olive trees in Libya, Int. Nematol. Netw. Newslett., Volume 6 (1989), pp. 36-37

[42] R. Peña-Santiago Plant-parasitic nematodes associated with olive (Olea europea L.) in the province of Jaén, Spain, Rev. Nematol., Volume 13 (1990), pp. 113-115

[43] I.M. de O. Abrantes; M.S.N. Santos Meloidogyne lusitanica n. sp. (Nematoda: Meloidogynidae), a root-knot nematode parasitizing olive tree (Olea europaea L.), J. Nematol., Volume 23 (1991), pp. 210-224

[44] I. Ibrahim, Volume 7 (1990), pp. 33-38

[45] I. Ibrahim; Z. Handoo; A. El-Sherbiny A survey of phytoparasitic nematodes on cultivated and non-cultivated plants in northwestern Egypt, J. Nematol., Volume 32 (2000), pp. 478-485

[46] I. Ibrahim; A. Mokbel; Z. Handoo Current status of phytoparasitic nematodes and their host plants in Egypt, Nematropica, Volume 40 (2010), pp. 239-262

[47] S.A. Hosseininejad; Z. Tanha Moafy; S.H. Barooty, Volume 65 (1996), pp. 46-53

[48] S. Sanei; S. Okhovvat Incidence of plant-parasitic nematodes associated with olive planting stocks at nurseries in northern Iran, Int. J. Appl., Volume 1 (2011), pp. 79-82

[49] C. Cilbircioğlu Plant-Parasitic Nematodes Associated with Olea europea L. Fauna of Turkey, J. Agric. Urban Entomol., Volume 24 (2007), pp. 227-231

[50] I. Kepenekci Preliminary list of Tylenchida (Nematoda) associated with olive in The Black Sea and The Mediterranean Regions of Turkey, Nematol. Mediterr., Volume 29 (2001), pp. 145-147

[51] B. Pérez; D. Barreto; D. Docampo; M. Otero; M. Costilla; M. Roca; S. Babbitt Current status of the drying syndrome (seca) of olive trees in Argentina, Phytopathology, Volume 91 (2001), p. S71

[52] M. Ayoub; L. Ghaoui Nematode problems on olive from nurseries to orchards, Report diploma, Plant Protection Department, Faculty of Agriculture, University of Tishreen, Lattakia, Syria, 2011 (in Arabic)

[53] Z. Hashim Distribution, pathogenicity and control of nematodes associated with olive, Rev. Nematol., Volume 5 (1982), pp. 169-181

[54] F. Lamberti; B.F. Lownsbery Olive varieties differ in reaction to the root-knot nematode, Meloidogyne javanica, Phytopathol. Mediterr., Volume 7 (1968), pp. 91-106

[55] F. Lamberti; R. Baines Pathogenicity of four species of Meloidogyne on three varieties of olive trees, J. Nematol., Volume 1 (1969), pp. 111-115

[56] N. Sasanelli; T. D’Addabbo; R. Lemos Influence of Meloidogyne javanica on growth of olive cuttings in pots, Nematropica, Volume 32 (2002), pp. 59-63

[57] N. Sasanelli; G. Fontanazza; F. Lamberti; T. D’Addabbo; M. Patumi; G. Vergari Reaction of olive cultivars to Meloidogyne species, Nematol. Mediterr., Volume 25 (1997), pp. 183-190

[58] F. Lamberti; R. Baines Effect of Pratylenchus vulnus on the growth of Ascolano and Manzanillo olive trees in a glasshouse, Plant Dis. Rep., Volume 53 (1969), pp. 557-558

[59] A. Graniti, Olearia, Volume 9 (1955), pp. 114-120

[60] K. Diab; S. El-Eraki Plant-parasitic nematodes associated with olive decline in the United Arab Republic, Plant Dis. Rep., Volume 52 (1968), pp. 150-154

[61] R. Inserra; N. Vovlas The biology of Rotylenchulus macrodoratus, J. Nematol., Volume 12 (1980), pp. 97-102

[62] P. Castillo; N. Vovlas; A. Troccoli The reniform nematode Rotylenchulus macrosoma, infecting olive in southern Spain, Nematology, Volume 5 (2003), pp. 23-29

[63] N. Vovlas; R. Inserra Biology of Heterodera mediterranea, J. Nematol., Volume 15 (1983), pp. 571-576

[64] P. Castillo; N. Vovlas; A.I. Nico; R.M. Jiménez-Díaz Infection of olive trees by Heterodera mediterranea in orchards in southern Spain, Plant Dis., Volume 83 (1999), pp. 710-713

[65] F. Lamberti; N. Vovlas Plant-parasitic nematodes associated with olive1, EPPO Bull., Volume 23 (1993), pp. 481-488

[66] N. Vovlas; P. Castillo; H.F. Rapoport; R.M. Jiménez-Díaz Parasitic nematodes associated with olive in countries bordering the Mediterranean sea, in: IVth International Symposium on Olive Growing, Acta Hort., Volume 586 (2002), pp. 857-860

[67] N. Sasanelli, Springer (2009), pp. 275-315

[68] P. Castillo; A.I. Nico; J.A. Navas-Cortés; B.B. Landa; R.M. Jiménez-Díaz; N. Vovlas Plant-parasitic nematodes attacking olive trees and their management, Plant Dis., Volume 94 (2010), pp. 148-162

[69] T. Bongers The maturity index: an ecological measure of environmental disturbance based on nematode species composition, Oecologia, Volume 83 (1990), pp. 14-19

[70] R. Inserra; N. Vovlas; A.M. Golden Helicotylenchus oleae n. sp. and H. neopaxilli n. sp.(Hoplolaimidae), two new spiral nematodes parasitic on olive trees in Italy, J. Nematol., Volume 11 (1979), p. 56

[71] A. Nico; R. Jiménez-Díaz; P. Castillo Host suitability of the olive cultivars Arbequina and Picual for plant-parasitic nematodes, J. Nematol., Volume 35 (2003), p. 29

[72] S. Koenning; S. Walters; K. Barker Impact of soil texture on the reproductive and damage potentials of Rotylenchulus reniformis and Meloidogyne incognita on cotton, J. Nematol., Volume 28 (1996), p. 527

[73] A. Nyczepir; J. Halbrendt; K. Evans; D. Trudgill; J. Webster (1993), pp. 381-425

[74] G. Karssen; M. Moens; R.N. Perry Root-knot nematodes, Plant Nematol. (2006), pp. 59-90

[75] L. Francl; T. Wheeler, Nematode interactions, Springer (1993), pp. 79-103

[76] F. Lamberti; N. Sasanelli; T. D’Addabbo; A. Ambrico; F. Ciccarese; D. Schiavone Relationship between plant-parasitic nematodes and Verticillium dahliae on olive [Olea europaea L.], Nematol. Mediterr., Volume 29 (2001), pp. 3-9

[77] A. Saeedizadeh; A. Kheiri; M. Okhovat; A. Hoseininejad Study on interaction between root-knot nematode Meloidogyne javanica and wilt fungus Verticillium dahliae on olive seedlings in greenhouse, Commun. Agric. Appl. Biol. Sci., Volume 68 (2003), pp. 139-143

[78] G.P. Martelli; C.E. Taylor, Advances in disease vector research, Springer (1989), pp. 151-189

[79] M. Bravo; F. Roca, Volume 46 (1998), pp. 101-121

[80] C.E. Taylor; D. Brown Nematode vectors of plant viruses, International, London, 1997 (286 p.)

[81] M. Marte; F. Gadani; V. Savino; E. Rugini Strawberry latent ringspot virus associated with a new disease of olive in Central Italy, Plant Dis., Volume 70 (1986), pp. 171-172

[82] B. Lownsbery; E. Serr Fruit and nut tree rootstocks as hosts for a root-lesion nematode, Pratylenchus vulnus, Proc. Am. Soc. Hortic. Sci. (1963), pp. 250-254

[83] M. Ridolfi; M. Patumi; T. D’addabbo; N. Sasanelli; R. Lemos Enzymatic response of olive varieties to parasitism by Xiphinema index (Nematoda: Longidoridae), Russ. J. Nematol., Volume 9 (2001), pp. 25-32

[84] M. Ridolfi; N. Sasanelli; M. Patumi; T. D’Addabbo; G. Fontanazza; F. Lamberti Phenolic and peroxidase metabolism in olive trees attacked by root-knot nematodes (Meloidogyne spp.), Ital. Hort., Volume 5 (1998), pp. 22-26

[85] D.J. Hunt; Z.A. Handoo, Root-knot nematodes, Volume 1 (2009), pp. 55-88

[86] G. De Guiran; C. Netscher Les nématodes du genre Meloidogyne, parasites de cultures tropicales, Cah. ORSTOM., Ser. Biol., Volume 11 (1970), pp. 151-185

[87] A.C. Tarjan Geographic distribution of some Meloidogyne spp. in Israel, Plant Dis. Rep., Volume 37 (1953), pp. 315-316

[88] G. Minz, Volume 11 (1961), pp. 69-70

[89] B. Yang; X. Zhong The identification of root-knot nematode in Olea europaea L, Sci. Silvae Sin., Volume 16 (1980), pp. 264-265

[90] P. Castillo; N. Vovlas; S. Subbotin; A. Troccoli A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in Southern Spain, Phytopathology, Volume 93 (2003), pp. 1093-1102

[91] N. Vovlas; G. Liébrans; P. Castillo SEM studies on the Mediterranean olive root-knot nematodes, Meloidogyne beatica and histopathology on two additional natural hosts, Nematology, Volume 5 (2004), pp. 749-754

[92] I.M. de; O. Abrantes; N. Vovlas; M.S.N. Santos Host-parasite relationships of Meloidogyne javanica and M. lusitanica with Olea europaea, Nematologica, Volume 38 (1992) no. 1, pp. 320-327

[93] F. Lamberti Plant nematode problems in the Mediterranean region, Helminthol. Abstr., Ser. B, Plant Nematol. (1981), pp. 145-166

[94] Z. Hashim A preliminary report on the plant-parasitic nematodes in Jordan, Nematol. Mediterr., Volume 7 (1979), pp. 177-186

[95] R. Inserra; N. Vovlas; F. Lamberti; T. Bleve-Zacheo Plant-parasitic nematodes associated with declining olive trees in southern Italy, Poljoprivredna Znanstvena Smotra, Agric. Conspec. Sci. (1976), pp. 419-424

[96] M. Santos Studies on root-knot nematodes, Meloidogyne spp. From olive trees in Portugal, Nematologica, E. J. Brill, Leiden, The Netherlands, 1982 (169 p.)

[97] M.E. Doucet; E.L. de Ponce de León y; N. Poloni Alteraciones histológicas inducidas por Meloidogyne incognita en raíces de olivo en Catamarca, Argentina, Nematol. Mediterr., Volume 25 (1997), pp. 275-277

[98] G. Thorne Principles of Nematology, McGraw-Hill Book Company, 1961 (553 p.)

[99] G. Agrios Plant Pathology, Academic Press, New York, NY, 1969

[100] W.R. Nickle Plant and insect nematodes, Marcel Dekker, Inc., 1984

[101] R. Colbran Studies of plant and soil nematodes. 7. Queensland records of the order Tylenchida and the genera Trichodorus and Xiphinema, Queensl. J. Agric. Sci., Volume 21 (1964), pp. 77-123

[102] L.J. Condit; W.T. Horne Nematode infestation of olive roots, Phytopathology, Volume 28 (1938), pp. 756-757

[103] H. Hirschmann; N. Paschalaki-Kourtzi; A. Triantaphyllou A survey of plant-parasitic nematodes in Greece, Ann. Inst. Phytopathol. Benaki, Volume 7 (1966), pp. 144-156

[104] F. Lamberti; N. Grecon; H. Zauchi A nematological survey of date palms and other major crops in Algeria, FAO Plant Prot. Bull., Volume 23 (1975), pp. 156-160

[105] P. Castillo; N. Vovlas Pratylenchus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management, Nematology Monographs and Perspectives, Vol. 6, Brill Leiden–Boston, The Netherlands–USA, 2007 (529 p.)

[106] F. Lamberti Presenza in Italia di un deperimento dell’olivo causato dal nematode Pratylenchus vulnus, All. et Jens, Phytopathol. Mediterr., Volume 8 (1969), pp. 232-234

[107] J. Pinochet; S. Verdejo-Lucas; J. Marull Host Suitability of Eight Prunus spp. and One Pyrus communis Rootstocks to Pratylenchus vulnus, P. neglectus, and P. thornei, J. Nematol., Volume 23 (1991), pp. 570-575

[108] A. Tarjan Plant-parasitic nematodes in the United Arab Republic, FAO Plant Prot. Bull., Volume 12 (1964), pp. 49-56

[109] S. Sher Revision of the Hoplolaiminae (Nematoda) VI. Helicotylenchus Steiner, 1945 1), Nematologica, Volume 12 (1966), pp. 1-56

[110] F. Fiume I generi dei nematodi viventi nella rizosfera dell’olivo in Calabria, Informat. fitopat., Volume 7 (1978), pp. 11-14

[111] N. Vovlas; R.N. Inserra Notes on Helicotylenchus dihystera on Olive in Sicily, Informat. fitopat., Volume 31 (1981), pp. 23-25 (in Italian)

[112] F. Roca; F. Lamberti Xiphinema aequum sp. n. (Nematoda: Dorylaimida) from Italy, with the description of male of Longidorus eridanicus, Nematol. Mediterr., Volume 16 (1988), pp. 87-91

[113] F. Lamberti; F. Roca; A. Agostinelli; T. Bleve-Zacheo Xiphinema barense n. sp. (Nematoda: Dorylaimida) from Italy, Nematol. Mediterr., Volume 14 (1986), pp. 101-106

[114] F. Lamberti The olive as a host for Xiphinema americanum Cobb, Phytopathol. Mediterr., Volume 8 (1969), p. 230

[115] A. Navas; A. Bello; M. Arias Ecology and potential distribution of Xiphinema diversicaudatum and X. pachtaicum (Nematoda: Longidoridae) in continental Spain, Nematologica, Volume 34 (1988), pp. 314-330

[116] F. Lamberti; T. Bleve-Zacheo; P.G.P. Martelli Un case di intersesso in Xiphinema ingens Luc et Dalmasso (Nematoda, Longidoridae), Nematol. Mediterr., Volume 3 (1975), pp. 181-183

[117] F. Lamberti; F. Roca; A. Agostinelli Xiphinema macroacanthum (Nematoda, Dorylaimida) a new species from southern Italy closely resembling X. ingens Luc and Dalmasso, Nematol. Mediterr., Volume 17 (1989), pp. 115-119

[118] M. Arias Nuevas aportaciones al conocimiento del genero Xiphinema (Nematoda) y su distribucion en los suelos espanoles, An. Edafol. Agribiolog., Volume 34 (1975), pp. 183-198

[119] G.P. Martelli; C.E. Taylor, Advances in disease vector research, Springer (1990), pp. 151-189

[120] D.P. Gallo; R.M. Jiménez, Volume 4 (1976), pp. 105-109

[121] N. Sasanelli; M. Coiro; T. D’Addabbo; R. Lemos; M. Ridolfi; F. Lamberti Reaction of an olive cultivar and an olive rootstock to Xiphinema index, Nematol. Mediterr., Volume 27 (1999), pp. 253-256

[122] E. Cohn; M. Mordechai The Influence of Some Environmental and Cultural Conditions On Rearing Populations of Xiphinema and Longidorus, Nematologica, Volume 16 (1970), pp. 85-93

[123] M. McKenry, Nematodes of olive, Olive Production Manual, University of California, Division of Agriculture and Natural Resources, 3353, Oakland Publications (1994), pp. 97-99

[124] R. Baines; J. Cameron; R. Soost Four biotypes of Tylenchulus semipenetrans in California identified, and their importance in the development of resistant citrus rootstocks, J. Nematol., Volume 6 (1974), pp. 63-66

[125] D. Stokes Andropogon rhizomatus parasitized by a strain of Tylenchulus semipenetrans not parasitic to four citrus rootstocks, Plant Dis. Rep., Volume 53 (1969), pp. 882-885

[126] F. Lamberti; N. Vovlas; A. Tirro Infettivita e patogenicita dei tre popolazioni italiane di Tylenchulus semipenetrans su agrumi ed altri ospidi, Nematol. Mediterr., Volume 4 (1976), pp. 85-91

[127] R.N. Inserra; N. Vovlas; J.H. O’Bannon A classification of Tylenchulus semipenetrans biotypes, J. Nematol., Volume 12 (1980), pp. 79-102

[128] R.N. Inserra; N. Vovlas; J.H. O’Bannon; R.P. Esser Tylenchulus graminis n. sp. and T. palustris n. sp.(Tylenchulidae), from native flora of Florida, with notes on T. semipenetrans and T. furcus, J. Nematol., Volume 20 (1988) no. 2, pp. 266-287

[129] S. Verdejo-Lucas; F.J. Sorribas; J. Pons; J.B. Forner; A. Alcaide Biotypes of Tylenchulus semipenetrans from Spanish citrus orchards, Fundam. Appl. Nematol., Volume 20 (1997), pp. 399-404

[130] F. Lamberti; R. Baines Infectivity of three biotypes of the citrus nematode (Tylenchulus semipenetrans) on two varieties of olive, Plant Dis. Rep., Volume 54 (1970), pp. 717-718

[131] N. Vovlas; R. Inserra Istopatologia di radici di olivo infestate da Rotylenchulus macrodoratus Dasgupta, Raski et Sher, Nematol. Mediterr., Volume 4 (1976), pp. 223-230

[132] E. Cohn; M. Mordechai Morphology and parasitism of the mature female of Rotylenchulus macrosomus, Rev. Nematol., Volume 11 (1988), pp. 385-389

[133] C. Koliopanos; N. Vovlas Records of some plant-parasitic nematodes in Greece with morphometrical descriptions, Nematol. Mediterr., Volume 5 (1977), pp. 207-215

[134] D.R. Dasgupta; D.J. Raski; S.A. Sher A revision of the genus Rotylenchulus Linford and Oliveira, 1940 (Nematoda: Tylenchidae), Proc. Helminthol. Soc. Wash., Volume 35 (1968), pp. 169-192

[135] N. Vovlas; F. Lamberti Nuovi ospiti naturali di Rotylenchulus macrodoratus Dasgupta, Raski and Sher, 1968 nella regione mediterranea, Nematol. Mediterr., Volume 2 (1974), pp. 177-179

[136] R.N. Inserra; N. Vovlas Life-cycle and biology of Rotylenchulus macrodoratus, 23–26 July, l8th Annual Meeting, Salt Lake City, Utah, J. Nematol., Volume 11 (1979), p. 302 (Abstract)

[137] R.N. Inserra; N. Vovlas; G. Fontanazza; G. La Casta Comportamento di alcune cultivar di olivo alle infestazioni di quarto specie di nematodi, Riv. Ortoflorofruttic. Ital., Volume 65 (1981), pp. 143-148

[138] J.G. Baldwin; M. Mundo-Ocampo Heteroderinae, cyst-and non-cyst-forming nematodes, Manual Agric. Nematol. (1991), pp. 275-362

[139] P. Castillo; N. Vovlas Factors affecting egg hatch of Heterodera mediterranea and differential responses of olive cultivars to infestation, J. Nematol., Volume 34 (2002), pp. 146-150

[140] W. Decraemer; J.E. Palomares-Rius; C. Cantalapiedra-Navarrete; B.B. Landa; I. Duarte; T. Almeida; N. Vovlas; P. Castillo Seven new species of Trichodorus (Diphtherophorina, Trichodoridae) from Spain, an apparent centre of speciation, Nematology, Volume 15 (2013) no. 1, pp. 57-100

[141] D. De Waele; G. Mancini; F. Roca; F. Lamberti Trichodorus taylori sp. n. (Nematoda: Dorylaimida) from Italy, Nematol. Mediterr., Volume 10 (1982), pp. 27-37

[142] W. Decraemer The family Trichodoridae: Stubby root and virus vector nematodes, Springer, 1995

[143] M. Almeida; D. De Waele; M.D.A. Santos; D. Sturhan Species of Trichodorus (Nematoda: Trichodoridae) from Portugal, Rev. Nematol., Volume 12 (1989), pp. 219-233

[144] D. Raski Revision of the genus Paratylenchus Micoletzky, 1922 and descriptions of new species. Part II of three parts, Gracilacus, J. Nematol., Volume 8 (1976), pp. 97-115

[145] R.N. Inserra; N. Vovlas Parasitic habits of Gracilacus peratica on olive feeder roots, Nematol. Mediterr., Volume 5 (1977), pp. 345-348

[146] I.M. de O. Abrantes; N. Vovlas; M.S.N. Santos Morphological studies on six, tylenchid nematode species associated with olive in Portugal, Cienc. Biol. Ecol. Syst., Volume 7 (1987), pp. 1-9

[147] R. Pena Santiago; E. Geraert New data on Aorolaimus perscitus (Doucet, 1980) and Gracilacus teres Raski, 1976 (Nematoda: Tylenchida) associated with olive (Olea europea L.) in the province of Jaén, Spain, Nematologica, Volume 36 (1990) no. 1, pp. 408-416

[148] N. Vovlas; R.N. Inserra Parasitic habits of Ogma rhombosquamatum and description of the male, J. Nematol., Volume 13 (1981), pp. 87-90

[149] P.S. Lehman Dissemination of phytoparasitic nematodes, Nematology circular No. 208, Florida, Departement of agriculture and consumer Services, Gainesville, FL, USA, 1994

[150] EPPO/OEPP Certification schemes, n^o 7 Nursery requirements-recommended requirements for establishments participating in certification of fruit or ornamental crops, Bull. OEPP/EPPO Bull., Volume 23 (1993), pp. 249-252

[151] N. Sasanelli; T.D. Addabbo; P. Dell Orco; M. Mencuccini The in vitro use of olive explants in screening trials for resistance to the root-knot nematode, Meloidogyne incognita, Nematropica, Volume 30 (2000), pp. 101-106

[152] J. Pinochet; S. Verdejo; A. Soler; J. Canals Host range of a population of Pratylenchus vulnus in commercial fruit, nut, citrus, and grape rootstocks in Spain, J. Nematol., Volume 24 (1992), pp. 693-698

[153] J. Katan Solar pasteurization of soils for disease, Plant Dis., Volume 64 (1980), pp. 450-454

[154] J. Katan Solar heating (solarization) of soil for control of soil-borne pests, Annu. Rev. Phytopathol., Volume 19 (1981), pp. 211-236

[155] A. Raio; A. Zoina; L. Moore The effect of solar heating of soil on natural and inoculated agrobacteria, Plant Pathol., Volume 46 (1997), pp. 320-328

[156] J.J. Stapleton; C.M. Heald Management of phytoparasitic nematodes by soil solarization (J. Katan; J.E. DeVay, eds.), Soil Solarization, CRC Press, Boca Raton, FL, USA, 1991, pp. 51-56

[157] A.I. Nico; R.M. Jiménez-Díaz; P. Castillo Solarization of soil in piles for the control of Meloidogyne incognita in olive nurseries in southern Spain, Plant Pathol., Volume 52 (2003), pp. 770-778

[158] J. Katan Soil solarisation (I. Chet, ed.), Innovative Approaches to Plant Disease Control, John Wiley, New York, USA, 1987, pp. 77-105

[159] R. Rodriguez-Kabana; G. Morgan-Jones; I. Chet, Plant and soil, Volume 100 (1987), pp. 237-247

[160] A.I. Nico; R.M. Jiménez-Dı́az; P. Castillo Control of root-knot nematodes by composted agro-industrial wastes in potting mixtures, Crop Prot., Volume 23 (2004), pp. 581-587

[161] H. Mojtahedi; G. Santo; A. Hang; J. Wilson Suppression of root-knot nematode populations with selected rapeseed cultivars as green manure, J. Nematol., Volume 23 (1991), p. 170

[162] T. D’Addabbo; G. De Mastro; N. Sasanelli; A. Di Stefano; R. Omidbaigi Suppressive action of different crocuferous crops on the root-knot nematode Meloidogyne incognita, Agroindustria, Volume 3 (2004), pp. 379-380

[163] P. Castillo; A.I. Nico; C. Azcón-Aguilar; C. Del Río Rincón; C. Calvet; R.M. Jiménez-Díaz Protection of olive planting stocks against parasitism of root-knot nematodes by arbuscular mycorrhizal fungi, Plant Pathol., Volume 55 (2006), pp. 705-713

[164] T. Mateille; P. Cadet; M. Fargette, Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes, Springer (2008), pp. 79-97

[165] T. Mateille; M. Achouri; M. Ater; A. Belaj; G. Besnard; P. Castillo; E. Chapuis; R. De La Rosa; F. De Lucas; Z. Devran; A.M. D’Onghia; H. El Maraghi; C. El Modafar; A. El Mousadik; A. El Oualkadi; Z. Ferji; N. Horrigue-Raouani; R. Jimenez-Diaz; M. Kadiri; S. Kallel; B. Khadari; M. Labiadh; B. Landa-Blanca; L. Leon; M. Montes-Borrego; A. Moukhli; M. Msallem; J.A. Navas-Cortes; N. Sasanelli; J. Tavoillot; M.A. Triki; A. Troccoli; E. Tzortzakakis; M. Ulas; N. Vovlas; T. Yaseen PESTOLIVE: an historical and ecological approach for understanding and managing soil-borne parasite communities on olive in the Mediterranean Basin, Adana, Turkey, 23–27 Sept (2012)

[166] ARIMNet Coordination of agricultural research in the Mediterranean area, 2012 (www.arimnet.net)

[167] F. Lamberti; E. Vouyoukalou; A. Agostinelli Longidorids (Nematoda: Dorylaimoidea) occurring in the rhizosphere of olive trees in Western Crete, Greece, Nematol. Mediterr., Volume 24 (1996), pp. 79-86

[168] E. Tzortzakakis; V. Peneva; D. Brown; A. Avgelis A literature review on the occurrence of nematodes of the family Longidoridae in Greece, Nematol. Mediterr., Volume 36 (2008), pp. 153-156

[169] E. Vlachopoulos Nematode species in nurseries of Greece, Ann. Inst. Phytopathol. Benaki (1991), pp. 115-122

[170] G. Minz; D. Strich-Harari; E. Cohn Plant-parasitic nematodes in Israel and their control, 1963 (84 p.) (in Hebrew)

[171] Anon, Department of Agricultural Research, Ministry of Agriculture, Jordan (1970), pp. 92-96 (in Arabic)

[172] A. Tobar Jiménez Ditylenchus virtudesae n. sp. (Nematoda: Tylenchidae), habitante de los suelos granadinos, Revta Iber. Parasit., Volume 24 (1964), pp. 51-56

[173] M. Talavera; A. Tobar-Jimenez Plant-parasitic nematodes from unirrigated fields in Alhama, southeastern Spain, Nematol. Mediterr., Volume 25 (1997), pp. 73-82

[174] U.K. Mehta; D. Raski Revision of the genus Criconema Hofmänner and Menzel, 1914 and other related genera (Criconematidae: Nematoda), Indian J. Nematol., Volume 1 (1971), pp. 145-198

[175] C.E. Rossi; L. Ferraz Fitonematóides das Superfamílias Criconematoidea e Dorylaimoidea Associados a Fruteiras de Clima Subtropical e Temperado nos Estados de São Paulo e Minas Gerais, Nematol. Bras., Volume 29 (2005), pp. 183-192

[176] N. Vovlas Macroposthonia sicula n. sp. (Nematoda: Criconematidae), a parasite of olive trees in Sicily, J. Nematol., Volume 14 (1982), pp. 95-99

[177] Z. Hashim Re-diagnosis and a key to species of Neolobocriconema Mehta and Raski, 1971 (Nematoda: Tylenchida), with a description of N. olearum n. sp. from Jordan, Syst. Parasitol., Volume 6 (1984), pp. 69-73

[178] F.P. D’Errico; F. Lamberti; F. Fiume Ritrovamento di Dolichodorus heterocephalus Cobb nell’Italia meridionale, Nematol. Mediterr., Volume 5 (1977), pp. 99-101

[179] J. Philis; M. Siddiqi A list of plant-parasitic nematodes in Cyprus, Nematol. Mediterr., Volume 4 (1976), pp. 171-174

[180] J. Bridge Plant Nematology in Jordan, Report of Scientific Liaison Office, Overseas Development Ministry, London, UK, 1978 (20 p.)

[181] C. Rossi; L. Ferraz Plant-parasitic nematodes of the superfamily Tylenchoidea associated with subtropical and temperate fruits in the States of São Paulo and Minas Gerais, Brazil, Nematol. Bras., Volume 29 (2005), pp. 171-182

[182] M. Romero; M. Arias Nematodes of Solanaceae in the Mediterranean zone of southern Spain. 1. Tylenchida, Boln R. Soc. esp. Hist. nat. (Biol.), Volume 67 (1969), pp. 121-142

[183] C. Sethi; H. Gaur; K. Kaushal; A. Srivastava; E. Khan Occurrence of root-knot nematodes on fruit plants in association with Agrobacterium tumefaciens, Int. Nematol. Netw. Newslett., Volume 5 (1988), pp. 12-13

[184] F. Lamberti; M. Di Vito Sanitation of root-knot nematode infected olive-stocks, Proceeding of the 3th Congress of the Mediterranean Phytopathology Union, Oeiras, Portugal, 1972, pp. 401-411

[185] W. Abu-Gharbieh; K. Makkouk; A. Saghir Response of different tomato cultivars to the root-knot nematode, tomato yellow leaf curl virus, and Orobanche in Jordan, Plant Dis. Rep., Volume 62 (1978), pp. 263-266

[186] A. Saad; F. Nienhaus, Pflanzenpathologie und Pflanzenschutz, Volume 76 (1969), pp. 537-551

[187] I.M. de O. Abrantes Nematode problems of olive trees, European Society of Nematologists, Bari, Italy, 24–30 August (1980), pp. 27-28

[188] A. Macara A importância agrícola dos nemátodos Meloidogyne spp. no espaço portugues, Bol. Agron. Nitrat. Portugal Agran, Volume 9 (1971), pp. 3-15

[189] A. Zari; F. Khozeini; S. Barouti; H. Zamanizadeh Detection and distribution of Root-lesion nematodes (Pratylenchidae) on fruit trees in Northeast regions of Iran, Phytopathology, Volume 101 (2011), p. S175

[190] R.N. Inserra; A. Zepp; N. Vovlas I Pratylenchus dell’Italia meridionale, Nematol. Mediterr., Volume 7 (1979), pp. 137-162

[191] R. McLeod; F. Reay; J. Smyth Plant nematodes of Australia listed by plant and by genus, NSW Agric. (1994)

[192] T. Badra; M. Khattab The effect of nitrogen fertilizers on the growth of olive and in relation to infestations of Rotylenchulus reniformis, Nematol. Mediterr., Volume 8 (1980), pp. 67-72

[193] M.R. Siddiqi New plant nematode genera Plesiodorus (Dolichodorinae), Meiodorus (Meiodorinae subfam. n.), Amplimerlinius (Merliniinae) and Gracilancea (Tylodoridae grad. n.), Nematologica, Volume 22 (1976), pp. 390-416

[194] Z. Hashim Description of Tylenchorhynchus tenuis n. sp. and observation on Rotylenchus cypriensis Antoniou, 1980 (Nematoda: Tylenchida) from Jordan, Syst. Parasitol., Volume 6 (1984), pp. 33-38

[195] R. Baines Citrus-root nematodes on olive: Pest pathologically and morphologically similar to that on orange roots infests and reproduces on olive roots, Calif. Agric., Volume 5 (1951) (11 p.)

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