Brassicacea-based management strategies as an alternative to combat nematode pests: A synopsis

Crop Protection 80 (2016) 21e41

Contents lists available at ScienceDirect

Crop Protection journal homepage: www.elsevier.com/locate/cropro

Review

Brassicacea-based management strategies as an alternative to combat nematode pests: A synopsis Hendrika Fourie a, *, Preeti Ahuja a, Judith Lammers b, Mieke Daneel c a

Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, 2520 Potchefstroom, South Africa Laboratory of Nematology, P.O. Box 8123, Wageningen University and Research Centre, Netherlands c Agricultural Research Council e Institute for Tropical and Subtropical Crops, Private Bag X11208, Nelspruit 1200, South Africa b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 August 2015 Received in revised form 25 October 2015 Accepted 27 October 2015 Available online 13 November 2015

Nematode pests parasitise and cause substantial crop yield and quality losses to a wide range of crops worldwide. To minimize such damage, the exploitation and development of alternative nematode control strategies are becoming increasingly important, particularly as a result of global efforts to conserve the ozone layer as well as our soil and water substrates. Inclusion of Brassicaceae crops in cropping systems is one such alternative and has been demonstrated in most cases to be effective in managing the top-three rated economically important nematode pests, viz. root-knot (Meloidogyne), cyst (Heterodera and Globodera) and lesion (Pratylenchus) nematodes as well as others. In the past nematode pests were and still are generally managed successfully by the use of synthetically-derived nematicides, which are progressively being removed from world markets. However, fragmented and limited information about the use of Brassicaceae crops as a nematode management tool exists in various countries. The need thus arose to summarize, compare and discuss the vast amount of information that has been generated on this topic in a concise article. This paper therefore represents a comprehensive, practical and critical review of the use and effect(s) of Brassicaceae-based management strategies and the biofumigation and cover-crop/rotation characteristics of Brassicaceae in reducing nematode-pest population levels in global cropping systems. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Biofumigation Brassicaceae Cover/green manure crop Resistance PPN Soil amendments

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 The family Brassicaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 2.1. Mechanisms of Brassicaceae spp. to manage PPN . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 2.2. Biofumigation and the role of GSL-degradation products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 Effects of biofumigation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34 3.1. Root-knot nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34 3.2. Cyst nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 3.3. Lesion nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 3.4. Other economically important nematode pests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 3.5. Non-target, beneficial nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 3.6. Factors contributing to the success of nematode-pest control using biofumigation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 Cover and rotation crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 4.1. Root-knot nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 4.2. Lesion nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 4.3. Other economically important nematode pests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

* Corresponding author. E-mail addresses: [email protected] (H. Fourie), [email protected] (P. Ahuja), [email protected] (J. Lammers), [email protected] (M. Daneel). http://dx.doi.org/10.1016/j.cropro.2015.10.026 0261-2194/© 2015 Elsevier Ltd. All rights reserved.

22

5. 6.

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

1. Introduction Plant-parasitic nematodes (PPN) are important pests of a wide range of agri- and horticultural crops and therefore a major constraint to intensive crop production systems worldwide (Nyczepir and Thomas, 2009; Singh et al., 2013; Stirling, 2014). The latter scenario is particularly true for the recently top-ten rated nematode pests of which root-knot (Meloidogyne), cyst (Heterodera and Globodera) and root lesion (Pratylenchus) nematodes fill the top three positions (Jones et al., 2013). According to these authors, 10 of the 98 described Meloidogyne species are listed as agricultural pests, while five cyst and six lesion nematode species respectively are of economic concern worldwide. Effective management of nematode pests is hence crucial to ensure sustainable crop production and food security in both developed and developing countries. During the major part of the 20th century, control of economically important PPN was generally based on the application of synthetically-derived nematicides (Vervoort et al., 2014). These chemicals pose big health risks because they are extremely toxic to animals and humans and also contaminate the air and groundwater sources (EPA, 2008; Onkendi et al., 2014; Zasada et al., 2010). Currently, nematicides that are classified as organophosphates, carbamates or soil fumigants are frequently used for nematode control in various countries (EPA, 2014; Van Zyl, 2013). The challenge to control nematode pests is, however, becoming more difficult as Class I, red-band nematicides are progressively withdrawn from world markets (EPA, 2008; Gamliel et al., 2000; Ruzo, 2006; Verdoorn, 2012). For example, aldicarb, endosulfan and methyl bromide that were used to control nematode and other soilborne pests in high value crops in particular, are no longer available for use in many countries and several others will most likely follow suit in the near future. Repetitive use of such nematicides also results in reduced efficacy because of the buildup of microbe populations that degrade the active substances of such products over time (Oka, 2010). A progressive need thus exists to exploit and identify alternative management strategies to protect food crops against nematode pests (Singh and Prasad, 2014). In many world countries the nematode-pest problem is further aggravated by the use of cropping systems that are conducive to the build-up of populations of PPN (Desaeger and Rao, 1999; Riekert and Henshaw, 1998), the limited availability of genetic host-plant resistance to economically important nematode pests in some crops (Cook and Starr, 2006), the general ineffective use of biological control (Agbenin, 2011; Fourie et al., 2014) as well as the poor quality of agricultural soils in general (Hugo et al., 2014; Widmer et al., 2002). Degraded soils, which are predominant in crop production areas in most parts of the world, do not favour, for example the build-up of beneficial nematodes that can contribute to soil quality (Gruver et al., 2010) and sustainable food production in the presence of economically important nematode pests. Although being advocated as suitable and superior for their adverse effects on nematode pest populations, Brassicaceae crops are associated with a wide range of PPN that parasitize them (Tables 1e3). Economically important plant-parasitic nematode genera such as cyst- (Globodera and Heterodera), dagger- (Xiphinema) lesion- (Pratylenchus), reniform- (Rotylenchulus), ring-

(Criconema), root-knot (Meloidogyne), spiral- (Helicotylenchus, Rotylenchus, Scutellonema), stubby-root (Paratrichodorus and Nanidorus), stunt (Tylenchorhynchus) and others have been reported to infect a wide spectrum of Brassicaceae species. These include Barbarea vulgaris, Brassica campestris, Brassica carinata, Brassica chinensis, Brassica hirta, Brassica juncea, Brassica napus, Brassica nigra, Brassica oleraceae, Brassica oxyrrhina and Lange, Brassica rapa, Capsella bursa-pastoris, Eruca sativa, Erucastrum gallicum, Hesperis matronalis, Lepidium draba, Lepidium latifolium, Lepidium sativum, Moricandia moricandioides, Nasturtium officinale, Raphanus sativus, Sinapsis alba, Sisymbrium austriacum and Sisymbrium irio (Table 1). Although the use of Brassicaceae crops for their biofumigation, cover- and/or, poor-host characteristics is not always effective in reducing population levels of PPN, it has been proven in many studies as an effective alternative option to combat the majority of these pests (Tables 2 and 3). An added benefit of using Brassicaceae spp. as cover crops is that they can also significantly reduce population levels of other soil-borne pathogens (Sarwar et al., 1998), pests (Brown and Morra, 1997) and weeds (Fourie et al., 2015; Nyczepir and Thomas, 2009). Ultimately, such cover crops can reduce the ecological footprint of agriculture (Gruver et al., 2010), while improving soil structure (Nyczepir and Thomas, 2009). Biofumigation has been advocated as an eco-friendly tactic to manage nematode pests compared to synthetic fumigants (Kruger et al., 2013; Matthiessen and Kirkegaard, 2006). Isothiocyanates (ITCs) released by Brassicaceae crops can, however, be equally or even more toxic than their synthetically-derived peers (Gimsing and Kirkegaard, 2009; Vervoort et al., 2014). In addition, ITCs do not only affect the target nematode pest, but can also impact adversely on a wide range of other soil biota. This way it may even lead to the destabilization of the soil food webs as has been reported by Cao et al. (2004). Furthermore, reports on the efficacy of biofumigation in reducing plant-parasitic nematode populations under field conditions have also been variable (Ploeg, 2008). In some cases, high levels of nematode-pest management were demonstrated (Mojtahedi et al., 1993; Rahman and Somers, 2005) as opposed to reports of insignificant or no reduction in levels of target nematode pests (Engelbrecht, 2012; Johnson et al., 1992; Stirling and Stirling, 2003). Ultimately, acceptable levels of suppression of nematode pest populations as a result of biofumigation with Brassicaceae plant tissues have been demonstrated in several regions worldwide (Table 2). Due to controversial reports about the useful- and/or effectiveness of Brassicaceae strategies to manage PPN, a need exists to concisely summarize the vast range of related literature that became available since the inception of research related to this topic. This way researchers, other interested experts and producers can focus on lessons learnt in the past by adopting and/or changing such options to manage target nematode pests. In this review, no detailed description of the family Brassicaceae, mode of action of chemical substances such as glucosinolate (GSL) degradation products and their roles as bionematicides during biofumigation processes has been included. This has been done extensively by various authors such as Avato et al. (2013), Brown and Morra (1997), Cohen et al. (2005), Gimsing and Kirkegaard (2006), Lazzeri et al. (1993), Muller (2009), Sikora (1992), Stirling (1991) and Zasada and Ferris (2003). This paper mainly focuses

H. Fourie et al. / Crop Protection 80 (2016) 21e41

23

Table 1 A range of plant-parasitic nematodes associated with Brassicaceae crops in some world countries. Brassicaceae species

Associated plant-parasitic nematodes

Country

Reference

Brassica sp.

Aphelenchoides bicaudatus, Ditylenchus sp., Helicotylenchus dihystera, Hemicriconemoides strictathecatus, Meloidogyne sp., Pratylenchus coffeae, Rotylenchulus reniformis, Scutellonema clathricaudatum, Quinisulcius capitatus, Tylenchulus sp., Xiphinema sp. Heterodera cruciferae Meloidogyne incognita, Tylenchorhynchus mashhoodi, Hoplolaimus indicus, Helicotylenchus indicus, Xiphinema sp., Longidorus sp., Paralongidorus sp., Paratrichodorus porosus Meloidogyne incognita, Meloidogyne javanica, Meloidogyne arenaria Meloidogyne incognita, Meloidogyne javanica, Meloidogyne arenaria Criconema sp., Meloidogyne incognita, Helicotylenchus sp., Rotylenchus sp., Scutellonema sp., Tylenchorhynchus sp. Meloidogyne arenaria Pratylenchus neglectus Helicotylenchus sp., Hoplolaimus sp., Meloidogyne sp., Pratylenchus sp., Criconemoides sp., Heterodera sp., Hemicycliophora sp., Longidorus sp., Rotylenchulus sp. Pratylenchus sp., Tylenchorhyncus sp., Paratylenchus sp. Geocenamus brevidens, Meloidogyne sp., Paratylenchus microdorus, Paratylenchus sp., Pratylenchus neglectus, Pratylenchus thornei, Pratylenchus zeae, Rotylenchulus parvus, Scutellonema brachyurus, Tylenchorhynchus capitatus, Tylenchorhynchus sp. Hoplolaimidae, Meloidogyne spp., Paratrichodorus spp., Pratylenchus spp., Xiphinema spp. Criconemella ornata, Meloidogyne incognita, Meloidogyne javanica Meloidogyne javanica Meloidogyne arenaria Aphelenchoides fragariae, Criconemella sp., Ditylenchus dipsaci, Globodera rostochiensis, Helicotylenchus diltystera, Hoplolaimus sp., Meloidogyne sp., Longidorus sp., Paratrichodorus sp., Pratylenchus penetrans, Trichodorus sp., Tylenchus sp., Xiphinema americanum Belonolaimus longicaudatus, Paratrichodorus minor, Helicotylenchus sp., Hoplolaimus columbus, Meloidogyne incognita, Pratylenchus penetrans Heterodera cruciferae Pratylenchus brachyurus, Pratylenchus zeae, Pratylenchus scribneri, Pratylenchus neglectus, Pratylenchus loosi, Meloidogyne sp., Tylenchorynchus sp., Belonolaimus sp., Scutellonema sp., Helicotylenchus sp., Hoplolaimus sp., Trichodorus sp., Paratrichodorus sp., Xiphinema sp., Longidorus sp., Criconemoides sp., Hemicriconemoides sp., Hemicycliophora sp., Tylenchus sp., Coslenchus sp., Polenchus sp., Paratylenchus sp., Quinisulcius sp. Pratylenchus thornei, Helicotylenchus sp., Heterodera cruciferae Heterodera mediterranea, Pratylenchus neglectus, Tylenchus sp., Irantylenchus sp., Zygotylenchus sp., Paratylenchus sp., Amplimerlinius sp., Meloidogyne incognita Meloidogyne sp. Criconema mutabile, Helicotylenchus dihystera, Helicotylenchus krugeri, Hemicycliophora lutosa, Hemicycliophora natalensis, Heterodera schachtii, Longidorus pisi, Meloidogyne incognita, Meloidogyne javanica, Paratrichodorus minor, Pratylenchus zeae, Rotylenchus unisexus, Scutellonema brachyurus, Tylenchorhynchus capitatus Meloidogyne incognita, Meloidogyne javanica, Meloidogyne arenaria Meloidogyne javanica, Meloidogyne spp., Radopholus similis, Quinisulcius capitatus Helicotylenchus nannus, Meloidogyne arenaria, Meloidogyne javanica, Meloidogyne incognita, Meloidogyne spp. Meloidogyne spp. Aphelenchoides sp., Aphelenchus avenae, Helicotylenchus dihystera, Helicotylenchus egyptiensis, Helicotylenchus nannus, Meloidogyne javanica, Meloidogyne incognita, Scutellonema sp., Trichodorus sp. Ditylenchus dipsaci Meloidogyne arenaria, Meloidogyne hapla, Meloidogyne incognita, Meloidogyne javanica Aphelenchoides fragariae, Criconemella sp., Ditylenchus dipsaci, Globodera rostochiensis, Helicotylenchus dihystera, Hoplolaimus sp., Meloidogyne sp., Longidorus sp., Paratrichodorus sp., Pratylenchus penetrans, Trichodorus sp., Tylenchus sp., Xiphinema americanum Belonolaimus longicaudatus, Paratrichodorus minor, Helicotylenchus sp., Hoplolaimus Columbus, Meloidogyne incognita, Pratylenchus penetrans Criconema sp., Meloidogyne incognita, Helicotylenchus sp., Rotylenchus sp., Scutellonema sp., Tylenchorhynchus sp. Meloidogyne incognita, Meloidogyne javanica, Meloidogyne arenaria Meloidogyne sp. Heterodera schachtii, Meloidogyne javanica, Pratylenchus zae, Rotylenchus unisexus Aporocelaimellus radicus Meloidogyne incognita, Meloidogyne javanica, Meloidogyne arenaria Radopholus similis Meloidogyne javanica Meloidogyne javanica Meloidogyne incognita, Meloidogyne javanica

Benin

Baimey et al. (2009)

United States of America India

Bird (2008) Vyas et al. (2008)

Fiji Nepal South Africa

Khurma et al. (2008) Bhardwaj and Hogger (1984) Engelbrecht (2012)

Zimbabwe Czech Republic Egypt

Keetch and Buckley (1984) Kumari (2012) Korayem et al. (2011)

South Africa South Africa

Mouton et al. (2011) Marais (2008)

South Africa

Nel et al. (2008)

United States of America Zimbabwe Zimbabwe Philippines

Johnson et al. (1992) Keetch and Buckley (1984) Keetch and Buckley (1984) Pedroche et al. (2013)

Pakistan

Anwar and Mckenry (2012)

Russia Kenya

Chizov et al. (2009) Waceke (2007)

Turkey

Mennan and Handoo (2006)

New Zealand South Africa

Knight et al. (1997) Kleynhans et al. (1996)

Nepal South Africa Zimbabwe

Bhardwaj and Hogger (1984) Keetch and Buckley (1984) Keetch and Buckley (1984)

Angola Malawi

Keetch and Buckley (1984) Keetch and Buckley (1984)

New Zealand Zimbabwe

Knight et al. (1997) Keetch and Buckley (1984)

Philippines

Pedroche et al. (2013)

Pakistan

Anwar and Mckenry (2012)

South Africa

Engelbrecht (2012)

Fiji New Zealand South Africa India Nepal South Africa Malawi Malgasy Republic Zimbabwe

Khurma et al. (2008) Knight et al. (1997) Kleynhans et al. (1996) Jain and Saxena (1993) Bhardwaj and Hogger (1984) Keetch and Buckley (1984) Keetch and Buckley (1984) Keetch and Buckley (1984) Keetch and Buckley (1984)

Brassica spp. Brassica campestris

Brassica campestris Brassica chinensis Brassica juncea Brassica juncea Brassica napus Brassica napus Brassica napus Brassica napus

Brassica napus Brassica Brassica Brassica Brassica

napus napus nigra oleracea

Brassica oleracea Brassica oleracea Brassica oleracea

Brassica oleracea

Brassica oleracea Brassica oleracea

Brassica oleracea Brassica oleracea Brassica oleracea Brassica oleracea Brassica oleracea

Brassica rapa Brassica rapa Raphanus sativus

Raphanus sativus Raphanus sativus Raphanus Raphanus Raphanus Raphanus Raphanus Raphanus Raphanus Raphanus Raphanus

sativus sativus sativus sativus sativus sativus sativus sativus sativus

24

Table 2 Effects of biofumigation on plant-parasitic nematode population levels and plant parameters using plant amendments of various Brassicaceae species. Brassicaceae species used as a management tool

Cultivar/variety/ selection

Follow-up crop(s)

Type of soil amendment

Target nematode pest genus and/or species

Effect on the target nematode pest

Country

Reference

Barbarea vulgaris

Not available

Solanum tuberosum

Aqueous leaf extracts

Globodera pallida

United Kingdom

Lord et al. (2011)

Brassica campestris

Not available

Solanum tuberosum

Green manure

Meloidogyne chitwoodi, Pratylenchus neglectus

Brassica campestris

Cvs Barkant, Polybra

Vitis vinifera

Green manure

Meloidogyne javanica

Brassica carinata

Not available

Solanum tuberosum

Seed meal

Globodera pallida

Brassica carinata

Not available

Seed meal

Meloidogyne chitwoodi

Brassica carinata

Not available

Seed meal

Meloidogyne incognita

Brassica carinata

Accession 94044

Solanum tuberosum, Solanum lycopersicum Cucurbita pepo Solanum lycopersicon Not available

Green manure

Pratylenchus neglectus

Brassica juncea

Cv Caliente 199

Vitis vinifera

Green manure

Meloidogyne javanica, Criconemoides xenoplax

Brassica juncea

Cv Caliente 99

Solanum tuberosum

Green manure

Globodera pallida

Brassica juncea

CvsTerrafit, Terratop, Terraplus Cv Nemat

Not available

Green manure

Solanum tuberosum

Green manure

Tricodorus spp., Tylenchorhynchus spp. Meloidogyne incognita

Arctium lappa, Raphanus sativus cv Bantyukitaichi Solanum tuberosum

Green manure

Pratylenchus penetrans

Seed meal

Globodera pallida

Brassica juncea

Breeding lines: Y-010, 17-10 Cvs Nemfix, Arid.#6, Fumus, ISC199 Not available

Solanum lycopersicum

Leaf and seed meal

Meloidogyne incognita, Meloidogyne javanica, Meloidogyne enterolobii, Heterodera glycines

Brassica juncea

Cv Pacific Gold

Capsicum annuum

Seed meal

Meloidogyne incognita

Brassica juncea

Not available

Daucus carota

Seed meal

Heterodera carotea

Brassica juncea

Cv Pacific Gold

Pyrus malus

Seed meal

Pratylenchus penetrans

Brassica juncea

Cv Nemfix, BQ Mulch

Vitis vinifera

Green manure

Meloidogyne javanica

Brassica juncea

Cv Pacific Gold

Not available

Seed meal

Brassica juncea

Var. PBR 97

Solanum lycopersicum

Green manure

Meloidogyne incognita, Pratylenchus penetrans Meloidogyne incognita

<5% reduction in J2 population levels 48% reduction in Meloidogyne chitwoodi J2 levels; >16% increase in tuber mass 54% reduction in P. neglectus populations Reduced egg production between 61 and 73% <5% reduction in J2 population levels >80% reduced tuber infection >70% reduction in J2 populations Zero to 65% reduction in population levels 51% reduction in Meloidogyne javanica populations but no effect on Criconemoides xenoplax Significant reduction in viable encysted eggs No significant reduction in population levels Increase in population levels Increased population levels from 14 to 57% 50e95% reduction in J2 population levels 76e94% reduction in Meloidogyne incognita J2 population levels, 73e93% for galling and 87e98 for egg masses per root 95e98% RKN and cyst J2 mortality in soil >96% reduction in population levels <46% reduction in the number of viable eggs of cyst nematode at the time of harvest >90% reduction in nematode populations 75% reduction in nematode populations >90% suppression of both plant-parasitic nematodes Reduced root galling by 14%; increased seedling

Brassica juncea Brassica juncea

Australia

McLeod and Steel (1999)

United Kingdom

Lord et al. (2011)

United States of America Henderson et al. (2009) Italy

Lazzeri et al. (2009)

Australia

Potter et al. (1998)

South Africa

Kruger et al. (2015) Kruger (2013)

United Kingdom

Ngala et al. (2014)

Germany

Vervoort et al. (2014)

South Africa

Engelbrecht (2012)

Japan

Sakuma et al. (2011)

United Kingdom

Lord et al. (2011)

Brazil

Oliveira et al. (2011)

United States of America Meyer et al. (2011) Denmark

Grevsen (2010)

United States of America Mazzola et al. (2009) Australia

Rahman et al. (2009)

United States of America Zasada et al. (2009) India

Randhawa and Sharma (2007)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Brassica juncea

United States of America Al-Rehiayani et al. (1999)

Cucurbita pepo cv Seneca, Cucumis melo cv Athena, Lycopersicon esculentum cv BHN 640 Pyrus malus

Green manure Cover crop

Meloidogyne incognita

Seed meal

Pratylenchus spp.

Cvs Florida Broadleaf, Curly leaf, Fumus L71, Fumus E75, Ida gold

Brassica juncea

Cv Pacific Gold

Brassica juncea

Cv Forge

Seed meal and bran Solanum tuberosum cv Russet Burbank, Fragaria x ananassa cv Veestar and Zea mays cv Extra early super sweet

Pratylenchus penetrans, Pratylenchus neglectus, Heterodera glycines Heterodera schachtii, Meloidogyne incognita, Meloidogyne hapla

Brassica juncea

Cv Nemfix

Vitis vinifera

Meloidogyne javanica

Brassica juncea

Cvs 99Y-1-1, Claret, Ebony, Ruby, Topaz

Vitis vinifera

Green manure and seed meal Green manure

Brassica juncea

Accession 99Y11

Not available

Green manure

Pratylenchus neglectus

Brassica napus

Cv AV Jade

Vitis vinifera

Green manure

Meloidogyne javanica, Criconemoides xenoplax

Brassica napus

Solanum tuberosum Cvs. Maxima Plus, Nemcon Cv Dwarf Essex, Sunrise Not available

Green manure

Globodera pallida

Seed meal

Brassica napus

Meloidogyne javanica

Brassica napus

Cv Dwarf Essex and Athena

Pyrus malus

Seed meal

Meloidogyne incognita, Pratylenchus penetrans Pratylenchus penetrans

Brassica napus

Cv Athena

Pyrus malus

Seed meal

Pratylenchus spp.

Brassica napus

Var. GSL1

Solanum lycopersicum

Green manure

Meloidogyne incognita

Brassica napus

Not available

Pyrus malus

Seed meal

Pratylenchus sp.

Brassica napus

Cv Dwarf Essex

Pyrus malus

Seed meal

Pratylenchus penetrans

Brassica napus

Green manure

Meloidogyne javanica

Green manure

Pratylenchus neglectus

Brassica napus

Vitis vinifera Ssp. Oleifera biennis Cvs. Humus, Rangi, Winfred, Arran, Bonar, Hobson, Korina, Striker, Ssp. rapifera Cv Highlander Cv Dunkeld assession Not available no. 94713 Cv Humus Solanum tuberosum

Green manure

Meloidogyne chitwoodi race 2, Pratylenchus neglectus

Brassica napus

Cv Jupiter

Green manure

Meloidogyne chitwoodi

Brassica napus

Lycopersicon esculentum Solanum tuberosum Hordeum vulgare

99% reduction in population Reduced Pratylenchus penetrans populations between 66 and 74; high toxicity and anti-hatching effects on Heterodera glycines and Heterodera schachtii J2 Reduced population levels between 75 and 93% 63e86% reduction in egg production by Meloidogyne javanica 6e68% reduction in population levels Reduced Meloidogyne javanica and C.riconemoides xenoplax populations by 14 and 8% respectively Reduced J2 populations between 10 and 33% 90e95% reduction in recovery of both PPN Reduced nematode populations between 25 and 50% Reduced nematode populations by 56e72% 8% reduction in root galling and 8 and 12% increased in seedling height and weight respectively Reduced 76% Pratylenchus sp. populations Significantly reduced population levels 76e82% reduction in egg production

United States of America Mazzola et al. (2007) Canada

Yu et al. (2007)

Australia

Rahman and Somers (2005)

Australia

McLeod and Steel (1999)

Australia

Potter et al. (1998)

South Africa

Kruger et al. (2015) Kruger (2013)

United Kingdom

Lord et al. (2011)

United States of America Zasada et al. (2009) United States of America Mazzola et al. (2009)

United States of America Mazzola et al. (2007) India

Randhawa and Sharma (2007)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Brassica juncea

height by 10% and weight by 13% Reduced populations levels United States of America Monfort et al. (2007) between 23 and 91%

United States of America Cohen et al. (2005) United States of America Mazzola et al. (2001) Australia

Zero to 57% reduction in Australia population levels United States of America 79e94% reduction in Meloidogyne chitwoodi populations but no effect on Pratylenchus neglectus populations 89% reduction in United States of America population levels

McLeod and Steel (1999)

Potter et al. (1998) Al-Rehiayani and Hafez (1998)

Mojtahedi et al. (1993)

25

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26

Table 2 (continued ) Brassicaceae species used as a management tool

Cultivar/variety/ selection

Brassica napus

Type of soil amendment

Target nematode pest genus and/or species

Effect on the target nematode pest

Country

Green manure

Meloidogyne incognita, Meloidogyne javanica

Green manure

Brassica napus

Var Forage Star

Vigna subterranea

Green manure

Meloidogyne chitwoodi race 1 and 2 Meloidogyne incognita

Brassica nigra

Not available

Solanum lycopersicum

Green manure

Meloidogyne incognita

Brassica nigra

Assession no. 95067

Not available

Green manure

Pratylenchus neglectus

Brassica oleracea

Not available

Solanum lycopersicum

Green manure

Meloidogyne incognita

Brassica oleracea

Not available

Solanum tuberosum Solanum lycopersicum Capsiceae capsicum

Green manure

50e100% reduction in Meloidogyne spp. populations 98% reduction in population levels 10e95% reduction in root galling 37% reduction in root galling Zero to 56% reduction in population levels Reduced 88% gall numbers, 90% egg masses, 88% females, 99% developmental stages and 74% J2 at transplanting 40e100% reduction in nematode population levels

United States of America Johnson et al. (1992)

Brassica napus

Cvs Dwarf Essex, Elena, Cucurbita pepo cv Dixie Hybrid Indore, Cascade, Bridger, Humus, Jupiter Cvs Jupiter, Bridger Solanum lycopersicum

Brassica oleracea

Not available

Solanum lycopersicum

Ground leaching technology (GLT) system

Brassica oleracea Brassica oleracea

Var. Acephala, Botrytis, Solanum tuberosum Italic, Tapa, Ttronchuda Not available Cucumis spp.

Green manure

Brassica oleracea

Cv Liberty

Green manure

Brassica oleracea

Var. Acephala Cv Vitis vinifera Gruner Solanum lycopersicum Vars. Chinensis, Iitaliensis Capitata Compacta Var Drumhead, Glory of Vigna subterranea Enkuizen

Helicotylenchus spp., Pratylenchus spp., Meloidogyne spp., Tylenchus spp., Heterodera spp. Meloidogyne incognita race 94 and 61% reduction in 2 population levels and fresh fruit yield respectively Globodera rostochiensis 47e78% reduction in newly formed cysts Meloidogyne incognita 70e96% reduction in population levels Meloidogyne incognita, 66e98% reduction in Meloidogyne javanica Meloidogyne spp. population levels Meloidogyne javanica Significantly reduced egg productions Meloidogyne incognita 75e100% reduction in root galling

Brassica oleracea

Cucumis melo cv Durango

Green manure

Green manure Green manure

Green manure

Meloidogyne incognita

Brassica oxyrrhina

Assession no. 95060

Not available

Green manure

Pratylenchus neglectus

Brassica rapa

Not available

Solanum tuberosum

Green manure

Globodera pallida

Brassica rapa

Not available

Solanum tuberosum

Green manure

Globodera rostochiensis

Brassica rapa

Var. TL15

Solanum lycopersicum

Green manure

Meloidogyne incognita

Brassica rapa

Cvs Purple Top White Globe, White Egg, Dwarf Essex

Cucurbita pepo cv Seneca, Cucumis melo cv Athena Lycopersicon, sculentum cv BHN 640

Cover crop

Meloidogyne incognita

26e83% reduction in root galling using var Drumhead 60e94% reduction in root galling using var Glory of Enkhuizen 3395% reduction in population levels 65% reduction in J2 population levels 85% decreased in cyst formation 52% decrease in root galling; 26 and 34% increase in seedling height and weight respectively 41% reduction in population levels

Reference

United States of America Mojtahedi et al. (1991) South Africa

Kwerepe and Labuschagne (2003) United States of America Stapleton and Duncan (1998) Australia Potter et al. (1998) Egypt

Youssef and Lashein (2013)

Kenya

Kago et al. (2013)

South Africa

Mashela et al. (2013)

Portugal

Aires et al. (2009)

United States of America Roubtsova et al. (2007) United States of America Ploeg and Stapleton (2001)

Australia

McLeod and Steel (1999)

United States of America Stapleton and Duncan (1998)

Botswana and South Africa

Kwerepe and Labuschagne (2003)

Australia

Potter et al. (1998)

United Kingdom

Lord et al. (2011)

Portugal

Aires et al. (2009)

India

Randhawa and Sharma (2007)

United States of America Monfort et al. (2007)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Brassica oleracea

Follow-up crop(s)

Not available

Not available

Green manure

Pratylenchus neglectus

Cardaria draba

Not available

Solanum tuberosum

Green manure

Globodera pallida

Eruca vesicaria sativa

Not available

Cucumis spp.

Green manure

Meloidogyne incognita

Eruca sativa

Cv Nemat

Vitis vinifera

Green manure

Meloidogyne javanica, Criconemoides xenoplax

Eruca sativa

Cv Nemat

Solanum tuberosum

Green manure

Globodera pallida

Eruca sativa

Cv Caliente

Solanum tuberosum

Green manure

Meloidogyne incognita

Eruca sativa

Cvs 8, 9, Nemat

Solanum tuberosum

Green manure

Globodera pallida

Eruca sativa

Not available

Solanum tuberosum

Green manure

Eruca sativa

Var. TMLC 2

Solanum lycopersicum

Soil amendment

Meloidogyne chitwoodi, Meloidogyne hapla, Paratrichodorus allius Meloidogyne incognita

Hesperis matronalis

Not available

Solanum tuberosum

Green manure

Globodera pallida

Lepidium latifolium

Not available

Solanum tuberosum

Green manure

Globodera pallida

Lepidium sativum

Not available

Solanum tuberosum

Green manure

Globodera pallida

Moricandia moricandioides Nasturtium officinale Nasturtium officinale Raphanus sativus

Not available

Solanum tuberosum

Green manure

Globodera pallida

Not available

Solanum tuberosum

Green manure

Globodera pallida

Not available

Solanum tuberosum

Green manure

Globodera rostochiensis

Cv Bento

Solanum tuberosum

Green manure

Globodera pallida

Raphanus sativus

Var. Boss

Cucumis spp.

Green manure

M. incognita

Raphanus sativus

Cvs Terranova, Doublet

Solanum tuberosum

Green manure

Meloidogyne incognita

Raphanus sativus

Cv Weedcheck

Solanum tuberosum

Green manure

Globodera pallida

Raphanus sativus

Cv Terranova

Not available

Green manure

Globodera pallida

Raphanus sativus

Cv Nemex

Solanum tuberosum Allium cepa

Green manure

Pratylenchus teres

Zeroe66% reduction in population levels 12% reduction in J2 population levels 98% reduction in nematode population (plastic cover was used in combination with biofumigation) Reduced Meloidogyne javanica and Criconemoidesxenoplax populations by 51 and 18% respectively No significant reduction in viable encysted eggs Increase in population levels 25e75% reduction in J2 population levels 99% reduction in nematode populations in greenhouse studies 50% reduction in root galling; increased seedling height by 22% and weight by 29% 2% reduction in J2 population levels 15% reduction in J2 population levels 10% reduction in J2 population levels 60% reduction in J2 population levels 95% reduction in J2 population levels 88% reduction in cyst formation Significant reduction in viable encysted eggs 98% reduction in population levels (plastic cover was used in combination with biofumigation) Increase in population levels Up to 100% reduction in J2 population levels and >95% reduction in viability of encysted eggs 50% reduction in cyst population 72% reduction in nematode population levels; 8% increase in tuber yield 72% reduction in nematode population levels; 6% reduction in onion yield

Australia

Potter et al. (1998)

United Kingdom

Lord et al. (2011)

France

Haroutunian (2013)

South Africa

Kruger et al. (2015) Kruger (2013)

United Kingdom

Ngala et al. (2014)

South Africa

Engelbrecht (2012)

United Kingdom

Lord et al. (2011)

United States of America Riga (2011)

India

Randhawa and Sharma (2007)

United Kingdom

Lord et al. (2011)

United Kingdom

Lord et al. (2011)

United Kingdom

Lord et al. (2011)

United Kingdom

Lord et al. (2011)

United Kingdom

Lord et al. (2011)

Portugal

Aires et al. (2009)

United Kingdom

Ngala et al. (2014)

France

Haroutunian (2013)

South Africa

Engelbrecht (2012)

United Kingdom

Lord et al. (2011)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Brassica rapa

United States of America Dossey (2010) The Netherlands

Hartsema et al. (2005)

27

(continued on next page)

28

Table 2 (continued ) Cultivar/variety/ selection

Follow-up crop(s)

Type of soil amendment

Target nematode pest genus and/or species

Effect on the target nematode pest

Raphanus sativus

Not available

Solanum tuberosum

Green manure

Meloidogyne chitwoodi, Pratylenchus neglectus

Raphanus sativus

Not available

Solanum tuberosum

Green manure

Meloidogyne chitwoodi, Pratylenchus neglectus

Raphanus sativus

Vitis vinifera

Green manure

Meloidogyne javanica

Raphanus sativus Raphanus sativus

Ssp. Oleiformis Cvs Adagio, SCO 7024, Nemex, Pegletta Not available Cv Trez

United States of America Hafez and Sundararaj 46% reduction in (2000) Meloidogyne chitwoodi population levels, but 107% increase in that of P. neglectus; 40% increase in tuber weight United States of America Al-Rehiayani et al. (1999) >29% increase in tuber mass; 58% reduction in Meloidogyne. chitwoodi J2 levels 48% reduction in P. neglectus populations Significantly reduced egg Australia McLeod and Steel (1999) production

Vitis vinifera Solanum tuberosum

Green manure Green manure

Meloidogyne javanica Meloidogyne chitwoodi race 2, Pratylenchus neglectus

Raphanus sativus

Not available

Solanum lycopersicum

Soil amendment

Meloidogyne incognita

Sisymbrium austriacum Sinapis alba

Not available

Solanum tuberosum

Green manure

Globodera pallida

Cv Braco

Vitis vinifera

Green manure

Meloidogyne javanica, Criconemoides xenoplax

Sinapis alba

Cv Ida Gold

Not available

Seed meal

Sinapis alba

Cv Zlata

Solanum tuberosum

Green manure

Meloidogyne incognita, Pratylenchus penetrans Globodera rostochiensis, other herbivores

Sinapsis alba

Cv Kikarashi

Arctium lappa

Green manure

Pratylenchus penetrans

Sinapis alba

Not available

Solanum tuberosum

Green manure

Globodera pallida

Sinapis alba

Cv Ida Gold

Capsicum annuum

Seed meal

Meloidogyne incognita

Sinapis alba

Cv Ida Gold

Pyrus malus

Seed meal

Pratylenchus penetrans

Sinapis alba

Not available

Solanum tuberosum

Green manure

Pratylenchus sp., Trichodorus sp., Paratrichodorus sp.

Sinapis alba

Cv Metex

Not available

Trap crop

Sinapis alba

Cv Maxi

Vitis vinifera

Green manure

Globodera pallida and G. rostochiensis (mixed population) Meloidogyne javanica

No effect on egg production 79e94% reduction in Meloidogyne chitwoodi populations but no effect on Pratylenchus neglectus populations 47% reduction in root galling 45% reduction in J2 population levels 51% reduction in Meloidogyne javanica population levels, but no effect on Criconemoides xenoplax 90% suppression of both PPN No effect on cyst population levels, hatching and infectivity of J2 but generally reduced a range of herbivore population levels Increased 14e57% nematode population 65% reduction in J2 population levels >74% reduction in population levels 2863% reduction in population levels Increase population levels by 50% of Pratylenchus while 100% increase in the population of Trichodoridae 16% reduction of J2 in cysts levels

Country

Reference

Australia McLeod and Steel (1999) United States of America Al-Rehiayani and Hafez (1998)

United States of America Stapleton and Duncan (1998) United States of America Lord et al. (2011) South Africa

Kruger (2013) and Kruger et al. (2015)

United States of America Zasada et al. (2009) Belgium

Valdes et al. (2012)

Japan

Sakuma et al. (2011)

United Kingdom

Lord et al. (2011)

United States of America Meyer et al. (2011) United States of America Mazzola et al. (2007, 2009) The Netherlands

Hoek et al. (2006)

The Netherlands

Scholte and Vos (2000)

Significant reduction in egg Australia production

McLeod and Steel (1999)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Brassicaceae species used as a management tool

H. Fourie et al. / Crop Protection 80 (2016) 21e41

29

Table 3 The host status of various Brassicaceae crops to various plant-parasitic nematode species. Brassicaceae species Genotype

Target nematode pest species/race

Country

Reference

United States Ringer et al. of America (1987) Italy Curto et al. (2005) Australia Hay et al. (2014) Australia Hay et al. (2014)

Good host poor-/non host Aubrieta deltoidea

Not available

Cv upland cress

Heterodera zeae

Barbarea verma

Not available

Sel. ISCI 50

Meloidogyne incognita

Brassica spp.

Cvs.Bouncer, Subzero

Brassica spp.

Cvs.Bouncer, Subzero

Brassica spp.

Not available

Brassica campestris

Cv.BFTap

Cvs Bruxelas and Tronchuda Portuguesa

Meloidogyne Meloidogyne Meloidogyne Meloidogyne Meloidogyne Meloidogyne

javanica, hapla fallax, arenaria, incognita javanica

Brazil

Brassica campestris

Subsp. Pekinensis Cv Tokat-2

Not available

Meloidogyne javanica, Meloidogyne hapla Meloidogyne fallax, Meloidogyne arenaria, Meloidogyne incognita Heterodera cruciferae

Brassica campestris

Not available

Meloidogyne incognita

Egypt

Brassica campestris

Cvs. Hanna, Semu DNK, Tower, Semu 240/84, Lirasol, Duplo and Global Not available

Var. Tori

Nepal

Brassica carinata

Not available

Cv Bc007

Meloidogyne incognita and Meloidogyne javanica Meloidogyne javanica and Meloidogyne hapla Meloidogyne fallax, Meloidogyne javanica, Meloidogyne arenaria, Meloidogyne hapla, Meloidogyne incognita Rotylenchulus reniformis

Brassica campestris

Cv.BFTap

Brassica carinata

Cv. BFBCa

Brassica chinensis

Cv LV35

Not available

Brassica chinensis

Var. Pekinensis

Not available

Brassica juncea

Cv ISCI99, Nemfix

Not available

Meloidogyne arenaria race 1, Meloidogyne incognita races 1 and 3 and Meloidogyne javanica Meloidogyne javanica

Brassica juncea

Not available

Cv Nemat

Meloidogyne incognita

Brassica juncea

Not available

Cv Pusa Bold

Heterodera zeae

Brassica juncea Brassica juncea

Cvs. LV 1768, LV 2597 Sel. ISCI 20

Not available Not available

Rotylenchulus reniformis Meloidogyne incognita

Brassica juncea

Var. Curly

Not available

Meloidogyne hapla

Brassica juncea and Sinapis alba mixture Brassica napus

Cvs Caliente 61, Caliente 99

Not available

Meloidogyne arenaria, Meloidogyne incognita, Meloidogyne javanica

Not available

Cv Winfred

Meloidogyne hapla

Brassica napus

Cv.BFStr

Brassica napus Brassica napus

Cv.BFStr Cv.Goliath

Brassica napus

Cv.Goliath

Brassica napus Brassica napus

Cvs. Candle, PF 2/85, Golda Not available

Not available Var Giant English

Brassica napus

Not available

Brassica napus

Cv Can 420

Cvs. Crusher, Gladiator, Hudson, HyClass 601, Hylite, Marksman, Patriot, Proseed 2013, Rider, Skyhawk Not available

Brassica napus

Cvs. Beluga, Bambin, Belcanto, Betty, Hydromel and Standing

Brassica napus

Not available Cvs Hyola, Rainbow Not available

Brassica napus

Meloidogyne javanica, Meloidogyne hapla, Meloidogyne incognita Meloidogyne fallax, Meloidogyne arenaria Meloidogyne javanica, Meloidogyne hapla Meloidogyne fallax, Meloidogyne arenaria, Meloidogyne incognita Meloidogyne incognita Pratylenchus zeae, Xiphinema elongatum Heterodera glycines

Australia

Rosa et al. (2013) Hay et al. (2014) Hay et al. (2014)

Australia

Turkey

Aydinli and Menan (2012) Ismail (2011)

Bhardwaj and Hogger (1984) United States Edwards and of America Ploeg (2014) Australia Hay et al. (2014)

Indonesia

Marwoto (2010) United States McSorley and of America Frederick (1995) United States Edwards and of America Ploeg (2014) South Africa Engelbrecht (2012) India Srivastava and Jaiswal (2011) Indonesia Marwoto (2010) Italy Curto et al. (2005) Brazil Carneiro et al. (2000) United States Kokalis-Burelle of America et al. (2013) United States Edwards and of America Ploeg (2014) Australia Hay et al. (2014) Australia Hay et al. (2014) Australia Hay et al. (2014) Australia Hay et al. (2014) Egypt Ismail (2011) South Africa Berry et al. (2011) United States Poromarto and of America Nelson (2010)

Meloidogyne ethiopica

Brazil

Not available

Heterodera schachtii

Belgium

Cvs Hyola, Rainbow Not available Cv Dwarf Essex

Meloidogyne sp. Pratylenchus sp. Rotylenchulus reniformis

South Africa

Lima et al. (2009) Kazlauskaites and Coosemans (2009) Nel et al. (2008) Wang et al. (2003)

(continued on next page)

30

H. Fourie et al. / Crop Protection 80 (2016) 21e41

Table 3 (continued ) Brassicaceae species Genotype

Target nematode pest species/race

Country

Reference

Good host poor-/non host

Brassica napus

Cv HL99

Not available

Pratylenchus penetrans

Brassica napus

Not available

Cv Dwarf Essex

Rotylenchulus reniformis

Brassica napus

Not available

Cv Humus

Meloidogyne chitwoodi race 2

Brassica napus

Cv Humus

Not available

Pratylenchus neglectus

Brassica napus

Not available

Brassica napus

Ssp. Oleiferas cvs. Bridger, Gorzanski, H-47, Lindora and Viking Ssp. Oleiferas Cvs. Bridger, Gorzanski, Not available H-47, Lindora and Viking

Heterodera glycines and Pratylenchus scribneri

Cv Liberty

Meloidogyne incognita, Meloidogyne hapla and Helicotylenchus pseudorobustus Meloidogyne incognita

Brassica oleracea

Cv.Aurora, Bridge, Boris, Virgin

Meloidogyne hapla, Meloidogyne javanica Meloidogyne incognita

Brassica oleracea

Cv.Bridge

Meloidogyne hapla

Brassica oleracea

Not available

Brassica oleracea

Cv.Aurora, Boris, Virgin

Brassica oleracea

Var. Acephala Cv's OR-37, OR-46, Heterodera cruciferae T-20, T-4; Var. Capitata subvar. Alba Cv's 524C, 241C, 145C, 166T, 519C, 542C, 144C, 165C, 508C, 148C, 115T and 530T

United States of America Canada Belair et al. (2002) United States Wang et al. of America (2001) United States Al-Rehiayani of America and Hafez (1998) United States Al-Rehiayani of America and Hafez (1998) United States Bernard and of America Montgomery (1993) United States Bernard and of America Montgomery (1993) United States Edwards and of America Ploeg (2014) Australia Hay et al. (2014) Australia Hay et al. (2014) Australia Hay et al. (2014) Turkey Aydinli and Menan (2012)

Not available

Meloidogyne hispanica

Portugal

Brassica oleracea

Var. Acephala Cvs. OR-49, OR-51, S-6, Karadeniz, OR-38, OR-39; Var. Capitata subvar. Rubra Cvs. Mohrenkopf, Uludag; Var. convar. Oleraceae, Gemmifera Cv Star F1 Var. Botrytis Cv Temporao; Var. Capitata Cvs. Tronchuda Portuguesa, Coracao de boi, Bacalan; Var. Italic Cv Verde Not available

Var. Capitata, Italic, Botrytis

Meloidogyne incognita

Pakistan

Brassica oleracea

Not available

Var. Rotan

Rotylenchulus reniformis

Brassica oleracea

Not available

Cv Liberty

Meloidogyne incognita

Brassica oleracea

Not available

Meloidogyne enterolobii (¼Meloidogyne mayaguensis)

Brassica oleracea

Cv Florida BroadLeaf; Var. Botrytis Cv Waltham; Var. Acephala, Esculenta Cv Dwar Blue Curled Scotch

Not available.

Meloidogyne incognita

Brassica oleracea Brassica oleracea

Not available Not available

Brassica oleracea

Var. Capitata, Acephala, Botrytis Cvs. Flat dutch, Jersey wakefield, Bonanza, Red rock and Earliest stone head Not available

Var. Capitata Cvs. Earliest of all sovoy, Danish ball head, Triumph, Rochas triumph, Summer head, Green Monster, Sutton's best of all savoy, Kalimpong eclipse drum head, Elizabeth, Sutton's earliest, Red cabbage, Aligarth local, Verma's pride, Drum head, Kalimpong English ball Not available Var. Capitata Cvs. Danish ball head, Triumph, Summer head, Green Monster, Sutton's best of all savoy, Kalimpong eclipse drum head, Elizabeth, Sutton's earliest, Red cabbage, Aligarth local, Verma's pride Not available Cvs. Danish Ball Head, Triumph, Summer head, Green monster, Sutton's best of all savoy, Elizabeth, Sutton's earliest, Red cabbage, Aligarh local

Rotylenchulus reniformis Meloidogyne arenaria race 2; Meloidogyne incognita races 1 and 2; M. javanica races 1 and 2 Meloidogyne incognita races 1 and 2 India

Brassica oleracea

Brassica oleracea

Brassica oleracea

Maleita et al. (2012)

Anwar and Mckenry (2010) Indonesia Marwoto (2010) United States Lopez-Peres of America et al. (2010) United States Brito et al. of America (2007) United States of America India India

Monfort et al. (2007) Khan (2005) Khan et al. (2002) Khan et al. (2002)

Meloidogyne javanica races 1 and 2

India

Khan et al. (2002)

Meloidogyne arenaria race 2

India

Khan et al. (2002)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

31

Table 3 (continued ) Brassicaceae species Genotype

Target nematode pest species/race

Country

Reference

Machado and Inomoto (2001) Carneiro et al. (2000)

Good host poor-/non host Brassica oleracea

Not available

Var. Capitata Cv Chato de Brunswich

Pratylenchus brachyrus

Brazil

Brassica oleracea

Not available

Meloidogyne incognita race 3

Brazil

Brassica oleracea

Not available

Var. Acephala, Manteiga, Botrytis, Teresopolis giante Var. Acephala, Manteiga

Brazil

Carneiro et al. (2000)

Brassica oleracea

Not available

Brazil

Not available

Meloidogyne hapla

Brazil

Carneiro et al. (2000) Carneiro et al. (2000)

Brassica oleracea

Var. Captata, Hibrido Sekai, Coracao de Boi Var. Captata, Hibrido Sekai, Coracao de Boi, Botrytis, Teresopolis giante, Bola de Neve Not available

Meloidogyne Meloidogyne Meloidogyne Meloidogyne

Var. Botrytis Cvs. De Cicco, Georgia southern

Meloidogyne incognita races 1 and 3

Brassica oleracea

Not available

Var. Acephala Cv Georgia Southern

Meloidogyne arenaria race 1 and Meloidogyne javanica

Brassica oleracea

Not available

Var. Botrytis Cv De Cicco

Meloidogyne arenaria race 1

Brassica oleracea

Not available

Meloidogyne arenaria race 1; Meloidogyne incognita races 1 and 3 and Meloidogyne javanica Belonolaimus longicaudatus

Brassica oleracea

Var. Botrytis Cv Early Snowball; Var. Capitata Cv Copenhagen Early market Var. Capitata Cvs. Olympic, Genesis, Salto, Rio verde, Solid blue 780, Fortuna, Solid blue 770, Solid blue 760, Little rock, Impra, Krautman, Prime time, Gourmet, Green garden, Vorox, Comas, Field support, Minstrel, Tenoro and Albadan Not available

United States McSorley and of America Frederick (1995) United States McSorley and of America Frederick (1995) United States McSorley and of America Frederick (1995) United States McSorley and of America Frederick (1995) United States White and of America Rhoades (1992)

Brassica oleracea

Brassica oleracea

Brassica oleracea

Var. Capitata Cv Bravo, Superlite, Florida 33, Green cup, Grand Slam, Krautman, Izalco, Blue Pak and PSR 57684

arenaria race 2; javanica; hapla arenaria race 2

Heterodera zeae

United States Ringer et al. of America (1987)

Not available

Cvs. Dwarf Siberian, Green Comet, Snow Crown, Market Prize, Prince Marvel Var. Capitata, Botrytis, Italic

Meloidogyne javanica

Nepal

Brassica oleracea

Not available

Cv Botrytis

Hemicriconemoides mangiferae

Brassica rapa

Not available

Meloidogyne incognita Meloidogyne hapla

Brassica rapa

Cvs Br02206, Rondo Cvs Br02005, Br02006, Rondo and Samson Not available Var ATR Hyden

Var ATR Hyden

Brassica rapa

Cv Norfolk

Not available

Brassica rapa

Cv Seven top

Not available

Pratylenchus zeae, Paratrichodorus minor Xiphinema elongatum Meloidogyne arenaria race 2; Meloidogyne incognita race 1 and Meloidogyne javanica Belonolaimus longicaudatus

Brassica rapa

Not available

Brassica rapa

Cvs. Purple top white globe, Nabo, Nabo seven top Not available

Cv Purple-Top white globe

Meloidogyne arenaria race 1; Meloidogyne incognita races 1 and 3 and Meloidogyne javanica Heterodera zeae

Capsella bursa

Not available

Cv Pastoris

Heterodera zeae

Eruca sativa

Not available

Cv Nemat

Meloidogyne javanica

Eruca sativa

Not available

Cv Nemat

Eruca sativa

Not available

Cv Nemat

Meloidogyne incognita and Meloidogyne javanica Meloidogyne hapla

Eruca sativa

Not available

Cv Nemat

Eruca sativa

Cv Caliente

Not available

Meloidogyne Meloidogyne Meloidogyne Meloidogyne

Eruca sativa

Not available

Cv Nemat

Meloidogyne hapla

arenaria, incognita, javanica incognita

Bhardwaj and Hogger (1984) Pakistan Saeed and Ghaffar (1982) United States Edwards and of America Ploeg (2014) South Africa

Berry et al. (2011)

Spain

Liebanas and Castillo (2004)

United States of America United States of America

Bekal and Becker (2000) McSorley and Frederick (1995) Ringer et al. (1987) Ringer et al. (1987) Kruger et al. (2015) Edwards and Ploeg (2014) Melakeberhan et al. (2006) Kokalis-Burelle et al. (2013)

United States of America United States of America South Africa United States of America United States of America United States of America South Africa

Engelbrecht (2012) United States Melakeberhan of America et al. (2010) (continued on next page)

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H. Fourie et al. / Crop Protection 80 (2016) 21e41

Table 3 (continued ) Brassicaceae species Genotype

Target nematode pest species/race

Country

Italy

Reference

Good host poor-/non host Eruca sativa

Not available

Cv Nemat

Meloidogyne incognita

Lepidium campestre

Sel. ISCI 103

Not available

Meloidogyne incognita

Raphanus sativus

Not available Not available Cvs Adiago, Condor and Nemat

Meloidogyne incognita Meloidogyne javanica Meloidogyne hapla

Raphanus sativus

Cvs Terranova, Doublet

Cvs Adagio, Boss, Colonel, Comet, Defender and TerraNova Cvs Boss, TerraNova and Defender Cvs Colonel, Doublet, Final and TerraNova Not available

Raphanus sativus

Not available

Cv Pusa Chetki

Heterodera zeae

Raphanus sativus

Var. longipinnatus

Not available

Rotylenchulus reniformis

Raphanus sativus

Not available

Var. Oleiferus Cv IPR 116

Meloidogyne ethiopica

Raphanus sativus

Not available

Cv Siletina

Rotylenchulus reniformis

Raphanus sativus

Cv Scarlet Globe, White Icicle

Not available

Meloidogyne incognita

Raphanus sativus

Not available

Meloidogyne arenaria (NQ1), Meloidogyne arenaria race 2 (NQ5/7) and Meloidogyne javanica (NQ2)

Raphanus sativus Raphanus sativus

Not available Not available

Cvs. Nemex, Ultimo, Adagio, Colonel, Dacapo, Fortissimo, French breakfast, Idaho, Long Scarlet, Pegletta, Phpsal, Phptrze, Phpzg, Salad crunch, White icicle, Weedcheck Cv Adagio Cv Boss

Ditylenchus dipsaci Meloidogyne incognita

Germany Italy

Raphanus sativus

Not available

Heterodera schachtii

Raphanus sativus

Cv Cherry Belle

Cvs. Adagio, Arena, Colonel, Commodore, Rimbo Not available

Belonolaimus longicaudatus

Raphanus sativus

Not available

Meloidogyne hapla

Raphanus sativus

Var. Crison Gigante, Scarlet Globe Not available

United States of America United States of America Brazil

Cv Essex

Xiphinema sp.

Raphanus sativus

Cv Cherry belle

Not available

Raphanus sativus

Not available

Raphanus sativus

Var. Oleifera Cvs. Adagio, Nemex, Pegletta, Renova, Siletina, Siletta Nova and Ultimo Not available

Meloidogyne arenaria race 1; Meloidogyne incognita races 1 and 3 and Meloidogyne javanica Meloidogyne incognita and Meloidogyne javanica

Raphanus sativus

Meloidogyne incognita

Curto et al. (2005) Italy Curto et al. (2005) United States Edwards and of America Ploeg (2014)

South Africa

Engelbrecht (2012) India Srivastava and Jaiswal (2011) Indonesia Marwoto (2010) Brazil Lima et al. (2009) Brazil Asmus et al. (2008) United States Monfort et al. of America (2007) Australia Pattison et al. (2006)

United States of America United States of America

Knuth (2006) Curto et al. (2005) Smith et al. (2004) Bekal and Becker (2000) Carneiro et al. (2000) Halbrendt (1996) McSorley and Frederick (1995)

United States Gardener and of America Caswell-Chen (1994)

Meloidogyne chitwoodi race 1

United States Ferris et al. of America (1993)

Not available

Cvs. 4, Nemex, 3, Siletta Nova, Siletena, Pegletta, 6, 2, 5 and oilseed rape Cvs Renova, Pegletta, Nemex

Heterodera schachtii

Raphanus sativus

Not available

Cv Scarlet globe

Heterodera zeae

Rorripa rugosum

Not available

Sel. ISCI 15

Meloidogyne incognita

United States of America United States of America Italy

Rorripa nasturtium

Not available

Var. Spicy dry

Rorripa nasturtium

Var. Spicy dry

Not available

Meloidogyne arenaria race 2; Meloidogyne incognita race 3 and Meloidogyne javanica Meloidogyne hapla

Sinapis alba

Not available

Abraham

Meloidogyne incognita

Sinapis alba

Cv Pacific Gold

Not available

Meloidogyne incognita

Sinapis alba

Not available

Cvs. Tilney, Metex

Meloidogyne arenaria (NQ1) and Meloidogyne arenaria race 2 (NQ5/7); Meloidogyne javanica (NQ2)

Brazil

Brazil

Gardner et al. (1992) Ringer et al. (1987) Curto et al. (2005) Carneiro et al. (2000)

Carneiro et al. (2000) United States Edwards and of America Ploeg (2014) United States Monfort et al. of America (2007) Australia Pattison et al. (2006)

H. Fourie et al. / Crop Protection 80 (2016) 21e41

33

Table 3 (continued ) Brassicaceae species Genotype

Target nematode pest species/race

Country

Reference

Ditylenchus dipsaci Heterodera schachtii

Germany United States of America United States of America United States of America

Knuth (2006) Smith et al. (2004) Al-Rehiayani and Hafez (1998) McSorley and Frederick (1995)

Good host poor-/non host Sinapis alba Sinapis alba

Cvs. Concerta, Hohenheimer Not available

Sinapis alba

Cv Martegina

Not available Cvs. Concreta, Metex, Rivona, Salvo, Serval and Vertus Not available

Sinapis alba

Cv Florida broad leaf

Not available

Sinapis alba

Cvs. Albatross, Emergo, Maxi, Martigena, Metex

Not available

Sinapis alba

Not available

Cv Emergo

Heterodera schachtii

Sisymbrium irio sp.

Not available

Not available

Belonolaimus longicaudatus

on listing the outcomes of using various Brassicaceae crops in cropping systems through the implementation of different approaches/strategies as an option(s) to manage economically important nematode pests. Information was obtained mainly by means of internet-based search engines during which 187 papers, mainly including peer-reviewed articles, but also theses of postgraduate students and institutional reports, were accessed. It is important to bear in mind that nematode population levels differed substantially (from low to exceptionally high) in experiments from which data were listed in this article. This scenario should particularly take into account where reductions in nematode-pest populations are indicated in Table 2. Also, approximate estimations of such reductions in nematode-pest populations had to be calculated by the authors of this article in some cases where mean nematode numbers were not supplied in tables but only demonstrated in graphs in the articles accessed.

Pratylenchus neglectus and Meloidogyne chitwoodi race 2 Meloidogyne arenaria race 1; Meloidogyne incognita races 1 and 3 and Meloidogyne javanica Meloidogyne incognita and Meloidogyne javanica

United States Gardener and of America Caswell-Chen (1994) United States Gardner et al. of America (1992) United States Bekal and of America Becker (2000)

2.1. Mechanisms of Brassicaceae spp. to manage PPN Research on the use of Brassicaceae crops, their residues and breakdown products that act as bionematicides commenced in the 1930s (Smedley, 1939). Nowadays Brassicaceae crops are still attracting renewed interest primarily because of their pest management characteristics and especially their use as an alternative to toxic nematicides that are progressively being phased out of use due to animal, human and environmental concerns. Brassicaceae crops are particularly renowned for their i) biofumigation effects as a result of slashing and incorporation of aerial plant parts into the upper soil layers as soil amendments (green manures and seed meals) (Table 2) (Cardoza and Stewart, 2004) as well as ii) the poorhost status of several species that are used as cover- and/or rotation crops to reduce various nematode pest population levels (Table 3). 2.2. Biofumigation and the role of GSL-degradation products

2. The family Brassicaceae Brassicaceae crops are generally cool weather crops with a temperature optimum that varies between 14 and 21  C and minimum and maximum temperatures between 4 and 30  C depending on the variety (Bjorkman et al., 2011). Brassicaceous crops are thus produced in both temperate regions and in the colder areas or at high altitudes in tropical and subtropical regions. They generally prefer deep, well-drained, fertile, friable, sandy or silty loam soils and an approximately neutral pH (Dixon, 2007). The family Brassicaceae (Cruciferae) consists of 350 genera and approximately 3,500 species, including the genera Arabidopsis, Brassica, Camelina, Crambe, Raphnus, Sinapis and Thlaspi (AbuGhannam and Jaiswal, 2014; Fratianni et al., 2014). The genus Brassica is economically the most important one within the Brassicaceae family since it provides edible buds, flowers, leaves, roots, seeds and stems (Weerakoon and Somaratne, 2011). Brassica spp. are generally classified in three groups, viz coles, mustards and rape seeds. The B. oleracea genus represents cole crops such as vegetables and the oilseeds, while the mustard group includes species such as B. juncea, B. nigra and B. carinata. The rape seeds group includes B. campestris and B. napus (Weerakoon and Somaratne, 2011), representing valuable sources of edible oils and proteins (Raymer, 2002). The Brassica genus also contains several weedy species of which the most important is B. rapa (Holm et al., 1997) predominantly used for animal feed. Other Brassicaceae genera listed are Raphanus that provides edible tubers and Sinapis constituting an important source of condiments (Sridevi and Sarla, 2005).

Potential modes-of-action of Brassicaceae crops against PPN include the production of nematotoxic GSL-degradation products, viz. ITCs, thiocyanates, nitriles or oxazolidinethiones (Lazzeri et al., 1993; Sarwar et al., 1998; Zasada and Ferris, 2003), stimulation of antagonistic microbial communities in amended soil and the production of nitrogenous compounds that are toxic to nematodes (Cohen et al., 2005; Kirkegaard and Matthiessen, 2004; Larkin and Griffin, 2007; Van Dam et al., 2009). Such GSL-degradation products are formed as a result of the hydrolization of sulphurcontaining secondary metabolites by the enzyme myrosinase (stored separately in plant cells) to yield nitriles, epithionitriles and thiocyanates (Borgen et al., 2012). To optimise ITC release from aerial parts of Brassicaceae crops, the plant cells of such parts must be slashed/ruptured/damaged effectively and immediately be incorporated into the soil. Such actions are recommended to be done when ITC levels are at their highest in aerial plant parts of Brassicaceae crops, usually during flowering (Gimsing and Kirkegaard, 2006). GSLs are characteristic of the order Capparales, which is primarily represented by the family Brassicaceae (Bjorkman et al., 2011), but are also present in genera within the Capparaceae and Caricaceae families (Fahey et al., 2001). However, Brassicaceae crops are the most popular ones that are generally used for biofumigation due to the relatively high GSL contents. Such crops include B. oleracea (broccoli, Brussels sprouts, cabbage, cauliflower), B. oleracea acephala (kale), B. napus (canola and rape seed), B. rapa (turnip), R. sativus (radish) and a variety of mustards such as B. juncea (Indian mustard) and S. alba (white mustard) (Bennet et al., 2006). Other

34

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Brassica crops that produce GSLs are Alliaria petiolata (garlic mustard), Arabidopsis thaliana (thale cress), B. campestris (Chinese cabbage), B. rapa (turnip), B. carinata (Ethiopian mustard), Brassica fruticulosa (Mediterranean cabbage), B. nigra (black mustard), Cardamine cordifolia (Heartleaf bittercress), Cardamine diphylla (pepper root), Diplotaxis tenuifolia (perennial wall-rocket), E. sativa (salad rocket), L. sativum, (garden cress) and Thlaspi arvense (field penny-cress) (Karavina and Mandumbu, 2012). More than 200 GSLs have been identified mainly from plants in the Brassicaceae family (Ishida et al., 2014; Lelario et al., 2012) and are contained in seeds and vegetative bodies of cultural and wildgrowing species (Kirkegaard and Sarwar, 1998; Solov'yeva et al., 2013). The majority of these GSLs are unique for certain Brassicaceae genera and species in terms of their chemical characteristics (Ahuja et al., 2010; Avato et al., 2013; Padilla et al., 2007; Zasada and Ferris, 2004). Three major groups of GSLs have been reported, namely aliphatic, aromatic and indole forms, (Padilla et al., 2007; Zasada and Ferris, 2004) with sinigrin usually being the predominant GSL being identified from Brassicaceae plants (Gruver et al., 2010). Although GSL levels within Brassicaceae plants are genetically determined, the types and quantities of GSL vary between individual plant species, plant organs, developmental stages and environmental factors such as drought, sulphate and nitrogen nutrients, season and the diurnal cycle (Larkin and Griffin, 2007; Winde and Wittstock, 2011) as well as availability of sulphur in the soil (De Pascale et al., 2007). The canola cv Hyola 401 for example contains low levels of GSLs, while rape seed cv Dwarf Essex, turnip cv Purple Top and yellow mustard cv Ida Gold exhibit moderate levels (Kruger et al., 2013). Also, an undisclosed Indian mustard cv exhibits high GSL levels according to Larkin and Griffin (2007). Sang et al. (1984), furthermore reported that a single Brassicaceae species can also contain several different types of GSLs. Moreover, Kirkegaard and Sarwar (1998) reported diversified profiles, concentrations and production of GSL within and between Brassicaceae spp. when they were grown in the same environment. According to Bellostas et al. (2004) the growth stage of Brassicaceae crops as well as the amount of biomass slashed and incorporated into the soil are the two main factors that contribute towards the success obtained with biofumigation. Furthermore, the Brassicaceae crop that is planted and its adaptability to the environment also affect the efficacy of biofumigation (Monfort et al., 2007). The toxicity of a range of ITC compounds on plant-parasitic nematode species has been tested in vitro by various researchers (Buskov et al., 2002; Lazzeri et al., 1993, 2004; Potter et al., 1998; Schroeder and MacGuidwin, 2010; Zasada and Ferris, 2003, 2004; Zasada et al., 2009) with high efficacy being obtained but will not be discussed here since this article focuses on the practical application of biofumigants in the soil substrate. Seed meals of Brassicaceae crops have also been investigated for their effects on nematode pests (Table 2). Instead of growing green manure crops for the management of nematode pests, seed meals can be easily spread and incorporated into soil with no risk of frost damage as is the case for green manure crops (Rahman and Somers, 2005). In addition, seed meals cannot serve as hosts to PPN as can the roots/tubers of cover crops. Ultimately, seed meals can be applied to coincide with population build-ups of PPN and their use this way be optimized to combat such pests. However, disadvantages of using Brassicaceae seed meals as an option to manage PPN are their limited availability and cost (Rahman and Somers, 2005). 3. Effects of biofumigation During the past few decades, progress has been made in understanding how to maximize the efficacy of biofumigation by using Brassicaceae crops. This has led to renewed interest in their

role in controlling soil-borne nematode pests (Morra and Kirkegaard, 2002). It has been demonstrated by various researchers that biofumigation leads to the significant reduction of various economically important nematode pest populations and the symptoms they cause to crops, with subsequent increases in yield/quality of such crops (Table 2). Although the major body of research done in this regard focused on species of Globodera, Meloidogyne and Pratylenchus (Valdes et al., 2012), this review also includes literature on other economically important nematode pests such as Beloinolaimus longicaudatus, Criconemoides xenoplax, Ditylenchus dipsaci, Hemicriconemoides mangiferae, Paratrichodorus minor, Rotylenchulus reniformis and Xiphinema elongatum (Tables 2 and 3). The effect of biofumigation on non-target, beneficial nematodes is also referred to in this article. 3.1. Root-knot nematodes The number-one rated plant-parasitic nematode genus Meloidogyne (Jones et al., 2013) has been the target nematode pest in the majority of biofumigation experiments that were done on a global scale (Table 2). Biofumigation resulting from numerous Brassicaceae spp. green-manure amendments resulted in variable levels of reduction of root-knot nematode population and in most cases subsequent increases in crop/plant parameters (i.e. yield, quality and others) (Table 2). For example, Meloidogyne incognita root gall levels as low as 8% were recorded after use of B. napus soil amendments prior to growing tomato in India (Randhawa and Sharma, 2007). In contrast, up to 88% and 100% reductions were recorded in M. incognita popultion levels after B. oleracea green manure amendments were applied before tomato was planted in the US and Egypt, respectively (Stapleton and Duncan, 1998; Youssef and Lashein, 2013). For the Javanese root-knot nematode, Meloidogyne javanica, reduction in population levels using greenmanure amendments as a biofumigation tactic was recorded as ranging between 14 to an ultimate 100% when applied in vineyards in South Africa and pepper fields in the US, respectively (Kruger, 2013; Johnson et al., 1992). From Australia, McLeod and Steel (1999) also reported significant reductions in egg production of M. javanica in vineyards using green manures of four R. sativus cultivars and one S. alba cultivar. Focussing on Meloidogyne chitwoodi, population-level reductions recorded in the US ranged between >29 and 94% (Riga, 2011) and up to 99% in potato fields (AlRehiayani et al., 1999), while it was recorded to be between 89 and 98% in tomato plantings (Mojtahedi et al., 1991). Furthermore, oil radish amendments decreased M. chitwoodi densities by 46% in the US before potato was grown (Hafez and Sundararaj, 2000). From Brazil, population-level reductions of the emerging nematode pest Meloidogyne enterolobi (Jones et al., 2013), ranging between 95 and 98%, were reported using leaf and seed meal of B. juncea in tomato fields (Oliveira et al., 2011). By using B. oleracea for its biofumigation effect, Masheva et al. (2012) also reported a 71% reduction in Meloidogyne arenaria population levels in Bulgaria, while a 99% reduction in population levels of Meloidogyne hapla, was noted by Riga (2011) using E. sativa as a green manure in the US. Conversely to the successful management of root-knot nematodes, Engelbrecht (2012) reported no reduction in M. incognita numbers in soil after biofumigation with green manures of B. juncea (cv Nemat), R. sativus (cvs. Terranova and Doublet) and E. sativus (cv Caliente). In fact, population levels of M. incognita were 115% higher in roots of potato at tuber initiation in plots where aerial parts of cv Caliente was used for its biofumigation action compared to that of the untreated control. It must, however, be borne in mind that a potato crop was also planted during the previous season at this site, resulting in very high M. incognita infestation levels (approximately

H. Fourie et al. / Crop Protection 80 (2016) 21e41

25,000/50g potato tuber). From The Netherlands it was also reported that using oil radish used as a green-manure crop, no reduction in M. chitwoodi population levels was achieved (Runia et al., 2006).

35

levels when B. juncea green manures were used as soil amendments in Japan. From the US, Al-Rehiayani and Hafez (1998) reported no reduction in P. neglectus populations using B. napus (cv Humus) and R. sativus (cv Trez) green-manure biofumigants in potato experiments.

3.2. Cyst nematodes 3.4. Other economically important nematode pests For the second most important rated nematode pest genera Globodera and Heterodera, population levels of the damaging Globodera pallida (Jones et al., 2013) have been reduced from a low 2 to 100% in the UK (Lord et al., 2011). This was achieved after using aqueous leaf extracts, seed meals and/or green manures of various Brassicaceae spp. The latter author also reported close to 100% reduction in the viability of encysted eggs of G. pallida. Ngala et al. (2014) also recently confirmed the efficicay of biofumigation using B. juncea and R. sativus green manures since significant reductions in C. pallida encysted egg populations in soils were recorded at a research experiment in the UK. With regard to the golden potato cyst nematode Globodera rostochiensis, up to 88% reduction in cyst population levels has been reported by using green manures of selected Brassicaceae crops in Portugal (Aires et al., 2009). For Heterodera spp., reductions in population levels that ranged between 40 and 100% were reported from Kenya by Kago et al. (2013) using soil amendments of B. oleracea. Also, a 46% reduction in the number of viable cysts of Heterodera carotea was reported using seed meal of B. juncea as a biofumigant in Denmark (Grevsen, 2010), while high toxicity and anti-hatching effects were recorded for Heterodera glycines and Heterodera schachtii using seed meal and bran of B. juncea as a similar tactic (Yu et al., 2007). When B. juncea leaf and seed meals were used as biofumigants by Oliveira et al. (2011), up to 98% mortality of H. glycines cysts in soils in Brazil were recorded. In contrast to the reported successes of reducing cyst nematode populations using Brassicaceae soil amendments, Valdes et al. (2012) reported no effect of using S. alba cv Zlets as a green manure biofumigant to manage G. rostochiensis in Belgium. 3.3. Lesion nematodes Resulting from the application of biofumigation with Brassicaceae soil amendments, various authors reported substantial reductions in population levels of various species of the overall thirdrated economically most important Pratylenchus genus (Table 2). In a Kenyan study, Kago et al. (2013) for example recorded 40e100% lower Pratylenchus sp. population levels after using soil amendments of B. oleracea prior to planting vegetable crops. In addition, Mazzola et al. (2009) demonstrated a similar trend with 56 and 72% reductions in population levels of Pratylenchus sp. being recorded using B. juncea seed meal as a soil amendment in apple orchards in the US. In another apple-research study in the US, Cohen et al. (2005) recorded up to 76% lower Pratylenchus sp. numbers in soils. With regard to Pratylenchus penetrans population levels, using B. napus and S. alba as seed-meal biofumigants resulted in <30% to 50 and 63% reductions in population levels in apples in the US (Mazzola et al., 2007, 2009). Ultimately, more than a 90% reduction in P. penetrans numbers was reported in the latter study using B. juncea seed meals. Yu et al. (2007) also reported substantial decreases ranging from 66 to 74% in P. penetrans numbers when B. juncea seed meal and bran soil amendments were used as biofumigants in Canada prior to potato, strawberry and maize plantings. For Pratylenchus neglectus, population-level reductions of below 60% were reported when using B. campestris and R. sativus green manures prior to planting potato in the US (Al-Rehiayani et al., 1999). In contrast to positive reports in terms of lesion nematode population reductions, Sakuma et al. (2011) demonstrated increases of between 14 and 57% in P. penetrans population

Regarding the ring nematode C. xenoplax, biofumigation of vineyard soils in South Africa with E. sativa (cv Nemat) and B. napus (cv AV Jade) green manures resulted in insignificant (18%) reductions in nematode population levels (Kruger, 2013). Furthermore, in the same study, application of B. juncea green manures of cv Caliente 199 had no effect on C. xenoplax numbers. In potatoes, population levels of the stubby-root nematode Paratrichodorus allius in the US were, however, reduced by 99% using E. sativa as a green manure (Riga, 2011). Contrary to successes as a result of biofumigation, Vervoort et al. (2014) concluded that population-level reductions of Trichodorus and Tylenchorhynchus spp. in their experiments in Germany were related to a combination of intense mechanical tilling and green manuring rather than ITCs that have been released by four respective B. juncea cvs. Terrafit, Terratop, Terraplus and ISCI-99. The absence of host plants of Trichodorus and Tylenchorhynchus spp. has been furthermore suggested to have contributed to the reduction of their population levels in the latter study. 3.5. Non-target, beneficial nematodes Although the majority of studies that were done to date emphasized the positive contributions of biofumigation towards managing nematode pests (Table 2), such a strategy has also been demonstrated to harm non-target, beneficial soil biota that act as biocontrol agents or as antagonists of other pests (Ramirez et al., 2009). This was for example the case where green manures of B. juncea cvs. Arid and Pacific Gold as well as S. alba were applied as biofumigants prior to a potato crop that resulted in a reduction of population levels of entomopathogenic nematodes (EPN), viz. Steinernema carpocapsae, Steinernema glaseri, S. riobrave, Heterorhabditis bacteriophora, Heterorhabditis marelatus and Heterorhabditis megidis (Ramirez et al., 2009). Henderson et al. (2009) further reported that biofumigation interfered with the biological control of M. chitwoodi through the use of the EPN Steinernema feltiae and Steinernema riobrave. According to Valdes et al. (2012) application of S. alba green manures as biofumigant or biological soil disinfestation strategies in a Belgium study resulted in an increase in bacterivores, a decrease in fungivores but no change in omnivore and predator soil populations. Also observed in the latter study was an increase in dauer larvae, which is in agreement with Gruver et al. (2010) to most probably be the result of the steep incline in and overgrazing by bacteriovers due to rapid nitrogen mineralisation after green manure application. Decreases in fungivores after green-manure application of Brassicaceae crops is suggested to be caused either by the direct effect of biological soil disinfestation, biofumigation itself or indirectly by the increase in nematode antagonists (Riga et al., 2004; Valdes et al., 2012). In a biofumigation experiment by Engelbrecht (2012), soil communities of bacteri- and fungivores increased substantially in South African soils regarding their diversity and population levels as a result of green manure amendment prior to planting potato. Consequently faunal analyses demonstrated that the soil-health status shifted from the enriched and unstructured quadrant prior to green manuring to the enriched and structured quadrant after biofumigation using cruciferous crops. In another study in Canada, the effect of seed meal and bran soil amendments was less significant

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on beneficial nematode species Caenorhabditis elegans compared to the effect it had on PPN (Yu et al., 2007). 3.6. Factors contributing to the success of nematode-pest control using biofumigation Although the majority of reports referred to in Table 2 illustrate the beneficial effect of biofumigation using Brassicaceae green manures and soil amendments, Morra and Kirkegaard (2002) and Roubtsova et al. (2007) reiterated that the nematicidal activity of Brassicaceae crops by means of biofumigation was limited/ineffective in some experiments. This phenomenon is generally ascribed to the use of cruciferous cultivars and species that contain variable concentrations of GSLs in their tissues (Craig et al., 2005). Efficacy is also affected by the stage of plant development, method of tissue maceration, method and speed of incorporation of tissues in the soil (Matthiessen et al., 2004). Furthermore, for biofumigation to be effective, thorough and even incorporation and distribution of the biofumigant material through the soil profile where the target nematode pest(s) occur is required (Morra and Kirkegaard, 2002; Roubtsova et al., 2007). Various other factors also determine the efficacy of biofumigation with regard to the reduction of nematode pest populations, including the availability of sufficient soil moisture at the time of plant tissue incorporation (Morra and Kirkegaard, 2002), soil characteristics, soil temperature, soil fluoride levels (reported to be positively correlated with the biocidal activity of Brassicaceae soil amendments), cultivar of the cruciferous crop used and rates of plant residues incorporated into the soil. Furthermore, research showed that a positive correlation exists between the rates of Brassicaceae green manures being incorporated in soils and the percentage of reduction in nematode pest populations (Kwerepe and Labuschagne, 2003; Lazzeri et al., 1993; Lopez-Perez et al., 2005; Matthiessen and Kirkegaard, 2006; Motjahedi et al., 1993; Youssef and Lashein, 2013). Kwerepe and Labuschagne (2003) for example suggested that low rates of cruciferous plant material (20 kg/ha) were ineffective in reducing M. incognita infection and damage in Vigna subterranea as opposed to higher rates of 60 kg/ha. However, high rates of cruciferous residues used resulted in phytotoxicity of crop plants that were grown in treated soils (Kwerepe and Labuschagne, 2003). The same trend was reported by Youssef and Lashein (2013) when different rates of B. oleraceae leaf residues were used in M. incognita-infested plots. Soil temperature at the time of tissue incorporation appears to determine to a large extent the level of nematode control and also the time needed to achieve such effective control (Ploeg and Stapleton, 2001). It is, however, unknown if differences in temperature requirements of the different nematode pest species have an influence on the adverse effect of biofumigation on their population levels. A study in Australia showed that M. javanica reproduced on B. juncea and B. napus at rates which increased the nematode population in the soil during their growth in the summer season; however nematode proliferation could be prevented if these plants were grown in the winter under low temperatures (Stirling and Stirling, 2003). An effective way of enhancing the nematode-control efficacy of biofumigation in small areas is to combine the incorporation of Brassicaceae plants with soil tarping using plastic film, which may prevent rapid emission of volatile nematicidal compounds from the soil to the atmosphere. This way the soil temperature is increased by means of a soil-solarization effect if performed in hot seasons. Elevation in soil temperatures, resulting from soil solarization, has been shown to improve the efficacy of Brassicaceae amendments in terms of nematode control (Ploeg and Stapleton, 2001; Stapleton and Duncan, 1998). According to Blok et al. (2000), anaerobic soil conditions following

application of the latter strategy result in killing pathogens, including nematodes. Moreover, combination of sub-lethal soil temperatures (30e38  C) and the biofumigation effect, resulting from toxic volatile compounds being released, may have a synergistic effect on the efficacy of nematode control. Furthermore, Mojtahedi et al. (1993) showed that the effect of Brassicaceae biofumigation was more pronounced in inactivating/killing secondstage juveniles (J2) of M. chitwoodi than the adverse effect it had on egg masses of the same species. It has thus been suggested that biofumigation would be most effective when PPN are in an active, motile life stage in soils. 4. Cover and rotation crops Brassicaceae spp. are also used as cover crops to substantially reduce population levels of economically important PPN (Nyczepir and Thomas, 2009). Lower nematode pest populations due to the use of cover crops have been attributed to their poor host status with regard to the particular target PPN (Rodriguez-Kabana et al., 1989), production/release of allelochemicals by aerial plant parts that were slashed and incorporated in the soil (Halbrendt, 1996) and/or enhancement of nematode-antagonistic flora and fauna in soils where these crops have been grown (Rodriguez-Kabana et al., 1989; Wang et al., 2002). Cover crops are usually grown between the planting of cash crops to enhance soil fertility and soil structure, reduce soil erosion and provide forage for grazing livestock while suppressing nematode pest populations. Such crops typically have no economic return for the producer (Nyczepir and Thomas, 2009). Subsequently, their benefits are rather measured as a result of reduced nematicide costs and/or enhanced productivity of followup rotation crops (Nyczepir and Thomas, 2009). The definition of a cover crop by Viaene and Abawi (1998) is more inclusive since according to them a good cover crop is not only one that exhibits a poor host status to the target nematode pest species, but also reduces the population of the nematode pest after incorporation of the crop into the soil. These authors thus included biofumigation in their definition of a cover crop. Based only on host suitability a range of Brassicaceae species that were used as cover crops in various studies showed nematicidal effects against multiple nematode pest species while others were good hosts (Table 3). As with literature on biofumigation, information on Meloidogyne dominates in this regard followed by that for cyst- and lesion nematodes as well as for other nematode genera such as Belonolaimus, Helicotylenchus, Hemicriconemoides and Rotylenchulus which is referred to below. 4.1. Root-knot nematodes Numerous genotypes of various Brassicaceae spp. have been identified as poor hosts of M. arenaria, M. chitwoodi, Meloidogyne ethiopica, M. hapla, M. incognita and M. javanica by various researchers from several countries (Table 3). Growing such genotypes as cover crops will thus generally benefit producers in areas where these nematode pests are present in agri- and/or horticultural soils. Lopez-Perez et al. (2010) and Monfort et al. (2007) for example reported reduced M. incognita-population levels and root galling of 36 and 100%, respectively, using various B. oleracea cvs. as cover crops in the US. Also, Monfort et al. (2007) reported a 41% reduction in population levels of M. incognita using four B. rapa cultivars (Purple Top, White Globe, White Egg and Dwarf Essex). In South Africa, the poor-host status of Brassicaceae crops was also illustrated in a 5-year crop rotation trial in the Vaalharts Irrigation Scheme. In the latter study, cultivation of B. napus (cv's Hyola and Rainbow) as winter rotation crops reduced Meloidogyne spp. population levels substantially (Nel et al., 2008). In a grapevine study in

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South Africa, Kruger et al. (2015) reported cv Nemat (E. sativa) as a poor host of M. javanica, while classifying S. alba (cv Braco), B. napus (cv AV Jade), B. juncea (cv Caliente 199) as maintenance crops that supported low egg-mass production of this nematode pest. Conversely, many genotypes belonging to the Brassicaceae family have also been reported as being susceptible to root-knot nematodes. This was illustrated in the US by Monfort et al. (2007) who recorded significant increases in population levels of M. incognita after using B. oleracea (cv Dwarf Blue Curled Scotch) and S. alba (cv Pacific Gold) as well as the B. napus cv American Purple Top cultivar as cover crops. A similar scenario was experienced when cultivars Scarlet Globe and White Icicle of R. sativus were used in the same study. Another report about the sub-optimal use of Brassicaceae cover crops indicated that high population levels of M. incognita were recorded with roots of E. sativa cv. Caliente (mean of 26,553 eggs and J2/50g roots) and tubers of R. sativus cvs. Terranova and Doublet (means of 2,470 and 1,927 eggs and J2/50g roots, respectively) in a field trial in the Free State Province of South Africa during 50% flowering of such crops (Engelbrecht, 2012). In the same study, significantly lower egg and J2 numbers (338/50g roots) were, however, extracted from roots of B. juncea cv Nemat. 4.2. Lesion nematodes A number of genotypes with poor-host suitability to two lesion nematode species, Pratylenchus brachyurus and Pratylenchus zeae, have also been reported (Table 3). Reductions in population levels of these lesion nematode species that ranged between 54 and 94% were recorded in sugarcane experiments in South Africa through cover cropping of B. rapa (var. ATR-Hyden) and B. napus (var. Giant English) (Berry et al., 2011). In South Africa, inclusion of Brassicaceae crops in a 5-year crop rotation trial in the Vaalharts Irrigation Scheme demonstrated that B. napus (cvs. Hyola and Rainbow) grown in winter resulted in an increase of Praylenchus spp. population levels (Nel et al., 2008). 4.3. Other economically important nematode pests For reniform nematodes, Wang et al. (2003) reported significant reductions of more than 90% in their population levels after using B. napus (cv Dwarf Essex) and S. alba (cv not reported) as intercycle cover crops in pineapple fields in the US. Wang and Sipes (1998) also reported a significant reduction in numbers of the same nematode species using S. alba as a cover crop, while in another study in Brazil Asmus et al. (2008) recorded a 73% reduction in R. reniformis population levels after growing R. sativus (cv Siletina) as a cover crop in vegetable production. With regard to C. xenoplax, Kruger (2013) suggested that the canola cv AV Jade and the B. juncea cv Caliente 199 have the best potential to suppress such nematode pests in vine orchards in South Africa. However, cv Nemat (E. sativa) has been classified as a maintance host of C. cenoplax (Kruger et al., 2015). For the economically important dagger nematode X. elongatum, Berry et al. (2011) reported an ultimate 100% reduction in population levels after using B. napus (Var. Giant English) as a cover crop. Increased population levels of X. elongatum (33%) and P. minor (23%) were, however, reported in the same study after growing B rapa (Var. ATR-Hyden) as a cover crop. Inclusion of B. napus (cvs. Hyola and Rainbow) as winter-rotation crops in South Africa had no effect on population levels of the peanut-pod nematode Ditylenchus africanus (Nel et al., 2008). 5. Conclusions The management of nematode pests is rarely successful in the

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long term when single strategies such as chemical control, host plant resistance, crop rotation and/or other methods are applied (Onkendi et al., 2014). Also, increased pressure to progressively withdraw Class 1 nematicides from world markets, nowadays more than ever, necessitates the integration of multiple nematode management strategies into integrated pest management programmes (IPM). Such interventions will assist in reducing population levels of economically important nematode pests and subsequently result in optimized and sustainable crop production. This is the platform where the use of cruciferous crops can be beneficial as has been accentuated by the majority of research that was done to date, proving such crops were in most of the cases effective in reducing nematode pest populations. Such a strategy thus offers the potential to be one of the proper alternative nematode management approaches to be tailor-made and applied in cropping systems. As with other nematode management strategies, the use of Brassicaceae crops as a single, stand-alone management strategy will not eliminate target nematode pests in soils. Although inefficacy to reduce nematode pests using Brassicaceae biofumigation and/or cover-/poor-host crop strategies has been reported, it is substantially less than positive reports in this regard and producers will thus benefit by adopting this approach. Ultimately, such a tool can assist in reducing population levels of economically important nematode pests substantially to allow sustainable production of susceptible, follow-up crops in nematode-infested fields. Furthermore, the added benefits of Brassicaceae-based management strategies such as increasing the overall structure as well as the chemical and physical status of soils (Shepherd et al., 2002) makes it worthwhile to progressively exploit it as an alternative, nematode management strategy. Also, the suppression of soil-borne pathogens, other than nematode pests, and diseases as well as increasing the population levels of beneficial nematodes in soils where biofumigation has been applied, render it a viable option to address nematode problems. However, when high nematode pest populations exist in soils, the use of several successive poor- or non-host Brassicaceae crops as well as their green manures/seed meals will have to be practiced before a nematode-susceptible crop may be grown successfully. Even then, the well-planned and responsible use of a nematicide(s) and/or application of other concurrent nematode management strategies may be needed. It is also important to bear in mind that different Brassicaceae species may vary in their ability to reduce population levels of specific nematode pests and the use of such a crop is also influenced by other factors such as the target nematode pest species, soil temperature and others as described earlier in the article. Cultivar selection thus plays a decisive role when using Brassicaceae crops as a management tool to combat nematode problems, since it is agreed with Monfort et al. (2007) and Edwards and Ploeg (2014) that it is unproductive to grow a good-host crop. It is non-negotiable that the host status of Brassicaceae poor-host- or cover crops be known with regard to the target plant-parasitic nematode species to prevent their build-ups and in this way optimize such a management strategy. Ultimately, research interventions illustrated that Brassicaceae crops in most cases suppressed population levels of economically important plantparasitic nematode genera such as Globodera, Heterodera, Meloidogyne, Pratylenchus and others. It thus without doubt qualifies as a versatile and valuable tool to assist in managing these pests and contribute to soil health and ultimately food security. 6. Recommendations The following important guidelines are of utmost importance should biofumigation and/or the use of cover- and/or poor-host crops be considered for use in cropping systems to reduce

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nematode pest levels: - Sufficient sources of irrigation water should be available should Brassicaceae crops be grown in low-rainfall areas to ensure optimal growth of the crops until flowering when the aerial plant parts are slashed and incorporated into the soil. - Knowledge about the host status of Brassicaceae-crop cultivars to be used as cover-/rotation crops to target nematode pest species, of which the identity should be known, is a prerequisite. - Knowledge about the GSLs content of commercially available Brassicaceae genotypes to be used for its biofumigation properties. - Knowledge about the growth stage during which the GSLs content of the Brassicaceae crop to be used for its biofumigation properties reaches its highest levels. - Appropriate equipment for macerating by crushing the plant cells. - The availability of sufficient water to maintain high soil moisture during the time of green material incorporation. Acknowledgements The authors express their gratitude towards the Protein Research Foundation (PRF) of South Africa who financially funded the compilation of this article. Opinions expressed and conclusions arrived at are those of the authors and not to be attributed to the PRF and/or NWU. References Abu-Ghannam, N., Jaiswal, A.K., 2014. Blanching as a treatment process: effect on polyphenol and antioxidant capacity of cabbage. In: Preedy, V. (Ed.), Processing and Impact on Active Components in Food. Elsevier/Academic Press, Amsterdam, pp. 35e43. Agbenin, N.O., 2011. Biological control of plant-parasitic nematodes: prospects and challenges for the poor Africa farmer. Plant Prot. Sci. 2, 62e67. Ahuja, I., Rohloff, J., Bones, A.M., 2010. Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review. Agron. Sustain. Dev. 30, 311e348. Aires, A., Carvalho, R., Barbosa, M.D., Rosa, E., 2009. Suppressing potato cyst nematode, Globodera rostochiensis, with extracts of Brassicaceae plants. Am. J. Potato Res. 86 (4), 327e333. Al-Rehiayani, S., Hafez, S., 1998. Host status and green manure effect of selected crops on Meloidogyne chitwoodi race 2 and Pratylenchus neglectus. Nematropica 28, 213e230. Al-Rehiayani, S., Hafez, S.L., Thornton, M., Sundararaj, P., 1999. Effects of Pratylenchus neglectus, Bacillus megaterium and oil radish or rapeseed green manure on reproductive potential of Meloidogyne chitwoodi on potato. Nematropica 29, 37e49. Anwar, S.A., McKenry, M.V., 2010. Incidence and reproduction of Meloidogyne incognita on vegetable crop genotypes. Pak. J. Zool. 42 (2), 135e141. Anwar, S.A., Mckenry, M.V., 2012. Incidence and population density of plantparasitic nematodes infecting vegetable crops and associated yield losses in Punjab. Pak. J. Zool. 44 (2), 327e333. Asmus, G.L., Inomoto, M.M., Cargnin, R.A., 2008. Cover crops for reniform nematode suppression in cotton: greenhouse and field evaluations. Trop. Plant Pathol. 33 (2), 85e89. Avato, P., Addabbo, T.D., Leonetti, P., Argentieri, M.P., 2013. Nematicidal potential of Brassicaceae. Phytochem. Rev. 12, 791e802. Aydinli, G., Menan, S., 2012. Screening resistance level of Brassicaceae plants to cabbage cyst nematode, Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turk. J. Entomol. 36 (1), 3e10. Baimey, H., Coyne, D., Dagbenonbakin, G., James, B., 2009. PPN associated with vegetable crops in Benin: relationship with soil physic-chemical properties. Nematol. Mediterr. 37, 227e236. Bekal, S., Becker, J.O., 2000. Host range of a California sting nematode population. Hortscience 35 (7), 1276e1278. Belair, G., Fournier, Y., Dauphinais, N., Dangi, O.P., 2002. Reproduction of Pratylenchus penetrans on various rotation crops in Quebec. Phytoprotection 83, 111e114. Bellostas, N., Sørensen, J.C., Sørensen, H., 2004. Qualitative and quantitative evaluation of glucosinolates in cruciferous plants during their life cycles. Agroindustria 4, 267e272. Bennet, R.N., Rosa, E.A.S., Mellon, F.A., Kroon, P.A., 2006. Ontogenic profiling of glicosinolates, flavoids and other secondary metabolites in Eruca sativa (salad

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