Annual Research & Review in Biology 5(3): 189-206, 2015, Article no.ARRB.2015.021 ISSN: 2347-565X

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Evolutionary Ecology of Diamondback , Plutella xylostella (L .) and insulare (Cresson) in North America: A Review

Sadia Munir 1* , Lloyd M. Dosdall 1 and John T. O’Donovan 2

1Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, T6G 2P5, Canada. 2Lacombe Research Centre, Agriculture and Agri-Food Canada, 6000 C and E Trail, Lacombe, AB, T4L 1W1, Canada.

Authors’ contributions

This work was carried out in collaboration between all authors. Author SM managed the literature searches and wrote the first draft of the manuscript. Author LMD supervised and critically reviewed the manuscript and author JTO helped in editing and final revision of manuscript. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/ARRB/2015/11834 Editor(s): (1) George Perry, Dean and Professor of Biology, University of Texas at San Antonio, USA. Reviewers: (1) Anonymous, Osmania University, India. (2) Anonymous, Southwest University, China. (3) Isabel Bertolaccini, Department of Plant Production, Facultad de Ciencias Agrarias (U.N.L.), Kreder 2805, (3080) Esperanza (Santa Fe), Argentina. Complete Peer review History: http://www.sciencedomain.org/review-history.php?iid=668&id=32&aid=6211

Received 5th June 2014 th Review Article Accepted 7 July 2014 Published 24 th September 2014

ABSTRACT

The (DBM), Plutella xylostella (L.), is recognized as a widely distributed destructive pest of Brassicaceae. The frequency and severity of P. xylostella outbreaks has increased in recent years, due to climate changes, high production of host plants (vegetable and oilseed Brassica crops), genetic flexibility of the pest that enables it to develop resistance to almost all known insecticides and establish quickly and easily in new environment. All life stages of P. xylostella are attacked by natural enemies but Diadegma insulare (Cresson) is one of the principal, effective and efficient larval parasitoids in North America. In this review, we synthesize published information on the primary aspects of P. xylostella origin, dispersal, migration, biology, and host plants and mainly focus on evolutionary ecology of bitrophic and tritrophic interactions among P. xylostella , its host plants and natural enemies. ______

*Corresponding author: Email: [email protected];

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

Keywords: Evolution; ecology; Diamondback moth; host plant; Diadegma insulare.

1. INTRODUCTION population in an area is regulated by climate, availability and quality of host plants and the Plutella xylostella is not only the most destructive presence of its natural enemies [10]. pest of brassicaceous crops throughout the world but is also among the most difficult to manage 3. BIOLOGY [1,2]. It was first introduced from Europe to North America (Illinois), in 1854. Plutella xylostella now The biology of P. xylostella has been studied occurs throughout North America, wherever its extensively in both laboratory and natural host plants are cultivated [3]. Its management conditions in relation to ecological factors. result in a US$4-5 billion annual cost to the However, its biological and developmental world economy [4]. A few review articles on P. parameters vary due to differences in host plant xylostella host-plant interactions, management species, temperature, and geographical and ecology have been published but a focus on population distribution [11]. The moth is detailed evolutionary ecology of tritrophic multivoltine and can produce four to 20 interactions among P. xylostella , its host plants generations per year in temperate and tropical and its principle parasitoid are lacking. The main regions, respectively [12,13]. In North America, it objective of this review paper is to address the can produce three to five generations per year gaps in the knowledge and understanding of P. [14]. At constant temperature, development can xylostella and D. insulare evolutionary ecology occur from 8-32ºC and under fluctuating and tritrophic interactions. It is believed that the temperature from 4 to 38ºC [15]. Plutella information presented here will encourage xylostella development has been studied by researchers to work on important aspects of P. Bahar et al. [16] at different constant (7,22,30ºC) xylostella and its natural enemies and help and fluctuating temperatures (0-14,15-29ºC, and designing appropriate management strategies 23-37ºC). The development was very slow at involving complete and in depth awareness of lowest constant (7ºC) and fluctuating tritrophic interactions in a particular agro- temperatures (0-14ºC) while fast development of ecosystem. P. xylostella was recorded at highest constant (30ºC) and fluctuating temperatures (23-30ºC). 2. DISTRIBUTION AND ORIGIN OF P. xylostella Plutella xylostella has four life stages: egg, larva, pupa and adult. Oviposition mainly occurs at Plutella xylostella is believed to be the most night in the first 24 to 48 hours of mating and widely distributed species of , then declines gradually. Egg laying reaches zero occurring universally wherever Brassicaceae are in 10 days after adult emergence [11]. Each grown [1]. Six economically important species of female can lay more than 200 eggs either singly the Genus Plutella (Schrank) have been or in small clusters [17,18]. Oviposition is greatly recorded worldwide but only P. xylostella is influenced by host plant species. For instance, cosmopolitan in distribution [5]. It has been oviposition on brassicaceous host plant (Brassica recorded throughout tropical and temperate napus L.) is reported to be higher than non- zones, as far north as Iceland (60°N) and as far brassicaceous hosts (Cleome hassleriana Chod. south as New Zealand (45ºS) [6]. The and Tropaeolum majus L.) [19]. geographical origin of P. xylostella is uncertain. Some have speculated its origin in Europe [7], Eggs are oval and pale to strong yellow in color the Mediterranean area [8] or China [9]. It is also [11]. Egg hatching occurs in 4-8 days [14]. assumed to have evolved in South Africa, based Larvae are pale yellow in color having a dark on the diversity of endemic Brassica plants and head in early instars, and are light to dark green its indigenous diverse parasitoid fauna [5]. North colored in later instars. The larva has V-shaped American populations are most probably of anal legs. First-instar larvae are leaf miners, European origin and were introduced about 150 feeding in the spongy mesophyll tissue of leaves. years ago [7]. Recently, some climatic models Other larval instars feed on all tissues of leaves, have been developed to predict P. xylostella buds, flowers, stems, and siliques [11,20]. The distribution and seasonal phenology in areas of average development time from first to fourth its occasional occurrence. However, the instar is reported as 4.0, 3.6, 3.4, and 4.2 days abundance and distribution of the P. xylostella respectively, under Canadian field conditions; pupation takes place over 7.8 to 9.8 days [14].

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The adult moth is slender and greyish [21]. The 5. EVOLUTIONARY ECOLOGY OF mean longevity of females is significantly INTERACTIONS AMONG P. xylostella reduced relative to males [11]. Development and AND ITS HOST PLANTS survival vary greatly depending on quality of food, quantity of adult feeding, difference in host Plutella xylostella has a wide ecological host plant cultivar and sources of carbohydrate range. The genetic and phenotypic flexibility of P. [22,11]. xylostella , and its ability to modify traits of its life history according to environmental conditions 4. DISPERSAL AND MIGRATION during development enables the pest to survive throughout the year in areas where Migration may evolve as a mechanism that environmental conditions are favorable and host permits individuals to avoid probable failures in plants are easily available, in the absence of survival [23]. may develop migratory other ecological and evolutionary pressures characteristics when their habitat deteriorates [28,37]. The moth feeds almost exclusively on [24]. Plutella xylostella possesses a high plants of the family Brassicaceae , particularly the migratory ability to disperse over long distances genus Brassica , which are widely distributed in a very short time. This can explain why it gets geographically, and include 338 genera and easily established in novel environments and 3709 species [38] (Table 1). newly planted Brassica crops [7,25,26]. Plutella xylostella does not diapause; therefore long- Plutella xylostella is commonly considered a distance immigration through aerial currents is a specialist on Brassicaceae . However, evidence major process affecting population outbreaks of its occasional occurrence on sugar snap peas [27,28]. Plutella xylostella migration and (Pisum sativum L., Fabaceae) in Kenya [70], population seasonality is well documented [1]. Taiwan and the Philippines [55,64], the Similar seasonal migrations have been reported chenopodiaceous vegetable Salsola kali L. in Japan's south western islands [29], in the (prickly saltwort, Russian thistle) in Russia [71], United Kingdom [7,30], New Zealand, South and okra in Ghana [72] have been recorded. Africa, and southern parts of Chile and Argentina Genetic analysis indicated an incomplete [1], and Australia [31]. In both eastern and evolutionary host range expansion and ability to western Canada, P. xylostella re-establishes complete development on the novel host plant each year from annual adult population (snap peas) by P. xylostella strain [67,68,70]. It immigrations from the southern U.S.A. and has also been documented by Dosdall et al. [34] Mexico [32,27,33]. Plutella xylostella adults have that an introduction of a novel crop into an area the ability to travel about 1500 km. Therefore, its can increase insect pest problems, including P. densities can vary considerably from year to year xylostella infestations. [32,27,34,33]. Plutella xylostella cannot survive severe winters. Dosdall [35] reported its survival Plutella xylostella is often studied in its under mild winter conditions in western Canada. relationship with its host plant’s specific However, successful overwintering in northern chemistry. The plants of the family Brassicaceae latitudes in large numbers is considered to be an are characterized by the presence of sulphur- unusual phenomenon [36]. Hence, it is assumed containing secondary metabolites known as that migration is the most important cause of glucosinolates that play a key role in plant population seasonality in P. xylostella. It is a defense against herbivores [73]. Some regular ecological event that occurs at glucosinolate hydrolysis products like approximately the same time of the year and a isothiocyanates are highly toxic to insect characteristic of the vast majority of insect herbivores, but those insects specialized in populations [28]. Campos et al. [37] noted that feeding on plants with these secondary low nutritional quality and short temporal compounds have a mechanism to overcome this persistence of mature host plants, reduced body toxicity [74,75]. Very little is known about the size, prolonged longevity and delayed sexual mechanisms evolved by herbivores to overcome maturation of due to unfavorable these defensive plant compounds [73]. There is environmental conditions. This will increase the some evidence of temporal association between chances of reaching new reproductive sites. the diversification of the host plants and insect Moths having such characteristics have greater herbivores [75]. However, the origin of an fitness and are active migrants, when the evolutionary novel defense mechanism and resources are limited and habitat deteriorated. diversification of Brassicales (90-85 mya) were most probably followed by co-evolution of insect

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herbivores and their host plants [76,77]. In Brassicaceae host plant species and cultivars Brassicaceae , the glucosinolates co-occur with vary considerably in their level of susceptibility myrosinases and are together known as for P. xylostella. Sarfraz et al. [40] proposed that “mustard oil bomb” [78]. These two compounds Sinapis alba L. and Brassica rapa L. are highly are compartmentalized in plants but come preferred for oviposition. The developmental together upon plant tissue damage and release time, longevity, body weight, and other toxic isothiocyanates. The larvae of P. xylostella parameters are greatly affected by host plant have evolved a defensive mechanism to detoxify species; e.g., larval and pupal developmental glucosinolate (mustard oil bomb) and its toxic times of females are faster on Brassica juncea hydrolysis products by an enzyme glucosinolate (L.) Czern. and S. alba than on several other sulfatase present in their gut. The enzyme Brassicaceae . actively prevents the formation of toxic hydrolysis products by converting glucosinolates to Accumulating evidence indicates that host plant desulfoglucosinolates rather than more toxic morphological characteristics like leaf color, size, nitrile and isothiocyanates. This mechanism and their position on the plant, epicuticular enables P. xylostella herbivory on wide range of waxes, trichome density, chemosensory Brassica plants [54,74]. stimulation and abiotic factors affect P. xylostella oviposition, development and herbivory [79,80]. Plutella xylostella adults rely on morphological For instance, P. xylostella females prefer glossy and chemical cues (glucosinolates like sinigrin, cultivars (i.e., low surface wax) over waxy sinalbin and glucocheirolin) for host plant cultivars (normal wax bloom) for oviposition; location, recognition, oviposition, stimulation and though larval survival is reduced on glossy feeding initiation [79,80,74]. The performance of cultivars [48]. Some studies reported oviposition P. xylostella varies on cultivars of the same plant preference of P. xylostella on lower leaf surfaces species with different glucosinolate contents and of host plants [11,87,88], while some reported a profiles; for example, high performance of larvae higher oviposition preference on the upper has occurred in plant species with intermediate surfaces of crucifer leaves [14,1]. Similarly, glucosinolate content [81] or with low myrosinase number of eggs laid and trichome density were content [82]. Similarly, higher densities of P. positively correlated [17,89]. A recent study xylostella larvae are reported to be associated showed a positive correlation between P. with plant cultivars having higher glucosinolate xylostella oviposition choice and larval survival contents [83]. High concentrations of allyl on undamaged host plants [90]. Variations in the isothiocyanates are reported to be toxic for host plant nutritional quality can affect the pest larvae and adults [82]. In fact, glucosinolates are directly. Usually sulphur-deficient plants are less not the only plant compounds that stimulate attractive but plants grown under a high fertilizer oviposition and feeding activity; other aspects of regime are more attractive for P. xylostella host plant nutritional quality, such as host plant oviposition [91,92]. volatiles, morphology and chemistry or a combination of these also play an important role The preferences and performance of P. xylostella [48,75]. vary significantly among brassicaceous wild and cultivated species. Sinapis alba is a most Some plant compounds like saponins, present on preferred host followed by B. rapa , B. juncea , the leaf surface of some Barbarea spp., act as and Brassica napus L. among the cultivated deterrents for larval development but attractants species [36], while Sinapis arvensis L. followed for oviposition. The presence of these by Erysimum cheiranthoides L. and Capsella compounds supports their ecological role in host bursa-pastoris (L.) are preferred wild recognition and stimulation of oviposition for the brassicaceous hosts [59]. One of the main diamondback moth [84]. Plutella xylostella adults reasons for variation in development and can also respond differently to different host plant fecundity of P. xylostella on different plant volatiles emitted as a result of insect damage. species or different cultivars of the same species Females rely on these volatile cues to recognize is due to the differences in plant quality, reflected acceptable hosts for its progeny survival, fitness either in insect nutrient requirements or and to reduce competition for food [85]. Reddy & phagostimulation of P. xylostella [93]. Guerrero [86] reported three cabbage green leaf volatiles that are highly attractive to P. xylostella females.

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Table 1. Host plants of Plutella xylostella

Cultivar/Species Common name Plant type Ref. No Brassica carinata L. Ethiopian mustard Vegetable, Oilseed [39,40,41] Brassica juncea L. Indian mustard, brown Vegetable, Trap [42,43,40,44] mustard crop, Oilseed Brassica napus L. Canola, Canadian Vegetable, Oilseed [45,42,40,41,46,47] turnip, rutabaga Brassica nigra L. Black mustard Vegetable, Spice [45] Brassica oleracea L. var. Collard, flowering kale Vegetable [45, 48, 49] acephala Brassica oleracea L. var. Kale Vegetable [1] alboglabra Brassica oleracea L. var. Cauliflower Vegetable [45,50,46] botrytis Brassica oleracea L. var. Savoy cabbage Vegetable [51] sabauda Brassica oleracea L. var. Cabbage Vegetable [52,45,46,47] capitata Brassica oleracea L. var. Brussels sprouts Vegetable [1] gemmifera Brassica oleracea L. var. Kohlrabi Vegetable [50,46] gongylodes Brassica oleracea L. var. Broccoli Vegetable [45,50] italica Brassica rapa L. var. Pak choi Vegetable [1] pakchoi Brassica rapa L. var. Chinese cabbage Vegetable [17,53,47] pekinensis Brassica rapa L. Canola Oilseed [40] Raphanus sativus L. Radish, bier radish Vegetable [52] Sinapis alba L. ( Brassica White mustard, yellow Vegetable, spice [42,40,41] hirta Moench) mustard Wild Cruciferous Arabidopsis thaliana (L.) Thalecress, mouse- [54] Heynh earcress Barbarea vulgaris (L.) R. Yellow rocket, [45,55,48] Br. rocketcress Berteroa incana (L.) DC. Hoary alyssum [45] Capsella bursa-pastoris L. Shepherd’s purse, [45,56] mother’s-heart Cardamine flexuosa With. Flexuous bittercress [57] Descurainia sophia L. Flixweed [1] Erysimum cheiranthoides Wormseed mustard, [58,45,56,59] L. treacle mustard Erucastrum arabicum - [60] (Fisch. & Mey.) Lepidium campestre (L.) R. Field pepperweed [45] Br. Lepidium virginicum L. Virginia pepperweed, [61] peppergrass Raphanus raphanistrum L. Wild radish, wild rape, [45,49] wild turnip Rorippa indica (L.) Hiern Indian marshcress [57,61] Rorippa islandica (Oeder) Marsh yellowcress [57] Barba`s Rorippa micrantha (Roth.) - [49]

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Cultivar/Species Common name Plant type Ref. No Jonsell Rorippa nudiuscula - [49] (E.Mey. ex Sond.) Thell. Sinapis arvensis L. Wild mustard, crunch [45,59,56] (Brassica kaber (DC) weed Wheeler) Sisymbrium altissimum L. Tumbling mustard, tall [1] hedge mustard Thlaspi arvense L. Stinkweed, pennycress, [45] French weed Non -cruciferous Tropaeolum majus L. Nasturtium, Indian cress Flowering [58] ornamental plant Cleome species Spider plant Flowering plant [62] Pisum sativum L. Peas Pulse [63,64,65,66,67,68] Hibiscus esculentus L. Okra, Lady fingers Vegetable [69]

6. NATURAL ENEMIES OF P. xylostella et al. [95]. Kirk et al. [104] reported 27 parasitoid species mainly of the hymenopteran genera All stages of P. xylostella are attacked by various Diadegma , Cotesia and Oomyzus on 115 parasitoids and predators (Table 2). populations of P. xylostella collected in 32 countries. The majority of these parasitoid Delvare [114] reported over 135 parasitoid species are known to come from Europe where species worldwide. Among these, the most P. xylostella is believed by some to have common ones include six species of egg originated. parasitoids, 38 larval, and 13 pupal parasitoids [115]. Egg parasitoids (genera Trichogramma In different geographical areas of the world, and Trichogrammatoidea ) (: various parasitoid species are responsible for Trichogrammatidae ) contribute little to natural suppressing P. xylostella populations. For control generally because of their nonhost- instance, Diadegma spp. and Diadromus spp. specific nature [116]. In addition, to utilize them predominate in Europe [7], New Zealand [123] in biological control initiatives requires frequent and South Africa [124]. Diadegma semiclausum inundated releases [1]. Larval parasitoids are (Helle´n), Diadegma rapi (Cameron) and predominant and have maximum control Diadromus collaris (Grav.) are collectively potential. The most effective P. xylostella larval responsible for 93% parasitism in Victoria, parasitoids belong to hymenopteran genera Australia [120]. Diadegma semiclausum has Microplitis (Braconidae ), Cotesia (Braconidae ), been reported to keep the P. xylostella and Diadegma ( ) [115,1]. A few population below economic threshold levels in prepupal and pupal parasitoids of the genus certain areas of Europe, Africa, Asia [1], Diadromus (Ichneumonidae ) also provide Malaysia, Taiwan, Philippines, Indonesia, significant control [7,1,117,104,2]. Occasionally Thailand, Zambia, New Zealand and Australia some species of Pteromalus (Hymenoptera: [125,96]. The most abundant parasitoids in east Pteromalidae) species parasitize P. xylostella Africa are Diadegma mollipla (Holmgren) and pupae [100]. Oomyzus sokolowskii (Kurdjumov) [126]. In Ethiopia, Diadegma spp. and Cotesia plutellae On a worldwide scale, large numbers of P. (Kurdj.) are key parasitoid species [39]. Cotesia xylostella parasitoid species have been reported plutellae and O. sokolowskii are considered the but some of them were misidentified [118,95]. most promising biological control agents in China Thompson [119] catalogued 48 species of [113]. In the relatively hotter lowlands of many parasitoids associated with P. xylostella , while Asia-Pacific regions, C. plutellae is the dominant Goodwin [120] reported over 90 such parasitoid and most effective larval parasitoid of P. species. Similarly, Mustata [121] listed 25 xylostella [1]. In the Eastern Cape (South Africa), parasitoid species from Moldavia (Romania). Ten four species viz., D. mollipla , C. plutellae , species of Diadegma that attack P. xylostella are D. collaris and O. sokolowskii , are recorded as recognized by Fitton & Walker [122]. Moreover, main parasitoids of P. xylostella [127]. Similarly, seven Diadegma species are revised by Azidah seven species are observed in Brasilia but only

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two species, D. leonitiniae (Brethe´s) and ability to function as biological control agents Apanteles piceotrichosus (Blanchard) are varies between species, and usually depends on dominant [128]. In general, few parasitoid their direct relationships with their host, species are responsible for a high level of environment and interspecific interactions. parasitism in an area. Lim [125] noted that the

Table 2. Example of some common natural enemies of Plutella xylostella

Natural Enemies Host stage attacked Ref. No A-Parasitoid Trichogrammatoidea bactrae ( Nagaraja) Egg [94] Trichogramma pretiosum (Riley) Trichogrammatidae spp. Diadegma insulare (Cresson) Larva [95] D. fenestrale (Holmgren) D. mollipla (Holmgren) D. varuna Gupta D. leontiniae (Brèthes) D. rapi (Cameron) D. semiclausum (Hellén) Larva [96] Apanteles ippeus (Nixon) Cotesia plutellae (Kurdjumov) Larva [97] Microplitis plutellae Muesbeck Larva [25] Oomyzus sokolowskii (Kurdjumov) Larva-Pupa [98] Tatrastichus ayyari (Rohwen) Pupa [99] Brachymeria phya (Walker) Pupa [96] Diadromus collaris (Gravenhorst) Pre-pupa, Pupa D. subtilicornis (Gravenhorst) Pre-pupa, Pupa [25] Pteromalus spp. Pupa [100] B-Pathogen Bacillus thuringiensis Berliner Larva [101] Zoophthora radicans (Brefeld) Batko, Larva [102, Beauveria bassiana (Balsamo) Vuillemin, 103, 104] Metarhizium anisopliae (Metsch.) Sorokin Paecilomyces farinosus (Holm ex Gray) Nomuraea rileyi (Farlow) Sampson Fusarium spp. Pandora spp. Erynia spp. Conidiobolus spp. Scopulariopsis spp. Granuloviruses (GVs) Larva [105,106] Nucleopolyhedrovirus NPVs Cypovirus CPVs Steinernema carpocapsae (Weiser) Larva [107] Heterorhabditis sp. [108] Nosema bombycis (Negali) [109] Vairimorpha sp. [110] C-Predator Lycosids Mostly Larva [111,112] Linyphiids Syrphids Egg, Larva [112] Staphylinids Reduviids Nabids Carabids Coccinella spp. Egg-Larva [113]

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Among parasitoids that attack P. xylostella , only [139,136]. On average, adult D. insulare live for a few solitary larval parasitoid species in the 26 days and lay 814 eggs per female at 23°C Ichneumonid genus Diadegma , solitary pupal [140]. Adults require a continuous nectar source parasitoids in the genus Diadromus , solitary for survival and longevity and as a result they larval parasitoids in the braconid genera prefer habitats with abundant food sources [141]; Microplitis and Cotesia , and the gregarious such habitats appear to enhance D. insulare larval-pupal parasitoid in the eulophid genus fecundity and longevity [142]. For instance, sites Oomyzus are considered to be predominant [2]. with flowering plants like alyssum, Lobularia maritime (L.) Desv. ( Brassicaceae ) [143], or with 6.1 Evolutionary Ecology of Diadegma borders of flowering buckwheat, Fagopyrum insulare : A Key Larval Parasitoid of esculentum Moench (Polygonaceae ) in cabbage P. xylostella fields enhance D. insulare populations [142]. The number of P. xylostella larvae parasitized by a The genus Diadegma Froster ( Hymenoptera: single D. insulare female may vary from zero to Ichneumonidae : Campopleginae ) represents a 150, depending upon the food source [144]. large group of koinobiont endoparasitoids of Unlike its host, D. insulare developmental biology Lepidoptera with 201 species known to occur has not been studied extensively. However, in a worldwide [129]. Several Diadegma species, recent study longer development time was such as D. fenestrale (Holmgren), D. insulare recorded at constant and lower temperatures. (Cresson), D. leontiniae , D. mollipla , D. rapi , and High pupal mortality of D. insulare was also D. semiclausum , are reported to attack P. observed at higher temperature, and this may xylostella [95,130]. There is a wide geographical explain the greater effectiveness of this variation in predominance of Diadegma species, parasitoid in cooler regions [16]. with the majority (131 species) having a Palearctic and a few (33 species) have a Resource variation and their spatiotemporal Nearctic distribution [1]. distribution has a significant impact on the physiology of herbivore pests, which in turn mediates pest-parasitoid interactions, as well as Diadegma insulare (Cresson) ( Hymenoptera: the effectiveness, survival, development, size, Ichneumonidae ) is native to the Neotropics [95], longevity, and fecundity of parasitoids and is a key parasitoid of P. xylostella in North [145,146,147]. The density and distribution of a America [131,132,133]. Diadegma insulare is parasitoid’s population is correlated with the also one of three major hymenopterans density and distribution of its herbivore’s host parasitoids of P. xylostella in Canada; the other plant. For instance, field populations of D. two include a larval parasitoid Microplitis plutellae insulare are often clustered, with distributions (Mues.), and a prepupal and pupal parasitoid, that correlate with their herbivore host Diadromus subtilicornis (Grav.) [12,25,27]. The populations and host plants having high sulphur D. insulare origin in western Canada is unknown, content [148,19,36]. but it likely migrates northward in spring along with its hosts rather than overwintering [134]. Parasitoid life history traits are influenced by the choice made by its herbivore host via mediated Diadegma insulare , a solitary endoparasitoid, host plant quality [149,150]. The nutritional feeds within the P. xylostella larva [12]. The quality of plants consumed by the herbivore host number of generations per year corresponds to of D. insulare affects the sex ratio of the the number of generations of its host as one host parasitoid; more female parasitoids emerged larva supports only one parasitoid larva [135]. It from P. xylostella larvae on well-fertilized plants can parasitize all four larval instars of [137]. Similarly, the performance of D. insulare is P. xylostella [136]. The specific larval instars improved when P. xylostella larvae are reared on parasitized by D. insulare can affect the sex ratio highly fertilized plants [92,36]. Survival, of offspring. More males than females are parasitism, and development time of D. insulare produced when second instars are parasitized, varied considerably among the plant genotypes but when third and fourth instars are parasitized utilized by its P. xylostella host [41]. Percentage the progeny comprise a greater proportion of parasitism of D. insulare is higher and females than males [137,138]. The parasitoid development time shorter on cultivated crucifers emerges as a mature larva from the pre-pupa of than on wild species [45]. Sarfraz et al. [41] its host, and spins its own cocoon within that of reported that S. alba supports high P. xylostella the host where it can easily be distinguished parasitism levels and parasitoid survival, and

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relatively rapid parasitoid development as The mortality risks appear to be high for compared to B. napus L. cv. Q2. koinobionts (that cause the host temporary or nonlethal paralysis), through hyperparasitism and The role of plants in the ecology and biology of multiparasitism [158,159,160] as they are parasitoids is clearly evident in their effect of competitively inferior to idiobionts (cause parasitoid host selection. Plant-associated visual permanent paralysis or death) [161,162]. cues are important in the process of host location Nonetheless, D. insulare has a significant by parasitoids [151]. Similarly, plants respond to ability to avoid multiparasitism and super herbivore damage by emitting complex mixtures parasitism [140]. of volatile compounds that attract natural enemies. Many field experiments suggested that 7. CONCLUSION parasitoids respond directly to both herbivores and their host plant volatile cues [152,153]. In In conclusion, understanding the evolutionary these studies, D. insular e was assumed to be ecology of a pest, its host plants, and its attracted to plant tissue damaged by P. xylostella parasitoid and their tritrophic interactions is very larvae [133]. complex and variable. It requires detailed studies of pest and parasitoid behaviors, their life When the herbivore host of a parasitoid feeds on histories, factors affecting their development, and a narrow range of plants, with similarities in pest-parasitoid interactions in various agro secondary chemistry, better discrimination for the ecosystems. For any effective management parasitoid is possible. However, the choice to strategy whether it involves habitat management, recognize a broad range of plants in many biological control or integration of different control families as harbouring potential host larvae may measures, up to date knowledge of pest and reduce the ability of parasitoids to recognize parasitoid behavior, population dynamics and and respond to qualitative differences among also cautious evolutionary interpretation of plants [152]. tritrophic relationship in a particular agro ecosystem is crucial. Different efficiencies of parasitoids are often correlated with the level of specificity of both host COMPETING INTERESTS and parasitoids [150]. Host-specialist parasitoids are supposed to have greater efficiencies in Authors have declared that no competing searching hosts and have specialized interests exist. adaptations to overcome host defense than generalist species that display relatively plastic REFERENCES foraging behaviours [154]. For instance, the host searching and parasitizing strategies employed by the specialist D. semiclasum are better 1. Talekar NS, Shelton AM. Biology, ecology, adapted than those strategies employed by and management of the diamondback generalist parasitoids [154]. Moreover, D. moth. Ann Rev Entomol. 1993;38:275-301. insulare is an efficient host searcher and shows 2. Sarfraz M, Keddie AB, Dosdall LM. very flexible behavior by sitting motionless near Biological control of the diamondback the silken thread, waiting for the suspended P. moth, Plutella xylostella : A review. xylostella larva to climb up and then attacking it Biocontrol Sci Tech. 2005;15:763-789. again. Sometimes, it may follow down the 3. Anonymous. Canola council of Canada. suspended larva by its silken thread and attempt Canola encyclopaedia. Diamondback quickly to parasitize it [2]. moth. Accessed 15 May 2014. Avaiable: http://www.canolacouncil.org/canola- Many studies indicate that parasitoids often encyclopedia/insects/diamondback-moth/ experience high levels of mortality. Therefore, 4. Furlong MJ, Wright DS, Dosdall LM. selection of hosts should favor developmental Diamondback moth ecology and strategies that maximize progeny survival. It is management: Problems, progress, and also proposed that rapid development time at the prospect. Ann Rev Entomol. cost of size may be preferred in parasitoids 2013;(58):517-541. whose hosts confront high risks of predation 5. Kfir R. Origin of the diamondback moth [155,156]. This indirectly suggests that (Lepidoptera: ). Ann Entomol parasitoids have evolved under selection Soc Am. 1998;91:164 -167. pressures exerted by risks of predation [157].

197

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

6. Ooi PAC. Diamondback moth in Malaysia. Ontario. II. Life history, behavior, and host In : Talekar NS, Griggs TD, editors. relationship. Can Entomol. 1957;12:554- Diamond back Moth Management: 564. Proceedings of the first international 15. Liu S, Chen FZ, Zalucki MP. Development workshop. AVRDC. Shanhua. Taiwan. and survival of the diamondback moth 1986;25-34. (Lepidoptera: Plutellidae ) at constant and 7. Hardy JE. Plutella maculipennis Curt., its alternating temperatures. Environ Entomol. natural and biological control in England. 2002;31:221-231. Bull Entomol Res. 1938;29(4):343-372. 16. Bahar MH, Soroka JJ, Dosdall LM. 8. Harcourt DG. The biology and ecology of Constant versus fluctuating temperatures the diamondback moth, Plutella in the interactions between Plutella maculipennis , Curtis, in Eastern Ontario. xylostella (Lepidoptera: Plutellidae ) and its Cornell Univ., Ithaca, NY. PhD thesis. larval parasitoid Diadegma insulare 1954;107. (Hymenoptera: Ichneumonidae ). Environ 9. Liu S, Wang XG, Guo SJ, He JH, Shi ZH. Entomol. 2012;41:1653-1661. Seasonal abundance of the parasitoid 17. Talekar NS, Liu S, Chen C, Yiin Y. complex associated with the diamondback Characteristics of oviposition of moth, Plutella xylostella (Lepidoptera: diamondback moth ( Lepidoptera: Plutellidae ) in Hangzhou, China. Bull Yponomeutidae ) on cabbage. ZoolStud. Entomol Res. 2000;90(3):221-231. 1994;33(1):72-77. 10. Zalucki MP, Furlong MJ. Predicting 18. Justus KA, Dosdall LM, Mitchell BK. outbreaks of a migratory pest: An analysis Oviposition by Plutella xylostella of DBM distribution and abundance (Lepidoptera: Plutellidae ) and effect of revisited. In: Srinivasan R, Anthony M. phylloplane waxiness. J Econ Entomol. Shelton and Hilda LC. Proceedings: The 2000;93:1152 -1159. Sixth International Workshop on 19. Sarfraz M, Dosdall LM, Keddie BA. Management of the Diamondback Moth Performance of the specialist herbivore and Other Crucifer Insect Pests. Plutella xylostella (Lepidoptera: Plutellidae ) International Workshop on Management of on Brassicaceae and non-Brassicaceae the Diamondback Moth and Other Crucifer species. Can Entomol. 2010;142:24-35. Insect Pests (6th, 2011 ), Nakhon Pathom, 20. Anonymous. Diamondback moth. Thailand. 2011;21-25. Canada’s Green Plan. 1996. Accessed 10 11. Alizadeh M, Rassoulian GR, Karimzadeh September 2013. Available: J, Hosseini-Naveh V, Farazmand H. http://www.agr.gov.sk.ca/docs/crops. Biological study of Plutella xylostella (L.) 21. Ooi PAC, Kelderman W. The biology of (Lep: Plutellidae) and its solitary three common pests of cabbage in endoparasitoid, Cotesia vestalis (Haliday) Cameron Highlands, Malaysia. Malay Agri (Hym. Braconidae) under laboratory J. 1979;52:85-101. conditions. Pak J Bio Sci. 22. Winkler K, Wackers FL, Stingli A, Van 2011;14(24):1090-1099. Lenteren JC. Plutella xylostella 12. Harcourt DG. Population dynamics of the (Diamondback moth) and its parasitoid diamondback moth in southern Ontario. In: Diadegma semiclausum show different Talekar NS, editor. Diamondback moth gustatory and longevity responses to a and other crucifer pests. Proceedings of range of nectar and honey dew sugars. the First International Workshop, 11-15 Entomol Exp Appl. 2005;115:187-192. March 1985. Tainan, Taiwan: Asian 23. Southwood TRE. Migration of terrestrial Vegetable Research and Development in relation to habitat. Biol Rev. Center. 1986;3-16. 1962;37:171-214. 13. Vickers RA, Furlong MJ, White A, Pell JK. 24. Harrison RG. Dispersal polymorphism in Initiation of fungal epizootics in insects. Annu Rev Ecol Syst. 1980;11:95- diamondback moth populations within a 118. large field cage: Proof of concept of auto- 25. Braun L, Olfert O, Soroka J, Mason P, dissemination. Entomol Exp Dosdall LM. Diamondback moth biocontrol Appl.2004;111:7-17. activities in Canada. In: Kirk AA, Bordat D, 14. Harcourt DG. Biology of the diamondback editors. Improving biocontrol of Plutella moth, Plutella maculipennis (Curt.) xylostella . Proceedings of the International (Lepidoptera: Plutellidae ), in Eastern Symposium, 21 -24 October 2002.

198

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

Montpellier, France. 2004;144-146. the crop and predicted effects of climate 26. Coulson SJ, Hodkinson ID, Webb NR, change on its pest status. In: Shelton AM, Mikkola K, Harrison JA, Pedgley DE. Aerial Collins HL, Zhang Y, Wu Q, editors. colonisation of high Artic islands by Proceedings of the Fifth International invertebrates: The diamondback moth Workshop on the Management of Plutella xylostella (Lepidoptera: Diamondback Moth and Other Crucifer Yponomeutidae ) as a potential indicator Pests, Beijing, China. 2008;112-121. species. Divers Distrib. 2002;8:327-334. 35. Dosdall LM. Evidence for successful 27. Dosdall LM, Mason PG, Olfert O, Kaminski overwintering of diamondback moth, L, Keddie BA. The origins of infestations of Plutella xylostellla (L.) ( Lepidoptera: diamondback moth, Plutella xylostella (L.), Plutellidae ), in Alberta. Can Entomol. in canola in western Canada. In: Endersby 1994;126:183 -185. NM, Ridland PM, editors. The 36. Dosdall LM, Soroka JJ, Olfert O. The management of diamondback moth and diamondback moth in canola and mustard: other crucifer pests. Proceedings of the Current pest status and future prospects. Fourth International Workshop, 26-29 Prairie Soils and Crops Journal. 2011;4:66- November 2001. Melbourne. Melbourne, 76. Australia: Department of Natural 37. Campos WG, Schoereder JH, Sperber CF. Resources and Environment. 2004;95-100. Does the age of the host plant modulate 28. Campos WG, Schoereder LH, DeSouza migratory activity of Plutella xylostella ? OF. Seasonality in neotropical populations Entomol Sci. 2004;7:323-329. of Plutella xylostella (Lepidoptera ): 38. Warwick SI, Francis A, Al-Shehbaz IA. Resource availability and migration. Popul Brassicaceae: Species checklist and Ecol. 2006;48:151-158. database on CD-Rom. Plant Syst Evol. 29. Honda K. Hibernation and migration of the 2006;259:249-258. diamondback moth in north Japan. In: 39. Ayalew G, Lohr B, Baumga¨rtner J, Ogol Talekar NS, editor. Diamondback moth CKPO. Diamondback moth, Plutella and other crucifer pests. Proceedings of xylostella (L.) ( Lepidoptera: Plutellidae ) the Second International Workshop, 10 -14 and its parasitoids in Ethiopia. In: Kirk AA, December 1990. Tainan, Taiwan: Asian Bordat D, editors. Improving biocontrol of Vegetable Research and Development Plutella xylostella . Proceedings of the Center. 1992;43 -50. International Symposium, 21-24 October 30. Chapman JW, Reynolds DR, Smith AD, 2002. Montpellier, France. 2004;140-143. Riley JR, Pedgley DE, Woiwod IP. High 40. Sarfraz M, Dosdall LM, Keddie BA. altitude migration of the diamondback moth Resistance of some cultivated Plutella xylostella to the UK: A study using Brassicaceae to infestations by Plutella radar, aerial netting, and ground trapping. xylostella (Lepidoptera: Plutellidae).J Econ Ecol Entomol. 2002;27:641 -650. Entomol. 2007;1:215-224. 31. Goodwin S, Danthanarayana W. Flight 41. Sarfraz M, Dosdall LM, Keddie BA. Host activity of Plutella xylostella (L.) plant genotype of the herbivore Plutella (Lepidoptera: Yponomeutidae ). J Aust xylostella (Lepidoptera: Plutellidae ) affects Entomol Soc. 1984;23:235 -240. the performance of its parasitoid Diadegma 32. Smith DB, Sears MK. Evidence of insulare (Hymenoptera: Ichneumonidae ). dispersal of diamondback moth, Plutella Biol Control. 2008;44:42-51. xylostella (Lepidoptera: Plutellidae ) into 42. Brown J, McCaffrey JP, Harmon BL, Davis southern Ontario. Proceedings of the JB, Brown AP, Erickson DA. Effect of late Entomological Society of Ontario. season insect infestation on yield, yield 1982;113:21 -27. components and oil quality of Brassica 33. Hopkinson RF, Soroka JJ. Air trajectory napus , B. rapa , B. juncea and Sinapis alba model applied to an in-depth diagnosis of in the Pacific Northwest region of the potential diamondback moth infestations United States. J Agric Sci. 1999;132:281- on the Canadian Prairies. Agric For 288. Meteorol. 2010;150:1-11. 43. Srinivasan K, Krishna Moorthy PN. Indian 34. Dosdall LM, Weiss RM, Olfert O, Mason mustard as a trap crop for management of PG, Soroka JJ. 2008. Diamondback major lepidopterous pests on cabbage. moth, Plutella xylostella (L.), as a pest of Trop Pest Manage. 1991;37:26-32. canola in Canada: Its historical impact on

199

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

44. Soufbaf M, Fathipour Y, Karimzadeh J, 54. Ratzka A, Vogel H, Kliebenstein DJ, Zaluck IMP. Development and age-specific Mitchell-Olds T, Kroymann J. Disarming mortality of diamondback moth on brassica the mustard oil bomb. Proceedings of the host plants: Pattern and causes of National Academy of SciencesUSA. mortality under laboratory conditions 2002;99:11223–11228. ecology and population biology. Ann 55. Shelton AM, Nault BA. Dead-end trap Entomol Soc Am. 2010;103:574-579. cropping: a technique to improve 45. Idris AB, Grafius E. Effects of wild and management of the diamondback moth. cultivated host plants on oviposition, Crop Prot. 2004;23:497-503. survival, and development of diamondback 56. Sarfraz MR, Dosdall LM, Keddie BA. moth ( Lepidoptera: Plutelliade ) and its Influence of the herbivore host’s wild food parasitoid Diadegma insulare plants on parasitism, survival and (Hymenoptera: Ichneumonidae ). Environ development of the parasitoid Diadegma Entomol. 1996;25:825-833. insulare. Biol Control. 2012;62:38-44. 46. Golizadeh A, Kamali K, Fathipour Y, 57. Muhamad O, Tsukuda R, Oki Y, Fujisaki K, Abbasipour H. Life table of the Nakasuji F. Influences of wild crucifers on diamondback moth, Plutella xylostella (L.) life historytraits and flight ability of the (Lepidoptera: Plutellidae ) on five cultivated diamondback moth, Plutella xylostella brassicaceous host plants. J Agric Sci (Lepidoptera: Yponomeutidae ). Res Popul Tech. 2009;11:115-124 Ecol. 1994;36:53-62. 47. Silva R, Furlong MJ. Diamondback moth 58. Renwick JAA, Radke CD. Plant oviposition: Effects of host plant and constituents mediating oviposition by the herbivory. Entomol Exp Appl. diamondback moth, Plutella xylostella (L.) 2012;143:218-230. (Lepidoptera: Plutellidae ). Phytophaga. 48. Badenes-Perez FR, Shelton AM, Nault BA. 1990;3:37-46. Evaluating trap crops for diamondback 59. Sarfraz M, Dosdall LM, Keddie BA, Myers moth, Plutella xylostella (Lepidoptera: J. Larval survival, host plant preferences Plutellidae ). J Econ Entomol. and developmental responses of the 2004;97:1365-1372. diamondback moth Plutella xylostella 49. Gathu RK, Lohr B, Poehling HM. (Lepidoptera: Plutellidae ) on wild Development and reproductive potential of brassicaceous species. Entomol Sci. diamondback moth Plutella xylostella 2011;14:20-30. (Lepidoptera: Plutellidae ) on cultivated and 60. Ayalew G, Lohr B, Ogol CKPO, wild crucifer species in Kenya. Intl J Trop Baumgärtner J. Suitability of cultivated and Insect Sci. 2008;28:19-29. wild crucifers for the development of 50. Reddy GVP, Tabone E, Smith MT. diamondback moth, Plutella xylostella L. Mediation of host selection and oviposition (Lepidoptera: Plutellidae ). J Entomol. behavior in the diamondback moth, Plutella 2006;3:82-88. xylostella and its predator, Chrysoperla 61. Begum S, Tsukuda R, Fujisaki K, carnea by chemical cues from cole crops. NakasujiF. The effects of wild cruciferous Bio Control. 2004;29:270-277. host plants on morphology, reproductive 51. Abro GH. Varietal resistance and performance and flight activity in the insecticide efficacy against the diamondback moth, Plutella xylostella diamondback moth , Plutellaxylostella L. (Lepidoptera: Yponomeutidae ). Res Popul PhD Thesis, University of London. Ecol. 1996;38:257-263. 1985;159. 62. Sarfraz M, Dosdall LM, Keddie BA. 52. Abro GH, Jayo AL, Syed TS. Ecology of Evidence for behavioral resistance by the diamondback moth, Plutella xylostella (L.) diamondback moth, Plutella xylostella (L.). in Pakistan. Host plant preference. Pak J J Appl Entomol. 2005;129:340-341. Zool. 1994;26:35-38. 63. Gupta PD, Thornsteinson AJ. Food plant 53. Liu S, Jiang L. Differential parasitism of relationships of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae ) (Plutella maculipennis (Curt)) II. Sensory larvae by the parasitoid Cotesia plutellae relationship of oviposition of the adult (Hymenoptera: Braconidae) on two host female. Entomol Exp Appl. 1960;3:305- plant species. Bull Entomol Res. 314. 2003;93:65-72.

200

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

64. Lohr B. Diamondback moth on peas, Academy of Sciences USA. really. Biocontrol News and Information. 2009;106:18054-18061. 2001;19:38-39N. 76. Wheat CW, Vogel H, Wittstock U, Braby 65. Lohr B, Gathu R. Evidence of adaptation of MF, Underwood D. The genetic basis of a diamondback moth, Plutella xylostella (L.), plant–insect coevolutionary key innovation. to pea, Pisumsativum L. Insect Sci Appl. Proceedings of the National Academy of 2002;22:161-173. Sciences USA. 2007;104:20427–20431. 66. Rossbach, Lohr B, Vidal S. Host shift to 77. Wikstrom N, Savolainen V, Chase MW. peas in the diamondback moth Plutella Evolution of the angiosperms: Calibrating xylostella (Lepidoptera: Plutellidae ) and the family tree. Proceedings of the Royal response of its parasitoid Diadegma Society of London. 2001;268:2211-2220. mollipla (Hymenoptera: Ichneumonidae ). 78. Luthy B, Matile P. The mustard oil bomb: Bull Entomol Res. 2006;96:413-419. rectified analysis of the subcellular 67. Henniges-Janssen K, Reineke A, Heckel organization of myrosinases system. DG, Groot AT. Complex inheritance of Biochemie und Physiologie der Pflanzen. larval adaptation in Plutella xylostella to a 1984;179:5-12. novel host plant. Heredity. 2011;107:421- 79. Sarfraz M, Dosdall LM, Keddie BA. 432. Diamondback moth host plant interactions: 68. Henniges-Janssen K, Schoefl G, Reineke Implications for pest management. Crop A, Heckel DG, Groot AT. Oviposition of Prot. 2006;25:625-639. diamondback moth in the presence and 80. Renwick JAA, Haribal M, Gouinguene S, absence of a novel host plant. Bull Stadler E. Isothiocyanates stimulating Entomol Res. 2011;101:99-105. oviposition by the diamondback moth, 69. Gupta JC. Okra, a new host of Plutella xylostella . J Chem Ecol. diamondback moth. FAO Plant Prot. Bull. 2006;32:755-766. 1971;19:89-90. 81. Siemens DH, Mitchell-Olds T. 70. Knolhoff LM, Heckel DG. Behavioral and Gluosinolates and herbivory by specialists genetic components of a host range (Coleoptera: Chrysomelidae , Lepidoptera: expansion in the diamondback moth. In: Plutellidae ): consequences of Srinivasan R, Shelton AM, Collins HL, concentration and induced resistance. editors. 2011. Proceedings of the Sixth Environ Entomol. 1996;25:1344-1353. International Workshop on Management of 82. Li Q, Eigenbrode SD, Stringam GR, the Diamondback Moth and Other Crucifer Thiagarajah MR. Feeding and growth of Insect Pests, 21 ‐25 March 2011, Kasetsart Plutella xylostella and Spodoptera eridania University, Nakhon Pathom, Thailand. on Brassica juncea with varying AVRDC – The World Vegetable Center, glocosinolate concentrations and Publication No. 11 ‐755. AVRDC – The myrosinase activities. J Chem Ecol. World Vegetable Center, Taiwan. 2000;10:2401-2419. 2011;321. 83. Bidart-Bouzat MG, Kliebenstein DJ. 71. Talekar NS, Yang HC, Lee ST, Chen BS, Differential levels of insect herbivory in the Sun LY. [compilers] . Annotated field associated with genotypic variation in bibliography of diamondback moth. Asian glucosinolates in Arabidopsis thaliana . J Vegetable Research and Development Chem Ecol. 2008;34:1026-1037. Center, Shanhua, Taiwan; 1985. 84. Badenes-Perez FR, Reichelt M, 72. Anonymous. Outbreaks and new records. Gershenzon J, Heckel DG. Phylloplane FAO Plant Prot Bull. 1971;19:89-92. location of glucosinolates in Barbarea spp. 73. Despres L, David JP, Gallet C. The (Brassicaceae ) and misleading evolutionary ecology of insect resistance to assessment of host suitability by a plant chemicals. Trends Ecol Evol. specialist herbivore. New Phytol. 2007;22:298-307. 2011;189:549-556. 74. Hopkins RJ, van Dam NM, van Loon JJA. 85. Abuzid MN, Mohamad Roff MN, Mansour Role of glucosinolates in insect-plant S, Idris AB. Olfactory responses of Plutella relationships and multitrophic interactions. xylostella to Chinese mustard volatiles. Ann Rev Entomol. 2009;54:57-83. The 6th International Workshop on 75. Futuyma DJ, Agrawal AA. Macroevolution Management of the Diamondback Moth and the biological diversity of plants and and Other Crucifer Insect Pests. AVRDC - herbivores. Proceedings of the National The World Vegetable Center. 2011;66-69.

201

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

86. Reddy GVP, Guerrero A. Behavioural (Hymenoptera: Ichneumonidae , responses of diamondback moth, Plutella Campoleginae) attacking the diamondback xylostella , to green leaf volatiles of moth, Plutella xylostella (Lepidoptera: Brassica oleracea subsp. capitata . J Agric Plutellidae ). Bull Entomolo Res. Food Chem. 2000;48:6025-6029. 2000;90:375-389. 87. Satpathy S, Shivalingaswamy TM, Kumar 96. Furlong MJ, Zalucki MP. Parasitoid A, Rai AM, Rai M. Potentiality of Chinese complex of diamondback moth in south- cabbage ( Brassica rapa subsp. east Queensland: First records of Pekinensis ) as a trap crop for Oomyzus sokolowskii (Hymenoptera: diamondback moth ( Plutella xylostella ) Eulophidae ) in Australia. Aust J Entomol. management. Indian J Agric Sci. 2007;46:167-75. 2010;80:240-243. 97. Verkerk RHJ, Wright DJ. Multitrophic 88. Charleston DS, Kfir R. The possibility of interactions and management of the using Indian mustard, Brassica juncea , as diamondback moth: a review. Bull Entomol a trap crop for diamondback moth, Plutella Res.1996;86:205-216. xylostella , in South Africa. Crop Prot. 98. Shi Z, Li Q, Li X, Liu S. Interspecific 2000;19:455-460. competition between Diadegma 89. Agerbirk N, Olsen CE, Bibby BM, semiclausum and Oomyzus sokolowskii , Frandsen HO, Brown L.D, Neilsen JK, parasitoids of diamondback moth, Plutella Renwick JAA. A saponin correlated with xylostella . In: Endersby NM, Ridland PM, variable resistance of Barbarea vulgaris to editors. The management of diamondback the diamondback moth, Plutella xylostella . moth and other crucifer pests. Proceedings J ChemEcol. 2003;29:1417-1433. of the Fourth International Workshop, 26- 90. Zhang PJ, Lu YB, Zalucki MP, Liu SS. 29 November 2001. Melbourne. Relationship between adult oviposition Melbourne, Australia: Department of preference and larval performance of the Natural Resources and Environment. diamondback moth, Plutella xylostella. J 2004;243-248. Pest Sci. 2012;85:247-252. 99. Ooi PAC, Lim GS. Introduction of exotic 91. Marazzi C, Patrian B, Sta¨ dler E. parasitoids to control diamondback moth in Secondary metabolites of the leaf surface Malaysia. J Plant Prot. 1989;6:103-111. affected by sulfur fertilization and 100. Chauhan U, Sharma KC. Status of perceived by the diamondback moth. biocontrol agents of Plutella xylostella (L.) Chemoecology. 2004;14:81-86. (Lepidoptera: Yponomeutidae ) in hilly 92. Sarfraz M, Dosdall LM, Keddie BA. Host areas of the north-west Himalayas, India. plant nutritional quality affects the In: Kirk AA, Bordat D, editors. Improving performance of the parasitoid Diadegma Biocontrol of Plutella xylostella . insulare . Biol Control. 2009;51:34-41. Proceedings of the International 93. Ebrahimi N, Talebi AA, Fathipour Y, Symposium, 21-24 October 2002. Zamani AA. Host plants effect on Montpellier, France. 2004;153-157. preference, development and reproduction 101. Bauer LS. 1995. Resistance: A threat to of Plutella xylostella (L.) ( Lepidoptera: the insecticidal crystal proteins of Bacillus Plutellidae ) under laboratory conditions. thuringiensis . Fla Entomol. 1995;78:414- Adv Enviro Biol. 2008;2:108-114. 443. 94. Liu S, Li Y, Tang Z. Host resistance to an 102. Cherry AJ, Mercadier G, Meikle W, insecticide and selection at larval stage Castelo-Blanco M, Schroer S. The role of favor development of resistance in the entomopathogens in DBM biological parasitoid, Cotesia plutellae . In: Endersby control. In: Kirk AA, Bordat D, editors. NM, Ridland PM, editors. The Improving Biocontrol of Plutella xylostella . management of diamondback moth and Proceedings of the International other crucifer pests. Proceedings of the Symposium, 21-24 October 2002. Fourth International Workshop, 26-29 Montpellier, France.2004;51-70. November 2001. Melbourne. Melbourne, 103. Vandenberg JD, Shelton AM, Wilsey WT, Australia: Department of Natural Ramos M. Assessment of Beauveria Resources and Environment. 2004;227- bassiana sprays for control of 233. diamondback moth ( Lepidoptera: 95. Azidah AA, Fitton MG, Quicke DLJ. Plutellidae ) on crucifers. J Econ Entomol. Identification of the Diadegma species 1998;91:624-630.

202

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

104. Kirk AA, Mercadier G, Bordat D, Delvare (Lepidoptera: Yponumeutidae ). University G, Pichon A, Arvanitakis L, Goude´gnon of Agricultural Sciences, Bangalore. PhD AE, Rincon C. Variability in Plutella and its Thesis. 1997;117. natural enemies: Implications for biological 111. Quan X, WU L, Zhou Q, Yun Y, Peng Y, control. In: Endersby NM, Ridland PM, Chen J. Identification of predation by editors. The management of diamondback spiders on the diamondback moth Plutella moth and other crucifer pests. Proceedings xylostella . Bull Insectology. 2011;64:223- of the Fourth International Workshop, 26- 227. 29 November 2001. Melbourne. 112. Ortiz FM. Biological control of Melbourne, Australia: Department of diamondback moth . The role of predators, Natural Resources and Environment. parasitoids and insecticides. Faculty of 2004;71-77. Natural Resources and Agriculture 105. Woodward DT, Grzywacz D, Winstanely D. Sciences. Department of Ecology. Biological and molecular characterization Uppsala. PhD Thesis; 2011. Available: of granuloviruses isolated from http://pub.epsilon.slu.se/8073/1/miranda_f_ diamondback moth ( Plutella xylostella , 110414.pdf Plutellidae) in Kenya. In: Kirk AA, Bordat 113. Gabriela LV. Interactions between Plutella D, editors. Improving Biocontrol of Plutella xylostella, Diadegma semiclausum and xylostella . Proceedings of the International some generalist predators of brassica Symposium, 21-24 October 2002. crops. University of Adelaide, School of Montpellier, France. 2004;263-266. Agriculture, Food and Wine. PhD Thesis; 106. Cherry AJ, Osae M, Djegui D. Relative 2011. Available: potency, yield and transmission of a http://digital.library.adelaide.edu.au/dspace Kenyan isolate of Plutella xylostella /handle/2440/65487 granulovirus in a population of 114. Delvare G. The taxonomic status and role diamondback moth from Benin, West of Hymenoptera in biological control of Africa. In: Kirk AA, Bordat D, editors. DBM, Plutella xylostella (L.) ( Lepidoptera: Improving Biocontrol of Plutella xylostella . Plutellidae ). In: Kirk AA, Bordat D, editors. Proceedings of the International Improving Biocontrol of Plutella xylostella . Symposium, 21-24 October 2002. Proceedings of the International Montpellier, France. 2004;158-162. Symposium, 21-24 October 2002. 107. Baur ME, Kaya HK, Tabashnik BE, Chilcutt Montpellier, France. 2004;17-49. CF. Suppression of diamondback moth 115. Lim GS. Biological control of diamondback (Lepidoptera: Plutellidae ) with an moth. In: Talekar NS, editor. Diamondback entomopathogenic nematode ( Rhabditida: moth and other crucifer pests. Proceedings Steinernematidae ) and Bacillus of the First International Workshop, 11-15 thuringiensis Berliner. J Econ Entomol. March 1985. Tainan, Taiwan: Asian 1998;91:1089-1095. Vegetable Research and Development 108. Mason JM, Matthews GA, Wright DJ. Center. 1986;159-171. Evaluation of spinning disc technology for 116. Goulet H, Huber JT. Hymenoptera of the the application of entomopathogenic world: An identification guide to families. nematodes against a foliar pest. J Agriculture Canada Publication.1993;668. Invertebr Pathol.1999;73:282–88. 117. Liu S, Wang XG, Guo SJ, He JH, Shi ZH. 109. Idris AB, Zainal-Abidin BAH, Sajap AS, Seasonal abundance of the parasitoid Noran AM, Hussan AK. Some studies on complex associated with the diamondback Nosema infecting DBM in Malaysia. In: moth, Plutella xylostella (Lepidoptera: Endersby NM, Ridland PM, editors. The Plutellidae ) in Hangzhou, China. Bull management of diamondback moth and Entomol Res. 2000;90:221-231. other crucifer pests. Proceedings of the 118. Noyes JS. The reliability of published host- Fourth International Workshop, 26-29 parasitoid records: A taxonomist’s view. November 2001. Melbourne. Melbourne, Norwegian Journal of Agricultural Australia: Department of Natural Sciences. 1994;16: 59-69. Resources and Environment. 2004;295- 119. Thompson WR. A catalogue of the 303. parasites and predators of insect pests. 110. Anuradha M. Possibility on integration of Section 1; Parasite Host Catalogue: Part 7; bio-agent for the management of Parasites of Lepidoptera (G-M):259-185. diamondback moth, Plutella xylostella (L.)

203

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

Imperial Agricultural Bureau, Belleville, Natural Resources and Environment. Ontario, Canada. 1946. 2004;249-253. 120. Goodwin S. Changes in numbers in 128. Guilloux T, Monnerat R, Castelo-Brancho parasitoid complex associated with the M, Kirk AA, Bordat D. Population dynamics diamondback moth, Plutella xylostella (L.) of Plutella xylostella (Lepidoptera: (Lepidoptera ) in Victoria. Aust J Zool. Yponomeutidae ) and its parasitoids in the 1979;27:981-989. region of Brasilia. In: Kirk AA, Bordat D, 121. Mustata G. Role of parasitoid complex in editors. Improving Biocontrol of Plutella limiting the population of diamondback xylostella . Proceedings of the International moth in Moldavia, Romania. In: Talekar Symposium, 21-24 October 2002. NS, editor. Diamondback moth and other Montpellier, France. 2004;184-189. crucifer pests. Proceedings of the Second 129. Yu DS, Horstmann K. A catalogue of world International Workshop, 10-14 December Ichneumonidae (Hymenoptera ). Memoirs 1990. Tainan, Taiwan. Asian Vegetable of the American Entomological Institute. Research and Development Center. 1997;58:1-1558. 1992;203-212. 130. Wagener B, Reineke A, Lohr B, Zebitz 122. Fitton M, Walker A. Hymenopterous CPW. Molecular identification of Diadegma parasitoids associated with diamondback species ( Ichneumonidae ) parasitizing moth: Taxonomic dilemma. In: Talekar NS, diamondback moth, Plutella xylostella editor. Diamondback moth and other (Plutellidae) in eastern and southern crucifer pests. Proceedings of the Second Africa. In: Kirk AA, Bordat D, editors. International Workshop, 10-14 December Improving Biocontrol of Plutella xylostella . 1990. Tainan, Taiwan. Asian Vegetable Proceedings of the International Research and Development Center. Symposium, 21-24 October 2002. Shanhua, Taiwan. 1992;225-232. Montpellier, France. 2004;252-257. 123. Todd DH. Incidence and parasitism of 131. Harcourt DG. Biology of cabbage insect pests of cruciferous crops in the caterpillars in Eastern Ontario. North Island, evaluation of data, 1955-58 Proceedings of the Entomological Society seasons. New Zeal J Agr Res. 1959;2:613- Ontario. 1963;83:61-75. 622. 132. Biever KD, Hostetter DL, Kern JR. 124. Kfir R. Parasitoids of Plutella xylostella Evolution and implementation of biological (Lepidoptera: Plutellidae ) in South Africa: control-IPM system for crucifers, 24 year An annotated list. Entomophaga. case history. American Entomologist. 1997;42:517 -523. 1994;40:103-108. 125. Lim GS. Integrated pest management of 133. Mitchell ER, Hu GY, Okine JS. diamondback moth. In: Talekar NS, editor. Diamondback moth ( Lepidoptera: Diamondback Moth and Other Crucifer Plutellidae ) infestation and parasitism by Pests: Proceedings of the Second Diadegma insulare (Hymenoptera: International Workshop. Tainan, Taiwan, Ichneumonidae ) in collards and adjacent 10-14 December 1990. Asian Vegetable cabbage fields. Florida Entomologist. Research and Development Center, 1997;80:54-62. Shanhua, Taiwan. 1992;565-576. 134. Dosdall LM, Mason PG. Key pests and 126. Lohr B, Kfir R. Diamondback moth Plutella parasitoids of oilseed rape or canola in xylostella (L.) in Africa. A review with North America and the importance of emphasis on biological control. In parasitoids in integrated management. In Improving Biocontrol of Plutella xylostella. Biocontrol-Based Integrated Management In: Kirk AA, Bordat D, editors. CIRAD, of Oilseed Rape Pests, ed. IH Williams. Montpellier, France. 2004;71-83. Dordrecht/London: Springer. 2010;167- 127. Smith TJ, Villet MH. Parasitoids associated 213. with the diamondback moth, Plutella 135. Sourakov A, Mitchell ER. Featured xylostella (L.), in the Eastern Cape, South Creatures. USDA. 2000. Accessed 10 Africa. In: Endersby NM, Ridland PM, March 2014. Available: editors. The management of diamondback http//creatures.ifas.edu/wasps/ moth and other crucifer pests. Proceedings diadegma_insulare.htm. of the Fourth International Workshop, 26- 136. Putnam LG. Experiments in the 29 November 2001. Melbourne. quantitative relationships between Melbourne, Australia: Department of Diadegma insularis (Hymenoptera:

204

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

Ichneumonidae ) and Microplitis plutellae 146. Sumerford DV, Abrahamson WG, Weis (Hymenoptera: Braconidae) with their host AE. The effects of drought on the Solidago Plutella maculipennis (Lepidoptera: altissima–Eurosta solidaginis– natural Plutellidae ). Can Entomol. 1968;100:11-16. enemy complex: Population dynamics, 137. Fox LR, Letourneau DK, Eisenbach J, local extirpations, and measures of Nouhuys SV. Parasitism rates and sex selection intensity on gall size. Oecologia. ratios of a parasitoid : Effects of 2000;122:240-248. herbivore and plant quality. Oecologia. 147. Teder T, Tammaru T. Cascading effects of 1990;83:414-419. variation in plant vigor on the relative 138. Monnerat RG, Kirk AA, Bordat ED. Biology performance of insect herbivores and their of Diadegma sp. ( Hymenoptera: parasitoids. Ecol Entomol. 2002;27:94-104. Ichneumonidae ), a parasitoid of Plutella 148. Ulmer BJ, Dosdall LM, Gibson GAP. xylostella (L.) ( Lepidoptera: Spatio-temporal distribution patterns of the Yponomeutidae ), from Reunion Island. diamondback moth and its principal Neotrop Entomol. 2002;31:271-274. parasitoid, Diadegma insulare , in canola 139. Harcourt DG. Biology of the diamondback crops and the occurrence of moth, Plutella maculipennis (Curt.) hyperparasitism. Brassica. 2005;6:63-69. (Lepidoptera: Plutellidae ), in eastern 149. Vet LEM, Dick M. Ecology of infochemicals Ontario. III. Natural enemies. Can Entomol. use by natural enemies in tritrophic 1960;29:419-428. contest. Ann Rev Entomol. 1992;37:141- 140. Bolter CJ, Laing JE. Competition between 172. Diadegma insulare (Hymenoptera: 150. GodfrayHCJ. Parasitoids. Behavioral and Ichneumonidae ) and Microplitis plutellae Evolutionary Ecology. Princeton University (Hymenoptera: Braconidae) for larvae of Press, Princeton University Press, diamondback moth, Plutella xylostella Princeton, New Jersey; 1994. (Lepidoptera: Plutellidae ). Proceedings of 151. Idris AB, Grafius E. Nectar-collecting the Entomological Society of Ontario. behavior of Diadegma 1983;14:1-10. insulare (Hymenoptera: Ichneumonidae ), a 141. Idris AB, Grafius E. Evidence of Diadegma parasitoid of diamondback moth, Plutella insulare (Cresson), a parasitoid of xylostella L. Environ Entomol. diamondback moth, Plutella xylostella (L.), 1997;26:114-120. present in various habitats. Pak J Biol Sci. 152. Fox LR, Kester KM, Eisenbach J. Direct 2001;1:742-743. and indirect responses of parasitoids to 142. Lee JC, Heimpel GE. Floral resources plants: Sex ratio, plant quality and impact longevity and oviposition rate of a herbivore diet breadth. Entomol Exp Appl. parasitoid in the field. J Anim Ecol. 1996;80:289-292. 2008;77:565-572. 153. McCormick AC, Sybille BU, Gershenzon J. 143. Johanowicz DL, Mitchell ER Effects of The specificity of herbivore-induced plant sweet alyssum flowers on the longevity of volatiles in attracting herbivore enemies. the parasitoid Cotesia Trends Plant Sci. 2012;17:303-310. marginiventris (Hymenoptera: Braconidae ) 154. Wang XG, Keller MA. A comparison of and Diadegma insulare (Hymenoptera: host searching efficiency of two larval Ichneumonidae ). Fla Entomol. 2000;83:41- parasitoids of Plutella xylostella. Ecol 47. Entomol. 2002;27:105-114. 144. Grafius EJ, Idris AB. Know your friends: 155. Whitfield JB. Phylogeny and evolution of Diadegma insulare , parasite of host–parasitoid interactions in diamondback moth. Midwest Biological Hymenoptera. Ann Rev Entomol. Control. 1997. Accessed 10 September 1998;43:129-151. 2013. Available: 156. Quicke DLJ, Fitton MG, Notton DG, Broad http://www.entomology.wisc.edu/mbcn/kyf4 GR, Dolphin K. Phylogeny of the 01.html Ichneumonidae (Hymenoptera ): A 145. Moon DC, Rossi AM, Stiling P. The effects simultaneous molecular and morphological of abiotically induced changes in host plant analysis. In Proceedings of the Fourth quality and morphology on a salt marsh International Hymenopterists Conference. plant hopper and its parasitoid. Ecol Canberra, Australia; 2000. Entomol. 2000;25:325-331. 157. Harvey JA, Strand MR. The developmental strategies of endoparasitoid wasps vary

205

Munir et al.; ARRB, 5(3): 189-206, 2015; Article no.ARRB.2015.021

with host feeding ecology. Ecology. Press, Princeton, New Jersey, USA. 2002;83:2349-2451. 2000;163-183. 158. Rosenheim JA, Kaya HK, Ehler LE, Marois 161. Shaw MR. Parasitoid host ranges. In: JJ, Jaffee BA. Intraguild predation among Hawkins BA, Sheehan W, editors. biological control agents: Theory and Parasitoid community Ecology. Oxford evidence. Biol Control. 1995;5:303-335. University Press, Oxford, UK. 1994;11- 159. Rosenheim JA. Higher-order predators and 144. the regulation of insect herbivore 162. Stiling P, Rossi AM. The window of populations. Ann Rev Entomol. parasitoid vulnerability to hyperparasitism: 1998;43:421-447. Template for parasitoid complex structure. 160. Brodeur J. Host specificity and trophic In: Hawkins BA, Sheehan W, editors. relationships of hyperparasitoids. In: Parasitoid Community Ecology. Oxford Hochberg ME, Ives AR, editors. Parasitoid University Press, Oxford, UK. 1994;228- Population Biology. Princeton University 244. ______© 2015 Munir et al.; This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0 ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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