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Biocontrol Science and Technology

ISSN 0958-3157 (Print) 1360-0478 (Online) Journal homepage httpwwwtandfonlinecomloicbst20

Plant-mediated vulnerability of an insect herbivoreto Bacillus thuringiensis in a plant-herbivore-pathogen system

Maryam Jafary Javad Karimzadeh Hossein Farazmand amp MohammadrezaRezapanah

To cite this article Maryam Jafary Javad Karimzadeh Hossein Farazmand amp MohammadrezaRezapanah (2016) Plant-mediated vulnerability of an insect herbivore to Bacillus thuringiensisin a plant-herbivore-pathogen system Biocontrol Science and Technology 261 104-115 DOI1010800958315720151078872

To link to this article httpdxdoiorg1010800958315720151078872

Accepted author version posted online 04Aug 2015Published online 26 Oct 2015

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RESEARCH ARTICLE

Plant-mediated vulnerability of an insect herbivore to Bacillusthuringiensis in a plant-herbivore-pathogen systemMaryam Jafarya Javad Karimzadehb Hossein Farazmandc andMohammadreza Rezapanahd

aDepartment of Entomology College of Agriculture Arak Branch Islamic Azad University Arak IranbDepartment of Plant Protection Isfahan Research and Education Center for Agriculture and NaturalResources Agricultural Research Education and Extension Organization (AREEO) Isfahan Iran cDepartmentof Agricultural Entomology Iranian Research Institute of Plant Protection AREEO Tehran Iran dDepartmentof Biological Control Iranian Research Institute of Plant Protection AREEO Tehran Iran

ABSTRACTLaboratory studies were performed to explore the effects of host-plant quality on the vulnerability of Plutella xylostella to Bacillusthuringiensis P xylostella were kept on different host plantsincluding Brassica pekinensis (Chinese cabbage) cv Hero Brassicaoleracea var botrytis (cauliflower) cv Royal and B oleracea varcapitata (common cabbage) cv Globe Master (white cabbage) andcv Red Dynasty (red cabbage) for at least two generations Thesehost plants are considered as the high (Chinese cabbage)intermediate (cauliflower and white cabbage) and low-quality (redcabbage) hosts for P xylostella The vulnerability of the pest larvaewas then tested using two formulation of B thuringiensis varkurstaki including Biolarvreg and Biolepreg The results demonstratedthat the susceptibility of P xylostella to B thuringiensis wasinfluenced by host-plant quality Indeed B thuringiensis actedbetter on the pest fed on the low-quality host plant comparedwith that on the high-quality host plant The interaction betweenthe pathogen and plant qualityresistance resulted in moremortality of the pest larvae implying a synergistic effect From apest management viewpoint these findings may be promising forthe integration of the pathogen and the low-qualitypartiallyresistant host plants against P xylostella in field studies

ARTICLE HISTORYReceived 2 January 2015Revised 19 July 2015Accepted 29 August 2015

KEYWORDSPlutella Bacillus host planttritrophic bottom-upsustainable strategies

1 Introduction

Host-plant resistance is a paramount component of sustainable pest management (Andra-hennadi amp Gillott 1998 Sarfraz Dosdall amp Keddie 2006) Plant resistance can happen viaone factor or a combination of factors such as antibiosis antixenosis and tolerance(Sarfraz Dosdall amp Keddie 2007) For example the mechanism of resistance in glossyBrassica oleracea to attack by the diamondback moth Plutella xylostella (L) (LepidopteraPlutellidae) is reduced larval survival (Ulmer Gillott Woods amp Erlandson 2002) Growthand reproduction of insect herbivores are affected by plant quality either via nutritionalquality or via the effects of plant defensive compounds (Awmack amp Leather 2002) In

copy 2015 Taylor amp Francis

CONTACT Javad Karimzadeh jkarimzadehirippir

BIOCONTROL SCIENCE AND TECHNOLOGY 2015VOL 26 NO 1 104ndash115httpdxdoiorg1010800958315720151078872

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addition insect defensive characteristics might be influenced by plant quality variabilityHost-plant suitability may indeed alter the fitness costs of pesticide resistance ofherbivorous insects (Janmaat amp Myers 2007)

Ecological pest management programmes attempt to combine host-plant resistancewith biocontrol but the compatibility of these two strategies may vary with the specificagro-ecosystem (Karimzadeh Bonsall amp Wright 2004 Karimzadeh Hardie amp Wright2013) Host plant may positively or negatively affect the third tritrophic level includingparasitoids predators and pathogens (Karimzadeh amp Wright 2008 Schuler amp vanEmden 2000) The tritrophic interactions between host plants insect herbivores andtheir parasitoids (Gols et al 2007 Karimzadeh et al 2004 2013 Sarfraz Dosdall ampKeddie 2008 Schuler Denholm Clark Stewart amp Poppy 2004) or their pathogens (Gass-mann Stock Tabashnik amp Singer 2010 Janmaat Ware amp Myers 2007 Karimzadeh ampSayyed 2011 Raymond Sayyed amp Wright 2007) are well documented The plant nutri-tional defensive or physical characteristics might mediate such influential multitrophicinteractions

Plutella xylostella has been reported as the most devastative pest of crucifers worldwide(Furlong Wright amp Dosdall 2013 Talekar amp Shelton 1993) In recent decades resistancein the field to all the classes of synthetic insecticide by P xylostella has occurred (Sheltonet al 1993) This has urgently promoted the assessment of more ecological strategies ofpest management such as biocontrol host-plant resistance and cultural control Successfulcontrol of P xylostella has been achieved by using different strains of the microbial biopes-ticideBacillus thuringiensisBerliner (Bacillales Bacillaceae) or its toxins Beside its high tox-icity to some insect pests B thuringiensis (Bt) has shown little or no toxicity to non-targetorganisms including beneficial insects (Tabashnik Finson amp Johnson 1991) The Bt insec-ticidal crystal proteins act by binding to and creating pores in insect midgut membranes Inaddition the spores of Bt increase the toxicity of its crystals to P xylostella larvae (LiuTabashnik Moar amp Smith 1998 Schnepf et al 1998 Syed amp Abro 2003)

The interaction between host-plant suitability and Bt may have different effects on thetarget pest based on the compatibility of these sustainable strategies The present studyaimed to examine the influence of host-plant suitability on vulnerability of a herbivore(P xylostella larvae) to a pathogen (Bt) Here it was shown that host plant-mediated influ-ences on an insect herbivore can determine hostndashpathogen interactions The cascadingeffect of variation in plant quality on the third trophic level is indicative of a strongbottom-up effect in a plant-herbivore-pathogen system

2 Materials and methods

21 Plants and insects

Chinese cabbage (Brassica pekinensis) cv Hero common cabbage (Brassica oleracea varcapitata) cv Globe Master (white cabbage) and cauliflower (B oleracea var botrytis) cvRoyal were grown under greenhouse conditions (25 plusmn 5degC and LD 168 h) without theapplication pesticide In addition common cabbage cv Red Dynasty (red cabbage)was grown in the field The 4ndash6-week-old Chinese cabbage and 6ndash8-week-old commoncabbages and cauliflower were used in experiments Plutella xylostella (originally fromIsfahan province central Iran) cultures were maintained on above-mentioned host

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plants in ventilated oviposition cages (40 times 40 times 40 cm) under standard constantconditions (25 plusmn 2degC 70 plusmn 5 RH LD 168 h) Insects were cultured on each host plantfor two generations before using them for the experiments (Karimzadeh et al 2004Schuler amp van Emden 2000)

22 Herbivore performance

To obtain synchronized eggs of P xylostella one plant 30 pairs (male and female) of newlyemerged P xylostella adults (reared from the same host plant) and aqueous honeysolution (20) were placed in each oviposition cage for 24 h Batches of 10 neonateP xylostella larvae were placed on leaf discs (58 cm dia) within individual Petri dishes(6 cm dia) containing a moistened filter paper Leaf discs were cut from randomly selectedleaves on different plants for each plant group used in experiments To prevent starvationof larvae the leaf discs were replaced every 24 h Pupae were transferred to separate Petridishes and kept until eclosion The experiments were conducted under controlled environ-ment conditions (25 plusmn 1degC 65 plusmn 5 RH LD 168 h) Life stage and mortality wererecorded every 24 h until all insects had either died or emerged as adults The meantime from oviposition to pupation and eclosion the survival percentage and pupalweight were calculated (Karimzadeh amp Wright 2008) Each treatment was replicated 17times based on the results from a preliminary experiment (Karimzadeh 2011)

23 Dose-response bioassays

Plutella xylostella larvae were treated with two commercial formulations of B thuringiensisvar kurstaki including Biolarvreg (3A3B 5 Agrimix Roma Italy) and Biolepreg (108 cellmlTabiatgera Karaj Iran) both containing δndashendotoxin crystals and viable spores The testproducts were freshly prepared in distilled water with Tween20reg (002) as a surfactantTo determine CFU three concentrations of Biolarvreg (10minus3 10minus6 and 10minus9) and Biolepreg

(10minus6 10minus9 and 10minus12) suspensions were prepared The suspensions (100 microl) were thenspread on the surface of nutrient agar (Merkreg Germany) plates which were incubatedfor 24 h at 27degC Each concentration was replicated four times The visible colonieswere counted and used as an index for calculating CFU (Izadyar Talebi-JahromiAskary amp Rezapanah 2003) To perform the bioassay the leaf discs (58 cm dia) of thehost plants were immersed in the test solution for 10 s and then kept on a corrugatedsheet of aluminium foil with the adaxial leaf surface uppermost for 2 h at room tempera-ture to dry up Control leaf discs were immersed in distilled water containing Tween20reg

(002) The leaf discs were then transferred to individual plastic Petri dishes (6 cmdia) containing a moistened filter paper Five third-instar larvae of P xylostella werethen placed on each leaf disc The leaf discs were then replaced every 24 h with freshuntreated ones Mortality was recorded after five days Six concentrations were used forBiolarv (375 times 10minus1 375 times 101 375 times 103 375 times 105 375 times 107 375 times 109 CFUml)and Biolep (295 times 102 295 times 104 295 times 106 295 times 108 295 times 1010 295 times 1012 CFUml) All the concentrations as well as the control treatment were replicated eight timesAll the bioassays were performed under the standard environment conditions (25 plusmn 2degC 70 plusmn 5 RH LD 168 h Karimzadeh amp Sayyed 2011 Sayyed Raymond Ibiza-PalaciosEscriche amp Wright 2004) In all the experiments the institutional and national guidelines

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for the care and use of laboratory animals (Institutional Animal Care and Use CommitteeGuidebook) were followed

24 Statistical analysis

Differences in the survival rates among host-plant types were analyzed using logisticanalysis of deviance (binomial error) The developmental periods and pupal weightwere analyzed using nested ANOVA where the individual larvae were nested withinPetri dishes and Petri dishes were nested within plants For these data a Petri dish (con-taining 10 individual larvae) was considered as a replication and the treatments (four hostplants) were replicated 17 times The dose-response data were corrected using Abbottrsquosformula and analyzed using probit analysis where regression lines were fitted to dose-mortality data on a log-probit scale and the estimated LC50s and associated confidenceintervals (CI) were then calculated from the estimated linear regression parameters Inaddition to compare the independent and combined effects of host plants and Bt formu-lations differences in percentage mortalities between host-plant types Bt formulationsand concentrations were analyzed using Analysis of Covariance after correction andarcsine transformation For these data a Petri dish (containing five individual larvae)was considered as a replication and the treatments (six different concentrations of eachBt formulation as well as the control) were replicated eight times Pairwise comparisonswere performed using Least Significant Difference (LSD) or Tukeyrsquos Honestly SignificantDifference (HSD Crawley 2013 Day amp Quinn 1989) All statistical analyses were com-pleted in R 2100 (R Development Core Team)

3 Results

31 Host-plant effects on P xylostella performance

There was a significant effect of host plant on P xylostella larval periods (F376 = 10119P lt 0001) The mean larval period of P xylostella on the red cabbage (1689 plusmn 053 days)was significantly greater than that on white cabbage (1132 plusmn 028 days) cauliflower(1029 plusmn 027 days) or Chinese cabbage (810 plusmn 007 days Table 1) However no signifi-cant influence of host plants on the pupal period of P xylostella was observed (F376 =154 P = 019 Table 1) In addition when sum of larval and pupal period was analyzedthere was a significant effect of host plant (F376 = 973 P lt 0001) such that the shortestand longest developmental period of P xylostella was obtained when the insect fed onChinese cabbage (1171 plusmn 046 days) and red cabbage (2098 plusmn 200 days) respectively(Table 1) The effect of host plant on the pupal weight of P xylostella was also significant

Table 1 Host-plant effects on developmental periods and pupal weight of P xylostellaDevelopmental periods (mean plusmn SE days) Pupal weight

(mean plusmn SE mg)Host plant L1-Adult Pupal L1-pupa

Chinese cabbage 1171 plusmn 046 a 361 plusmn 020 a 810 plusmn 007 aa 432 plusmn 006 aWhite cabbage 1505 plusmn 071 ab 373 plusmn 032 a 1132 plusmn 028 b 381 plusmn 011 abCauliflower 1444 plusmn 054 ab 415 plusmn 024 a 1029 plusmn 027 b 380 plusmn 006 bRed cabbage 2098 plusmn 200 b 409 plusmn 044 a 1689 plusmn 053 c 366 plusmn 019 baThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

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(F376 = 2697 P lt 0001 Table 2) The mean pupal weight of P xylostella on Chinesecabbage (432 plusmn 006 mg) was significantly greater than cauliflower (380 plusmn 006 mg)and red cabbage (366 plusmn 019 mg Table 1) Host plant had significant influences onthe larval (F380 = 5283 P lt 0001) and on L1-adult (F380 = 4414 P lt 0001) survivalrate of P xylostella Mean survival rate of both the larvae and the sum of larvae andpupae of P xylostella was significantly greater on Chinese cabbage compared withcommon cabbages (Table 2) But no significant difference for pupal survival rate(F375 = 178 P = 013) between the host plants was found

32 Host-plant effects on the Bt dose-mortality response

The results of CFU test showed that the number of viable spores of Biolarvreg and Biolepreg

were 375 times 1011 and 295 times 1014 CFUml respectively (Table 3) The probit analysisshowed that LC50 of Biolarvreg significantly varied among host plants such that LC50 ofBiolarvreg was significantly greater on Chinese cabbage compared with red cabbageHowever there was no significant difference between LC50 of Biolepreg on different hostplants (Table 3) The analysis of covariance (Table 4) showed that both the host plant(F3368 = 1543 P lt 0001) and Bt formulation (F1368 = 763 P lt 001) had significanteffects on the mortality of P xylostella larvae the proportion mortality of P xylostellalarvae was highest and lowest on red cabbage (068) and Chinese cabbage (038) respect-ively (Table 5 Figure 1) Furthermore the proportion P xylostella larvae killed by Biolarvreg

(057) was significantly greater than that for Biolepreg (049) There was however no signifi-cant interaction (F3368 = 054 P = 065) between host plant and formulation for theireffects on P xylostella larval mortality (Table 4) In addition there was a significant

Table 2 Host-plant effects on survival rate of P xylostella

Host plant

Survival rate (mean plusmn SE )

L1-pupa Pupal L1-adult

Chinese cabbage 8353 plusmn 542 aa 8592 plusmn 355 a 7176 plusmn 608 aCauliflower 6824 plusmn 509 ab 9052 plusmn 302 a 6175 plusmn 494 abWhite cabbage 4765 plusmn 597 b 9012 plusmn 391 a 4294 plusmn 574 bRed cabbage 2000 plusmn 462 c 8235 plusmn 526 a 1647 plusmn 383 caThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

Table 3 The effects of host-plant species on the susceptibility of P xylostella larvae to B thuringiensis

Bt Number of viablespores (CFUml) Host plant

Lethal dose (grml or mlml)a

Slopeplusmn SE PFormulation LC50 95 CI (n = 8)

Biolarvreg(WP) 375 times 1011 Chinesecabbage

23 times 10minus4 799 times 10minus6minus194 times 10minus1 045 plusmn 008 lt0001

White cabbage 124 times 10minus5 153 times 10minus6minus34 times 10minus3 051 plusmn 008 lt0001Cauliflower 945 times 10minus6 983 times 10minus7minus240 times 10minus2 043 plusmn 008 lt0001Red cabbage 197 times 10minus7 833 times 10minus8minus319 times 10minus6 040 plusmn 007 lt0001

Biolepreg(SC) 295 times 1014 Chinesecabbage

420 times 10minus4 223 times 10minus5minus48 times 10minus1 057 plusmn 007 lt0001

White cabbage 899 times 10minus5 449 times 10minus6minus017 times 10minus1 042 plusmn 008 lt0001Cauliflower 135 times 10minus5 229 times 10minus6minus590 times 10minus4 057 plusmn 007 lt0001Red cabbage 435 times 10minus6 691 times 10minus7minus940 times 10minus4 045 plusmn 008 lt0001

aLC50 units for Biolarvreg and Biolepreg respectively

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interaction (F3368 = 388 P lt 001) between plant type and Bt concentration (Table 4) as itcan be seen more clearly in Figure 1 for the Biolep formulation there is a significant differ-ence in mortality among the plant species at the lower concentrations but not at the higherconcentrations

4 Discussion

Using the laboratory experiments we demonstrate that host plant quality-mediatedeffects on an insect herbivore might be determinative in hostndashpathogen interactions Inparticular it was indicated that the species of the host plant may influence the suscepti-bility of the diamondback moth to Bt Host-plant quality clearly had a direct effect onthe herbivore performance the different stages of P xylostella developed faster and per-formed better on the high-quality host plant (Chinese cabbage) compared with intermedi-ate (white cabbage and cauliflower) or low-quality (red cabbage) host plants In additionthe lowest LC50 value of Bt against P xylostella larvae fed on red cabbage compared withother host plants demonstrated that the entomopathogen acts better on the herbivorelarvae that suffered from low plant quality Such an indirect effect of plant quality onthe third trophic level is indicative of a strong bottom-up cascading effect in a tritrophicsystem

The plant characteristics such as trichomes domatia or semiochemicals may havedirect or indirect (through alteration of herbivore physiology or behaviour) effects onnatural enemies For example diverse life history traits of viral pathogens and parasi-toids can be affected by variation in host-plant chemistry (Karimzadeh et al 2004Raymond et al 2002) The plant nutritional defensive or physical characteristics can

Table 4 Analysis of covariance of the effects of host plant Bt formulation and concentration onP xylostella mortalitySource Df Sum Sq Mean Sq F value P value

Plant 3 438 146 1543 lt0001Formulation 1 072 072 763 lt001Concentration 1 7236 7236 76516 lt0001Plant Formulation 3 015 005 054 065Plant Concentration 3 110 037 388 lt001Formulation Concentration 1 006 006 063 043Plant Formulation Concentration 3 029 010 102 039Residuals 368 3480 010

Table 5 The effects of host-plant species on the mortality of P xylostella larvae by B thuringiensis

Host plant

Proportion mortality of P xylostella larvae (mean plusmn SE)a

Bt formulationBiolarvreg Biolepreg Overall

Chinese cabbage 042 plusmn 008 033 plusmn 008 038 plusmn 006 ab

White cabbage 053 plusmn 008 050 plusmn 007 052 plusmn 005 bCauliflower 058 plusmn 008 051 plusmn 008 054 plusmn 006 bRed cabbage 075 plusmn 007 061 plusmn 008 068 plusmn 005 cOverall 057 plusmn 004 Ac 049 plusmn 004 BaThe mean proportional mortality of the total bioassay dosesbThe different letters within the column show a significant (P lt 005) difference (Tukeyrsquos HSD)cThe different capital letters within the row show a significant (P lt 005) difference (Tukeyrsquos HSD)

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

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plants in ventilated oviposition cages (40 times 40 times 40 cm) under standard constantconditions (25 plusmn 2degC 70 plusmn 5 RH LD 168 h) Insects were cultured on each host plantfor two generations before using them for the experiments (Karimzadeh et al 2004Schuler amp van Emden 2000)

22 Herbivore performance

To obtain synchronized eggs of P xylostella one plant 30 pairs (male and female) of newlyemerged P xylostella adults (reared from the same host plant) and aqueous honeysolution (20) were placed in each oviposition cage for 24 h Batches of 10 neonateP xylostella larvae were placed on leaf discs (58 cm dia) within individual Petri dishes(6 cm dia) containing a moistened filter paper Leaf discs were cut from randomly selectedleaves on different plants for each plant group used in experiments To prevent starvationof larvae the leaf discs were replaced every 24 h Pupae were transferred to separate Petridishes and kept until eclosion The experiments were conducted under controlled environ-ment conditions (25 plusmn 1degC 65 plusmn 5 RH LD 168 h) Life stage and mortality wererecorded every 24 h until all insects had either died or emerged as adults The meantime from oviposition to pupation and eclosion the survival percentage and pupalweight were calculated (Karimzadeh amp Wright 2008) Each treatment was replicated 17times based on the results from a preliminary experiment (Karimzadeh 2011)

23 Dose-response bioassays

Plutella xylostella larvae were treated with two commercial formulations of B thuringiensisvar kurstaki including Biolarvreg (3A3B 5 Agrimix Roma Italy) and Biolepreg (108 cellmlTabiatgera Karaj Iran) both containing δndashendotoxin crystals and viable spores The testproducts were freshly prepared in distilled water with Tween20reg (002) as a surfactantTo determine CFU three concentrations of Biolarvreg (10minus3 10minus6 and 10minus9) and Biolepreg

(10minus6 10minus9 and 10minus12) suspensions were prepared The suspensions (100 microl) were thenspread on the surface of nutrient agar (Merkreg Germany) plates which were incubatedfor 24 h at 27degC Each concentration was replicated four times The visible colonieswere counted and used as an index for calculating CFU (Izadyar Talebi-JahromiAskary amp Rezapanah 2003) To perform the bioassay the leaf discs (58 cm dia) of thehost plants were immersed in the test solution for 10 s and then kept on a corrugatedsheet of aluminium foil with the adaxial leaf surface uppermost for 2 h at room tempera-ture to dry up Control leaf discs were immersed in distilled water containing Tween20reg

(002) The leaf discs were then transferred to individual plastic Petri dishes (6 cmdia) containing a moistened filter paper Five third-instar larvae of P xylostella werethen placed on each leaf disc The leaf discs were then replaced every 24 h with freshuntreated ones Mortality was recorded after five days Six concentrations were used forBiolarv (375 times 10minus1 375 times 101 375 times 103 375 times 105 375 times 107 375 times 109 CFUml)and Biolep (295 times 102 295 times 104 295 times 106 295 times 108 295 times 1010 295 times 1012 CFUml) All the concentrations as well as the control treatment were replicated eight timesAll the bioassays were performed under the standard environment conditions (25 plusmn 2degC 70 plusmn 5 RH LD 168 h Karimzadeh amp Sayyed 2011 Sayyed Raymond Ibiza-PalaciosEscriche amp Wright 2004) In all the experiments the institutional and national guidelines

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for the care and use of laboratory animals (Institutional Animal Care and Use CommitteeGuidebook) were followed

24 Statistical analysis

Differences in the survival rates among host-plant types were analyzed using logisticanalysis of deviance (binomial error) The developmental periods and pupal weightwere analyzed using nested ANOVA where the individual larvae were nested withinPetri dishes and Petri dishes were nested within plants For these data a Petri dish (con-taining 10 individual larvae) was considered as a replication and the treatments (four hostplants) were replicated 17 times The dose-response data were corrected using Abbottrsquosformula and analyzed using probit analysis where regression lines were fitted to dose-mortality data on a log-probit scale and the estimated LC50s and associated confidenceintervals (CI) were then calculated from the estimated linear regression parameters Inaddition to compare the independent and combined effects of host plants and Bt formu-lations differences in percentage mortalities between host-plant types Bt formulationsand concentrations were analyzed using Analysis of Covariance after correction andarcsine transformation For these data a Petri dish (containing five individual larvae)was considered as a replication and the treatments (six different concentrations of eachBt formulation as well as the control) were replicated eight times Pairwise comparisonswere performed using Least Significant Difference (LSD) or Tukeyrsquos Honestly SignificantDifference (HSD Crawley 2013 Day amp Quinn 1989) All statistical analyses were com-pleted in R 2100 (R Development Core Team)

3 Results

31 Host-plant effects on P xylostella performance

There was a significant effect of host plant on P xylostella larval periods (F376 = 10119P lt 0001) The mean larval period of P xylostella on the red cabbage (1689 plusmn 053 days)was significantly greater than that on white cabbage (1132 plusmn 028 days) cauliflower(1029 plusmn 027 days) or Chinese cabbage (810 plusmn 007 days Table 1) However no signifi-cant influence of host plants on the pupal period of P xylostella was observed (F376 =154 P = 019 Table 1) In addition when sum of larval and pupal period was analyzedthere was a significant effect of host plant (F376 = 973 P lt 0001) such that the shortestand longest developmental period of P xylostella was obtained when the insect fed onChinese cabbage (1171 plusmn 046 days) and red cabbage (2098 plusmn 200 days) respectively(Table 1) The effect of host plant on the pupal weight of P xylostella was also significant

Table 1 Host-plant effects on developmental periods and pupal weight of P xylostellaDevelopmental periods (mean plusmn SE days) Pupal weight

(mean plusmn SE mg)Host plant L1-Adult Pupal L1-pupa

Chinese cabbage 1171 plusmn 046 a 361 plusmn 020 a 810 plusmn 007 aa 432 plusmn 006 aWhite cabbage 1505 plusmn 071 ab 373 plusmn 032 a 1132 plusmn 028 b 381 plusmn 011 abCauliflower 1444 plusmn 054 ab 415 plusmn 024 a 1029 plusmn 027 b 380 plusmn 006 bRed cabbage 2098 plusmn 200 b 409 plusmn 044 a 1689 plusmn 053 c 366 plusmn 019 baThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

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(F376 = 2697 P lt 0001 Table 2) The mean pupal weight of P xylostella on Chinesecabbage (432 plusmn 006 mg) was significantly greater than cauliflower (380 plusmn 006 mg)and red cabbage (366 plusmn 019 mg Table 1) Host plant had significant influences onthe larval (F380 = 5283 P lt 0001) and on L1-adult (F380 = 4414 P lt 0001) survivalrate of P xylostella Mean survival rate of both the larvae and the sum of larvae andpupae of P xylostella was significantly greater on Chinese cabbage compared withcommon cabbages (Table 2) But no significant difference for pupal survival rate(F375 = 178 P = 013) between the host plants was found

32 Host-plant effects on the Bt dose-mortality response

The results of CFU test showed that the number of viable spores of Biolarvreg and Biolepreg

were 375 times 1011 and 295 times 1014 CFUml respectively (Table 3) The probit analysisshowed that LC50 of Biolarvreg significantly varied among host plants such that LC50 ofBiolarvreg was significantly greater on Chinese cabbage compared with red cabbageHowever there was no significant difference between LC50 of Biolepreg on different hostplants (Table 3) The analysis of covariance (Table 4) showed that both the host plant(F3368 = 1543 P lt 0001) and Bt formulation (F1368 = 763 P lt 001) had significanteffects on the mortality of P xylostella larvae the proportion mortality of P xylostellalarvae was highest and lowest on red cabbage (068) and Chinese cabbage (038) respect-ively (Table 5 Figure 1) Furthermore the proportion P xylostella larvae killed by Biolarvreg

(057) was significantly greater than that for Biolepreg (049) There was however no signifi-cant interaction (F3368 = 054 P = 065) between host plant and formulation for theireffects on P xylostella larval mortality (Table 4) In addition there was a significant

Table 2 Host-plant effects on survival rate of P xylostella

Host plant

Survival rate (mean plusmn SE )

L1-pupa Pupal L1-adult

Chinese cabbage 8353 plusmn 542 aa 8592 plusmn 355 a 7176 plusmn 608 aCauliflower 6824 plusmn 509 ab 9052 plusmn 302 a 6175 plusmn 494 abWhite cabbage 4765 plusmn 597 b 9012 plusmn 391 a 4294 plusmn 574 bRed cabbage 2000 plusmn 462 c 8235 plusmn 526 a 1647 plusmn 383 caThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

Table 3 The effects of host-plant species on the susceptibility of P xylostella larvae to B thuringiensis

Bt Number of viablespores (CFUml) Host plant

Lethal dose (grml or mlml)a

Slopeplusmn SE PFormulation LC50 95 CI (n = 8)

Biolarvreg(WP) 375 times 1011 Chinesecabbage

23 times 10minus4 799 times 10minus6minus194 times 10minus1 045 plusmn 008 lt0001

White cabbage 124 times 10minus5 153 times 10minus6minus34 times 10minus3 051 plusmn 008 lt0001Cauliflower 945 times 10minus6 983 times 10minus7minus240 times 10minus2 043 plusmn 008 lt0001Red cabbage 197 times 10minus7 833 times 10minus8minus319 times 10minus6 040 plusmn 007 lt0001

Biolepreg(SC) 295 times 1014 Chinesecabbage

420 times 10minus4 223 times 10minus5minus48 times 10minus1 057 plusmn 007 lt0001

White cabbage 899 times 10minus5 449 times 10minus6minus017 times 10minus1 042 plusmn 008 lt0001Cauliflower 135 times 10minus5 229 times 10minus6minus590 times 10minus4 057 plusmn 007 lt0001Red cabbage 435 times 10minus6 691 times 10minus7minus940 times 10minus4 045 plusmn 008 lt0001

aLC50 units for Biolarvreg and Biolepreg respectively

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interaction (F3368 = 388 P lt 001) between plant type and Bt concentration (Table 4) as itcan be seen more clearly in Figure 1 for the Biolep formulation there is a significant differ-ence in mortality among the plant species at the lower concentrations but not at the higherconcentrations

4 Discussion

Using the laboratory experiments we demonstrate that host plant quality-mediatedeffects on an insect herbivore might be determinative in hostndashpathogen interactions Inparticular it was indicated that the species of the host plant may influence the suscepti-bility of the diamondback moth to Bt Host-plant quality clearly had a direct effect onthe herbivore performance the different stages of P xylostella developed faster and per-formed better on the high-quality host plant (Chinese cabbage) compared with intermedi-ate (white cabbage and cauliflower) or low-quality (red cabbage) host plants In additionthe lowest LC50 value of Bt against P xylostella larvae fed on red cabbage compared withother host plants demonstrated that the entomopathogen acts better on the herbivorelarvae that suffered from low plant quality Such an indirect effect of plant quality onthe third trophic level is indicative of a strong bottom-up cascading effect in a tritrophicsystem

The plant characteristics such as trichomes domatia or semiochemicals may havedirect or indirect (through alteration of herbivore physiology or behaviour) effects onnatural enemies For example diverse life history traits of viral pathogens and parasi-toids can be affected by variation in host-plant chemistry (Karimzadeh et al 2004Raymond et al 2002) The plant nutritional defensive or physical characteristics can

Table 4 Analysis of covariance of the effects of host plant Bt formulation and concentration onP xylostella mortalitySource Df Sum Sq Mean Sq F value P value

Plant 3 438 146 1543 lt0001Formulation 1 072 072 763 lt001Concentration 1 7236 7236 76516 lt0001Plant Formulation 3 015 005 054 065Plant Concentration 3 110 037 388 lt001Formulation Concentration 1 006 006 063 043Plant Formulation Concentration 3 029 010 102 039Residuals 368 3480 010

Table 5 The effects of host-plant species on the mortality of P xylostella larvae by B thuringiensis

Host plant

Proportion mortality of P xylostella larvae (mean plusmn SE)a

Bt formulationBiolarvreg Biolepreg Overall

Chinese cabbage 042 plusmn 008 033 plusmn 008 038 plusmn 006 ab

White cabbage 053 plusmn 008 050 plusmn 007 052 plusmn 005 bCauliflower 058 plusmn 008 051 plusmn 008 054 plusmn 006 bRed cabbage 075 plusmn 007 061 plusmn 008 068 plusmn 005 cOverall 057 plusmn 004 Ac 049 plusmn 004 BaThe mean proportional mortality of the total bioassay dosesbThe different letters within the column show a significant (P lt 005) difference (Tukeyrsquos HSD)cThe different capital letters within the row show a significant (P lt 005) difference (Tukeyrsquos HSD)

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

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for the care and use of laboratory animals (Institutional Animal Care and Use CommitteeGuidebook) were followed

24 Statistical analysis

Differences in the survival rates among host-plant types were analyzed using logisticanalysis of deviance (binomial error) The developmental periods and pupal weightwere analyzed using nested ANOVA where the individual larvae were nested withinPetri dishes and Petri dishes were nested within plants For these data a Petri dish (con-taining 10 individual larvae) was considered as a replication and the treatments (four hostplants) were replicated 17 times The dose-response data were corrected using Abbottrsquosformula and analyzed using probit analysis where regression lines were fitted to dose-mortality data on a log-probit scale and the estimated LC50s and associated confidenceintervals (CI) were then calculated from the estimated linear regression parameters Inaddition to compare the independent and combined effects of host plants and Bt formu-lations differences in percentage mortalities between host-plant types Bt formulationsand concentrations were analyzed using Analysis of Covariance after correction andarcsine transformation For these data a Petri dish (containing five individual larvae)was considered as a replication and the treatments (six different concentrations of eachBt formulation as well as the control) were replicated eight times Pairwise comparisonswere performed using Least Significant Difference (LSD) or Tukeyrsquos Honestly SignificantDifference (HSD Crawley 2013 Day amp Quinn 1989) All statistical analyses were com-pleted in R 2100 (R Development Core Team)

3 Results

31 Host-plant effects on P xylostella performance

There was a significant effect of host plant on P xylostella larval periods (F376 = 10119P lt 0001) The mean larval period of P xylostella on the red cabbage (1689 plusmn 053 days)was significantly greater than that on white cabbage (1132 plusmn 028 days) cauliflower(1029 plusmn 027 days) or Chinese cabbage (810 plusmn 007 days Table 1) However no signifi-cant influence of host plants on the pupal period of P xylostella was observed (F376 =154 P = 019 Table 1) In addition when sum of larval and pupal period was analyzedthere was a significant effect of host plant (F376 = 973 P lt 0001) such that the shortestand longest developmental period of P xylostella was obtained when the insect fed onChinese cabbage (1171 plusmn 046 days) and red cabbage (2098 plusmn 200 days) respectively(Table 1) The effect of host plant on the pupal weight of P xylostella was also significant

Table 1 Host-plant effects on developmental periods and pupal weight of P xylostellaDevelopmental periods (mean plusmn SE days) Pupal weight

(mean plusmn SE mg)Host plant L1-Adult Pupal L1-pupa

Chinese cabbage 1171 plusmn 046 a 361 plusmn 020 a 810 plusmn 007 aa 432 plusmn 006 aWhite cabbage 1505 plusmn 071 ab 373 plusmn 032 a 1132 plusmn 028 b 381 plusmn 011 abCauliflower 1444 plusmn 054 ab 415 plusmn 024 a 1029 plusmn 027 b 380 plusmn 006 bRed cabbage 2098 plusmn 200 b 409 plusmn 044 a 1689 plusmn 053 c 366 plusmn 019 baThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

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(F376 = 2697 P lt 0001 Table 2) The mean pupal weight of P xylostella on Chinesecabbage (432 plusmn 006 mg) was significantly greater than cauliflower (380 plusmn 006 mg)and red cabbage (366 plusmn 019 mg Table 1) Host plant had significant influences onthe larval (F380 = 5283 P lt 0001) and on L1-adult (F380 = 4414 P lt 0001) survivalrate of P xylostella Mean survival rate of both the larvae and the sum of larvae andpupae of P xylostella was significantly greater on Chinese cabbage compared withcommon cabbages (Table 2) But no significant difference for pupal survival rate(F375 = 178 P = 013) between the host plants was found

32 Host-plant effects on the Bt dose-mortality response

The results of CFU test showed that the number of viable spores of Biolarvreg and Biolepreg

were 375 times 1011 and 295 times 1014 CFUml respectively (Table 3) The probit analysisshowed that LC50 of Biolarvreg significantly varied among host plants such that LC50 ofBiolarvreg was significantly greater on Chinese cabbage compared with red cabbageHowever there was no significant difference between LC50 of Biolepreg on different hostplants (Table 3) The analysis of covariance (Table 4) showed that both the host plant(F3368 = 1543 P lt 0001) and Bt formulation (F1368 = 763 P lt 001) had significanteffects on the mortality of P xylostella larvae the proportion mortality of P xylostellalarvae was highest and lowest on red cabbage (068) and Chinese cabbage (038) respect-ively (Table 5 Figure 1) Furthermore the proportion P xylostella larvae killed by Biolarvreg

(057) was significantly greater than that for Biolepreg (049) There was however no signifi-cant interaction (F3368 = 054 P = 065) between host plant and formulation for theireffects on P xylostella larval mortality (Table 4) In addition there was a significant

Table 2 Host-plant effects on survival rate of P xylostella

Host plant

Survival rate (mean plusmn SE )

L1-pupa Pupal L1-adult

Chinese cabbage 8353 plusmn 542 aa 8592 plusmn 355 a 7176 plusmn 608 aCauliflower 6824 plusmn 509 ab 9052 plusmn 302 a 6175 plusmn 494 abWhite cabbage 4765 plusmn 597 b 9012 plusmn 391 a 4294 plusmn 574 bRed cabbage 2000 plusmn 462 c 8235 plusmn 526 a 1647 plusmn 383 caThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

Table 3 The effects of host-plant species on the susceptibility of P xylostella larvae to B thuringiensis

Bt Number of viablespores (CFUml) Host plant

Lethal dose (grml or mlml)a

Slopeplusmn SE PFormulation LC50 95 CI (n = 8)

Biolarvreg(WP) 375 times 1011 Chinesecabbage

23 times 10minus4 799 times 10minus6minus194 times 10minus1 045 plusmn 008 lt0001

White cabbage 124 times 10minus5 153 times 10minus6minus34 times 10minus3 051 plusmn 008 lt0001Cauliflower 945 times 10minus6 983 times 10minus7minus240 times 10minus2 043 plusmn 008 lt0001Red cabbage 197 times 10minus7 833 times 10minus8minus319 times 10minus6 040 plusmn 007 lt0001

Biolepreg(SC) 295 times 1014 Chinesecabbage

420 times 10minus4 223 times 10minus5minus48 times 10minus1 057 plusmn 007 lt0001

White cabbage 899 times 10minus5 449 times 10minus6minus017 times 10minus1 042 plusmn 008 lt0001Cauliflower 135 times 10minus5 229 times 10minus6minus590 times 10minus4 057 plusmn 007 lt0001Red cabbage 435 times 10minus6 691 times 10minus7minus940 times 10minus4 045 plusmn 008 lt0001

aLC50 units for Biolarvreg and Biolepreg respectively

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interaction (F3368 = 388 P lt 001) between plant type and Bt concentration (Table 4) as itcan be seen more clearly in Figure 1 for the Biolep formulation there is a significant differ-ence in mortality among the plant species at the lower concentrations but not at the higherconcentrations

4 Discussion

Using the laboratory experiments we demonstrate that host plant quality-mediatedeffects on an insect herbivore might be determinative in hostndashpathogen interactions Inparticular it was indicated that the species of the host plant may influence the suscepti-bility of the diamondback moth to Bt Host-plant quality clearly had a direct effect onthe herbivore performance the different stages of P xylostella developed faster and per-formed better on the high-quality host plant (Chinese cabbage) compared with intermedi-ate (white cabbage and cauliflower) or low-quality (red cabbage) host plants In additionthe lowest LC50 value of Bt against P xylostella larvae fed on red cabbage compared withother host plants demonstrated that the entomopathogen acts better on the herbivorelarvae that suffered from low plant quality Such an indirect effect of plant quality onthe third trophic level is indicative of a strong bottom-up cascading effect in a tritrophicsystem

The plant characteristics such as trichomes domatia or semiochemicals may havedirect or indirect (through alteration of herbivore physiology or behaviour) effects onnatural enemies For example diverse life history traits of viral pathogens and parasi-toids can be affected by variation in host-plant chemistry (Karimzadeh et al 2004Raymond et al 2002) The plant nutritional defensive or physical characteristics can

Table 4 Analysis of covariance of the effects of host plant Bt formulation and concentration onP xylostella mortalitySource Df Sum Sq Mean Sq F value P value

Plant 3 438 146 1543 lt0001Formulation 1 072 072 763 lt001Concentration 1 7236 7236 76516 lt0001Plant Formulation 3 015 005 054 065Plant Concentration 3 110 037 388 lt001Formulation Concentration 1 006 006 063 043Plant Formulation Concentration 3 029 010 102 039Residuals 368 3480 010

Table 5 The effects of host-plant species on the mortality of P xylostella larvae by B thuringiensis

Host plant

Proportion mortality of P xylostella larvae (mean plusmn SE)a

Bt formulationBiolarvreg Biolepreg Overall

Chinese cabbage 042 plusmn 008 033 plusmn 008 038 plusmn 006 ab

White cabbage 053 plusmn 008 050 plusmn 007 052 plusmn 005 bCauliflower 058 plusmn 008 051 plusmn 008 054 plusmn 006 bRed cabbage 075 plusmn 007 061 plusmn 008 068 plusmn 005 cOverall 057 plusmn 004 Ac 049 plusmn 004 BaThe mean proportional mortality of the total bioassay dosesbThe different letters within the column show a significant (P lt 005) difference (Tukeyrsquos HSD)cThe different capital letters within the row show a significant (P lt 005) difference (Tukeyrsquos HSD)

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

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(F376 = 2697 P lt 0001 Table 2) The mean pupal weight of P xylostella on Chinesecabbage (432 plusmn 006 mg) was significantly greater than cauliflower (380 plusmn 006 mg)and red cabbage (366 plusmn 019 mg Table 1) Host plant had significant influences onthe larval (F380 = 5283 P lt 0001) and on L1-adult (F380 = 4414 P lt 0001) survivalrate of P xylostella Mean survival rate of both the larvae and the sum of larvae andpupae of P xylostella was significantly greater on Chinese cabbage compared withcommon cabbages (Table 2) But no significant difference for pupal survival rate(F375 = 178 P = 013) between the host plants was found

32 Host-plant effects on the Bt dose-mortality response

The results of CFU test showed that the number of viable spores of Biolarvreg and Biolepreg

were 375 times 1011 and 295 times 1014 CFUml respectively (Table 3) The probit analysisshowed that LC50 of Biolarvreg significantly varied among host plants such that LC50 ofBiolarvreg was significantly greater on Chinese cabbage compared with red cabbageHowever there was no significant difference between LC50 of Biolepreg on different hostplants (Table 3) The analysis of covariance (Table 4) showed that both the host plant(F3368 = 1543 P lt 0001) and Bt formulation (F1368 = 763 P lt 001) had significanteffects on the mortality of P xylostella larvae the proportion mortality of P xylostellalarvae was highest and lowest on red cabbage (068) and Chinese cabbage (038) respect-ively (Table 5 Figure 1) Furthermore the proportion P xylostella larvae killed by Biolarvreg

(057) was significantly greater than that for Biolepreg (049) There was however no signifi-cant interaction (F3368 = 054 P = 065) between host plant and formulation for theireffects on P xylostella larval mortality (Table 4) In addition there was a significant

Table 2 Host-plant effects on survival rate of P xylostella

Host plant

Survival rate (mean plusmn SE )

L1-pupa Pupal L1-adult

Chinese cabbage 8353 plusmn 542 aa 8592 plusmn 355 a 7176 plusmn 608 aCauliflower 6824 plusmn 509 ab 9052 plusmn 302 a 6175 plusmn 494 abWhite cabbage 4765 plusmn 597 b 9012 plusmn 391 a 4294 plusmn 574 bRed cabbage 2000 plusmn 462 c 8235 plusmn 526 a 1647 plusmn 383 caThe different letters within columns show a significant (P lt 005) difference (Tukeyrsquos HSD)

Table 3 The effects of host-plant species on the susceptibility of P xylostella larvae to B thuringiensis

Bt Number of viablespores (CFUml) Host plant

Lethal dose (grml or mlml)a

Slopeplusmn SE PFormulation LC50 95 CI (n = 8)

Biolarvreg(WP) 375 times 1011 Chinesecabbage

23 times 10minus4 799 times 10minus6minus194 times 10minus1 045 plusmn 008 lt0001

White cabbage 124 times 10minus5 153 times 10minus6minus34 times 10minus3 051 plusmn 008 lt0001Cauliflower 945 times 10minus6 983 times 10minus7minus240 times 10minus2 043 plusmn 008 lt0001Red cabbage 197 times 10minus7 833 times 10minus8minus319 times 10minus6 040 plusmn 007 lt0001

Biolepreg(SC) 295 times 1014 Chinesecabbage

420 times 10minus4 223 times 10minus5minus48 times 10minus1 057 plusmn 007 lt0001

White cabbage 899 times 10minus5 449 times 10minus6minus017 times 10minus1 042 plusmn 008 lt0001Cauliflower 135 times 10minus5 229 times 10minus6minus590 times 10minus4 057 plusmn 007 lt0001Red cabbage 435 times 10minus6 691 times 10minus7minus940 times 10minus4 045 plusmn 008 lt0001

aLC50 units for Biolarvreg and Biolepreg respectively

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interaction (F3368 = 388 P lt 001) between plant type and Bt concentration (Table 4) as itcan be seen more clearly in Figure 1 for the Biolep formulation there is a significant differ-ence in mortality among the plant species at the lower concentrations but not at the higherconcentrations

4 Discussion

Using the laboratory experiments we demonstrate that host plant quality-mediatedeffects on an insect herbivore might be determinative in hostndashpathogen interactions Inparticular it was indicated that the species of the host plant may influence the suscepti-bility of the diamondback moth to Bt Host-plant quality clearly had a direct effect onthe herbivore performance the different stages of P xylostella developed faster and per-formed better on the high-quality host plant (Chinese cabbage) compared with intermedi-ate (white cabbage and cauliflower) or low-quality (red cabbage) host plants In additionthe lowest LC50 value of Bt against P xylostella larvae fed on red cabbage compared withother host plants demonstrated that the entomopathogen acts better on the herbivorelarvae that suffered from low plant quality Such an indirect effect of plant quality onthe third trophic level is indicative of a strong bottom-up cascading effect in a tritrophicsystem

The plant characteristics such as trichomes domatia or semiochemicals may havedirect or indirect (through alteration of herbivore physiology or behaviour) effects onnatural enemies For example diverse life history traits of viral pathogens and parasi-toids can be affected by variation in host-plant chemistry (Karimzadeh et al 2004Raymond et al 2002) The plant nutritional defensive or physical characteristics can

Table 4 Analysis of covariance of the effects of host plant Bt formulation and concentration onP xylostella mortalitySource Df Sum Sq Mean Sq F value P value

Plant 3 438 146 1543 lt0001Formulation 1 072 072 763 lt001Concentration 1 7236 7236 76516 lt0001Plant Formulation 3 015 005 054 065Plant Concentration 3 110 037 388 lt001Formulation Concentration 1 006 006 063 043Plant Formulation Concentration 3 029 010 102 039Residuals 368 3480 010

Table 5 The effects of host-plant species on the mortality of P xylostella larvae by B thuringiensis

Host plant

Proportion mortality of P xylostella larvae (mean plusmn SE)a

Bt formulationBiolarvreg Biolepreg Overall

Chinese cabbage 042 plusmn 008 033 plusmn 008 038 plusmn 006 ab

White cabbage 053 plusmn 008 050 plusmn 007 052 plusmn 005 bCauliflower 058 plusmn 008 051 plusmn 008 054 plusmn 006 bRed cabbage 075 plusmn 007 061 plusmn 008 068 plusmn 005 cOverall 057 plusmn 004 Ac 049 plusmn 004 BaThe mean proportional mortality of the total bioassay dosesbThe different letters within the column show a significant (P lt 005) difference (Tukeyrsquos HSD)cThe different capital letters within the row show a significant (P lt 005) difference (Tukeyrsquos HSD)

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

BIOCONTROL SCIENCE AND TECHNOLOGY 111

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

112 M JAFARY ET AL

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2015

interaction (F3368 = 388 P lt 001) between plant type and Bt concentration (Table 4) as itcan be seen more clearly in Figure 1 for the Biolep formulation there is a significant differ-ence in mortality among the plant species at the lower concentrations but not at the higherconcentrations

4 Discussion

Using the laboratory experiments we demonstrate that host plant quality-mediatedeffects on an insect herbivore might be determinative in hostndashpathogen interactions Inparticular it was indicated that the species of the host plant may influence the suscepti-bility of the diamondback moth to Bt Host-plant quality clearly had a direct effect onthe herbivore performance the different stages of P xylostella developed faster and per-formed better on the high-quality host plant (Chinese cabbage) compared with intermedi-ate (white cabbage and cauliflower) or low-quality (red cabbage) host plants In additionthe lowest LC50 value of Bt against P xylostella larvae fed on red cabbage compared withother host plants demonstrated that the entomopathogen acts better on the herbivorelarvae that suffered from low plant quality Such an indirect effect of plant quality onthe third trophic level is indicative of a strong bottom-up cascading effect in a tritrophicsystem

The plant characteristics such as trichomes domatia or semiochemicals may havedirect or indirect (through alteration of herbivore physiology or behaviour) effects onnatural enemies For example diverse life history traits of viral pathogens and parasi-toids can be affected by variation in host-plant chemistry (Karimzadeh et al 2004Raymond et al 2002) The plant nutritional defensive or physical characteristics can

Table 4 Analysis of covariance of the effects of host plant Bt formulation and concentration onP xylostella mortalitySource Df Sum Sq Mean Sq F value P value

Plant 3 438 146 1543 lt0001Formulation 1 072 072 763 lt001Concentration 1 7236 7236 76516 lt0001Plant Formulation 3 015 005 054 065Plant Concentration 3 110 037 388 lt001Formulation Concentration 1 006 006 063 043Plant Formulation Concentration 3 029 010 102 039Residuals 368 3480 010

Table 5 The effects of host-plant species on the mortality of P xylostella larvae by B thuringiensis

Host plant

Proportion mortality of P xylostella larvae (mean plusmn SE)a

Bt formulationBiolarvreg Biolepreg Overall

Chinese cabbage 042 plusmn 008 033 plusmn 008 038 plusmn 006 ab

White cabbage 053 plusmn 008 050 plusmn 007 052 plusmn 005 bCauliflower 058 plusmn 008 051 plusmn 008 054 plusmn 006 bRed cabbage 075 plusmn 007 061 plusmn 008 068 plusmn 005 cOverall 057 plusmn 004 Ac 049 plusmn 004 BaThe mean proportional mortality of the total bioassay dosesbThe different letters within the column show a significant (P lt 005) difference (Tukeyrsquos HSD)cThe different capital letters within the row show a significant (P lt 005) difference (Tukeyrsquos HSD)

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

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mediate such determinative interactions between plants herbivores and natural enemies(Awmack amp Leather 2002) The different plant suitability to P xylostella observed in thepresent study may be due to the presence and extent of nutritional factors and feedingstimulants (Syed amp Abro 2003) Chinese cabbage showed to be the most qualified hostfor P xylostella which completed its larval development fastest on this plant comparedwith other host plants The longer developmental times of insect herbivores on low-quality plants may increase the exposure time to natural enemies (Awmack ampLeather 2002) In addition the greatest pupal weight of P xylostella fed on Chinesecabbage might have increased the fitness and performance of P xylostella on such aplant The insect life-history parameters such as fecundity longevity and survival ratemay vary with body size as indicative of fitness (Karimzadeh et al 2004) Apartfrom other factors fecundity of an insect greatly depends on body weight or size(Begum Ritusko amp Fujisaki 1996 Miller 1957 Syed amp Abro 2003) The plant-mediated variation in insect fecundity has paramount implications for populationecology and pest management through the manifestations of the intrinsic rate of increaseand economic injury threshold respectively (Awmack amp Leather 2002 Carey 2001Karimzadeh et al 2004)

Host plants can mediate the interactions among insect herbivores and their pathogenssuch that the vulnerability of insects to infection and the production and persistence ofentomopathogens may be greatly affected by the variations in plant chemistry and struc-ture (Cory amp Hoover 2006) Plants influences on the insectndashentomopathogen interactionscan occur via leaf surface (for example leaf alkaline exudates containing basic ions thatcan inactivate baculoviruses or leaves with reduced wax bloom increase adhesion andgermination of the fungal conidia on the insect cuticle) plant architecture (for examplethe degree of shading can influence the time entomopathogens persist before degradationby UV irradiation) or phytochemicals (for example biologically activated phytochemicalscan bind to occlusion bodies in the larval midgut and reduce the subsequent infectivity ofthe virus to host insects) (Duffey Hoover Bonning amp Hammock 1995 Kouassi Loren-zetti Guertin Cabana ampMauffette 2001) In addition plant allelochemicals and nutrients

Figure 1 Dose-responsive curves for Biolarv (left) and Biolep (right) on different host plants Solid(filled circle) dashed (empty circle) dotted (filled square) and long-dashed (empty square) lines(points) represent cauliflower Chinese cabbage red cabbage and white cabbage respectively

110 M JAFARY ET AL

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

BIOCONTROL SCIENCE AND TECHNOLOGY 111

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

112 M JAFARY ET AL

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can affect pathogen fitness through the alteration of the physiology growth and behaviourof the insect host Entomopathogens could benefit from plants through the additionalpersistence on plant surface encountering higher host populations and increased hostvulnerability to pathogens (Elliot et al 2000) From the evolutionary point of view thisis a paramount role that plants play in the evolution of insectndashpathogen interactionsFrom a pest management viewpoint however the increased fitness costs of an insect her-bivore on poor quality plants would intensify the susceptibility of the insect to pathogensmainly viruses and bacteria Here it was also demonstrated that food plants of P xylostellaplay an important role in the pathogenicity of Bt as the higher concentrations of Bt wereneeded to control P xylostella larvae on a high-quality host plant (Chinese cabbage) com-pared with intermediate (white cabbage and cauliflower) or low-quality (red cabbage) hostplants Although the effects of plant resistancequalitygenotype on the interactionsbetween P xylostella and its parasitoids or predators are well documented (EigenbrodeMoodie amp Castagnola 1995 Gols et al 2007 Karimzadeh et al 2004 2013 Karimzadehamp Wright 2008 Liu amp Jiang 2003 Reddy Tabone amp Smith 2004 Sarfraz et al 2008Schuler et al 2003 2004 Verkerk amp Wright 1997) tritrophic studies focusing on theeffects of plant characteristics on the interactions between P xylostella and its pathogenor even on more complex interactions are rare (Karimzadeh amp Sayyed 2011 Raymondet al 2007) The present study in this regard revealed a strong effect of plant qualitysuit-ability for P xylostella on the hostndashpathogen interaction which is important from pestmanagement point of view Previous studies have also shown differential food plant-mediated effects of Bt on other insects such as Lymantria dispar (L) (Lepidoptera Ere-bidae) Trichoplusia ni (Huumlbner) (Lepidoptera Noctuidae) Spodoptera littoralis (Boisdu-val) (Lepidoptera Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera Noctuidae)(Bell 1978 Farrar Martin amp Ridgway 1996 Janmaat et al 2007) Some secondaryplant compounds have been reported to affect Bt efficiency on control of herbivorousinsects For example tannins and phenolic glycosides present in the foliage of aspenhave changed the impact of Bt or its delta endotoxins on L dispar larvae (Awmack ampLeather 2002)

The observed antagonisticsynergistic interactions between host plants of P xylostellaand Bt provide an additional advantage for the use of low-qualitypartially resistantplants in Bt-based pest management programmes against P xylostella The growth andadaption of P xylostella populations on such host plants would be slower Moreoversuch a synergism might result in a better control of P xylostella by Bt or other pathogenspredators and parasitoids (Awmack amp Leather 2002 Verkerk Leather amp Wright 1998)In addition low plant quality or plant defensive chemicals may favour Bt resistancemanagement For example fitness costs of Bt resistance in P xylostella have beenhigher on the low-quality plants (Raymond Wright amp Bonsall 2011) Increased accumu-lation of gossypol (a cotton defensive chemical) in pink bollworm (Pectinophoragossypiella) may also contribute to fitness costs associated with resistance to Bt toxins(Williams et al 2011)

The host plant influences on the efficiency of other entomopathogens have been alsoreported For instance feeding on different food plants caused significant variation ofLeptinotarsa decemlineata (Say) (Coleoptera Chrysomelidae) to attack by the fungusBeauveria bassiana (Hare amp Andreadis 1983) In another study Poprawski andJones (2001) have shown that mycosis from two different fungi B bassiana and

BIOCONTROL SCIENCE AND TECHNOLOGY 111

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Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

112 M JAFARY ET AL

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ovem

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2015

Paecilomyces fumosoroseus in nymphs of Bemisia argentifolii Bellows and Perring(Hemiptera Aleyrodidae) varied between the different host plants The influence offood plants on the vulnerability of Spodoptera frugiperda (J E Smith) and L disparto a nuclear polyhedrosis viruses have also been documented (Keating Yendol ampSchultz 1988) In addition Gassmann et al (2010) have shown plant-mediated resistanceto entomopathogenic nematodes in Grammia incorrupta (Hy Edwards) (LepidopteraErebidae)

The present study indicated that host-plant resistance can be successfully combinedwith the entomopathogenic bacterium B thuringiensis in sustainable pest managementof P xylostella Further studies are however needed to explore the mechanisms bywhich resistant crucifers increase the vulnerability of P xylostella larvae to Bt and totest the consequence of such a combination in field

Acknowledgements

We thank the late Dr Ali H Sayyed (Department of Biochemistry School of Life Sciences Univer-sity of Sussex Brighton UK) for advising on bioassays

Disclosure statement

No potential conflict of interest was reported by the authors

ORCID

Javad Karimzadeh httporcidorg0000-0002-4848-9293

References

Andrahennadi R amp Gillott C (1998) Resistance of Brassica especially B juncea (L) Czern gen-otypes to the diamondback moth Plutella xylostella (L) Crop Protection 17 85ndash94 doi101016S0261-2194(98)80016-1

Awmack A S amp Leather S R (2002) Host plant quality and fecundity in herbivorous insectsAnnual Review of Entomology 47 817ndash844 doi101146annurevento47091201145300

Begum S Ritusko T amp Fujisaki K (1996) The effects of wild cruciferous host plants on mor-phology reproductive performance and flight activity in the diamondback moth Plutella xylos-tella (Lepidoptera Yponomeutidae) Researches on Population Ecology 38 257ndash263 doi101007BF02515735

Bell J V (1978) Development and mortality in bollworms fed resistant and susceptible soybeancultivars treated with Nomuraea rileyi or Bacillus thuringiensis Journal of the GeorgiaEntomological Society 13 50ndash55

Carey J R (2001) Insect biodemography Annual Review of Entomology 46 79ndash110 doi101146annurevento46179

Cory J S amp Hoover K (2006) Plant-mediated effects in insect-pathogen interactions Trends inEcology amp Evolution 21 278ndash286 doi101016jtree200602005

Crawley M J (2013) The R book Chichester WileyDay R W amp Quinn G P (1989) Comparisons of treatments after an analysis of variance in

ecology Ecological Monographs 59 433ndash463 doi1023071943075Duffey S S Hoover K Bonning B amp Hammock B D (1995) The impact of host plant on the

efficacy of baculoviruses In R M Roe amp R J Kuhr (Eds) Reviews in pesticide toxicology(pp 137ndash275) Raleigh CTI Toxicology Communications

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Eigenbrode S D Moodie S amp Castagnola T (1995) Predators mediate host plant resistance to aphytophagous pest in cabbage with glossy leaf wax Entomologia Experimentalis et Applicata 77335ndash342 doi101111j1570-74581995tb02331x

Elliot S L Sabelis M W Janssen A van der Geest L P S Beerling E A M amp Fransen J(2000) Can plants use entomopathogens as bodyguards Ecology Letters 3 228ndash235 doi101046j1461-0248200000137x

Farrar R R Martin P A W amp Ridgway R (1996) Host plant effects on activity of Bacillus thur-ingiensis against gypsy moth (Lepidoptera Lymantriidae) larvae Environmental Entomology 251215ndash1223

Furlong M J Wright D J amp Dosdall M L (2013) Diamondback moth ecology and manage-ment Problems progress and prospects Annual Review of Entomology 58 517ndash541 doi101146annurev-ento-120811-153605

Gassmann A J Stock S P Tabashnik B E amp Singer M S (2010) Tritrophic effects of hostplants on an herbivore pathogen interaction Annals of the Entomological Society of America103 371ndash378 doi101603AN09130

Gols R Raaijmakers C E van Dam N M Dicke M Bukovinszky T amp Harvey J A (2007)Temporal changes affect plant chemistry and tritrophic interactions Basic and Applied Ecology8 421ndash433 doi101016jbaae200609005

Hare J D amp Andreadis T G (1983) Variation in the susceptibility of Leptinotarsa decemlineata(Coleoptera Chrysomelidae) when reared on different host plants to the fungal pathogenBeauveria bassiana in the field and laboratory Environmental Entomology 12 1892ndash1897

Izadyar S Talebi-Jahromi K Askary H amp Rezapanah M (2003) Determination of β-exotoxinin Iranian Isolates of Bacillus thuringiensis Journal of Entomological Society of Iran 23 55ndash68

Janmaat A F ampMyers J H (2007) Host-plant effects the expression of resistance to Bacillus thur-ingiensis kurstaki in Trichoplusia ni (Hubner) An important factor in resistance evolutionJournal of Evolutionary Biology 20 62ndash69 doi101111j1420-9101200601232x

Janmaat A F Ware J amp Myers J (2007) Effects of crop type on Bacillus thuringiensis toxicityand residual activity against Trichoplusia ni in greenhouses Journal of Applied Entomology131 333ndash337 doi101111j1439-0418200701181x

Karimzadeh J (2011) Sample size calculation in entomological studies using R language of statisti-cal computing Part 1 Comparison of means and proportions Iranian Journal of EntomologicalResearch 3 51ndash61

Karimzadeh J Bonsall M B amp Wright D J (2004) Bottom-up and top-down effects in a tri-trophic system The population dynamics of Plutella xylostella (L)ndashCotesia plutellae(Kurdjumov) on different host plants Ecological Entomology 29 285ndash293 doi101111j0307-6946200400609x

Karimzadeh J Hardie J amp Wright D J (2013) Plant resistance affects the olfactory response andparasitism success of Cotesia vestalis Journal of Insect Behavior 26 35ndash50 doi101007s10905-012-9331-y

Karimzadeh J amp Sayyed A H (2011) Immune system challenge in a host-parasitoid-pathogensystem Interaction between Cotesia plutellae (Hym Braconidae) and Bacillus thuringiensisinfluences parasitism and phenoloxidase cascade of Plutella xylostella (Lep Plutellidae)Journal of Entomological Society of Iran 30 27ndash38

Karimzadeh J amp Wright D J (2008) Bottom-up cascading effects in a tritrophic systemInteractions between plant quality and host-parasitoid immune responses EcologicalEntomology 33 45ndash52 doi101111j1365-2311200700933x

Keating S T Yendol W G amp Schultz J C (1988) Relationship between susceptibility of gypsymoth larvae (Lepidoptera Lymantriidae) to a baculovirus and host plant foliage constituentsEnvironmental Entomology 17 952ndash958

Kouassi K C Lorenzetti F Guertin C Cabana J amp Mauffette Y (2001) Variation in the sus-ceptibility of the forest tent caterpillar (Lepidoptera Lasiocampidae) to Bacillus thuringiensisvariety kurstaki HD-1 Effect of the host plant Journal of Economic Entomology 94 1135ndash1141 doi1016030022-0493-9451135

BIOCONTROL SCIENCE AND TECHNOLOGY 113

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Liu S S amp Jiang L H (2003) Differential parasitism of Plutella xylostella (LepidopteraPlutellidae) larvae by the parasitoid Cotesia plutellae (Hymenoptera Braconidae) on two hostplant species Bulletin of Entomological Research 93 65ndash72 doi101079BER2002208

Liu Y B Tabashnik B E Moar W J amp Smith R A (1998) Synergism between Bacillus thur-ingiensis spores and toxins against resistant and susceptible diamondback moths (Plutella xylos-tella) Applied and Environmental Microbiology 64 1385ndash1389

Miller C A (1957) A technique for estimating the fecundity of natural populations of the sprucebudworm Canadian Journal of Zoology 35 1ndash13

Poprawski T J amp Jones W J (2001) Host plant effects on activity of the mitosporic fungiBeauveria bassiana and Paecilomyces fumosoroseus against two populations of Bemisia whiteflies(Homoptera Aleyrodidae) Mycopathologia 151 11ndash20 doi101023A1010835224472

Raymond B Sayyed A H ampWright D J (2007) Host plant and population determine the fitnesscosts of resistance to Bacillus thuringiensis Biology Letters 3 83ndash86 doi101098rsbl20060560

Raymond B Vanbergen A Pearce I Hartley S Cory J amp Hails R (2002) Host plant speciescan influence the fitness of herbivore pathogens The winter moth and its nucleopolyhedrovirusOecologia 131 533ndash541 doi101007s00442-002-0926-4

Raymond B Wright D J amp Bonsall M B (2011) Effects of host plant and genetic background onthe fitness costs of resistance to Bacillus thuringiensis Heredity 106 281ndash288 doi101038hdy201065

Reddy G V P Tabone E amp Smith M T (2004) Mediation of host selection and ovipositionbehavior in the diamondback moth Plutella xylostella and its predator Chrysoperla carnea bychemical cues from cole crops Biological Control 29 270ndash277 doi101016S1049-9644(03)00162-2

Sarfraz M Dosdall L M amp Keddie B A (2006) Diamondback moth-host plant interactionsImplications for pest management Crop Protection 25 625ndash639 doi101016jcropro200509011

Sarfraz M Dosdall L M amp Keddie B A (2007) Resistance of some cultivated Brassicaceae toinfestations by Plutella xylostella (Lepidoptera Plutellidae) Journal of Economic Entomology100 215ndash224 doi1016030022-0493(2007)100[215ROSCBT]20CO2

Sarfraz M Dosdall L M amp Keddie B A (2008) Host plant genotype of the herbivore Plutellaxylostella (Lepidoptera Plutellidae) affects the performance of its parasitoid Diadegma insulare(Hymenoptera Ichneumonidae) Biological Control 44 42ndash51 doi101016jbiocontrol200710023

Sayyed A H Raymond B Ibiza-Palacios M S Escriche B amp Wright D J (2004) Genetic andbiochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac inthe diamondback moth Plutella xylostella Applied and Environmental Microbiology 70 7010ndash7017 doi101128AEM70127010-70172004

Schnepf E Crickmore N VanRie J Lereclus D Baum J Feitelson JhellipDean D H (1998)Bacillus thuringiensis and its pesticidal crystal proteins Microbiology and Molecular BiologyReviews 62 775ndash806

Schuler T H Denholm I Clark S J Stewart C N amp Poppy G M (2004) Effects of Bt plants onthe development and survival of the parasitoid Cotesia plutellae (Hymenoptera Braconidae) insusceptible and Bt-resistant larvae of the diamondback moth Plutella xylostella (LepidopteraPlutellidae) Journal of Insect Physiology 50 435ndash443 doi101016jjinsphys200403001

Schuler T H Potting R P J Denholm I Clark S J Clark A J Stewart C N amp Poppy G M(2003) Tritrophic choice experiments with Bt plants the diamondback moth (Plutella xylostella)and the parasitoid Cotesia plutellae Transgenic Research 12 351ndash361 doi101023A1023342027192

Schuler T H amp van Emden H F (2000) Resistant cabbage cultivars change the susceptibility ofPlutella xylostella to Bacillus thuringiensis Agricultural and Forest Entomology 2 33ndash38 doi101046j1461-9563200000042x

Shelton A M Wyman J A Cushing N L Apfelbeck K Dennehy T J Mahr S E R ampEigenbrode S D (1993) Insecticide resistance of diamondback moth (LepidopteraPlutellidae) in North America Journal of Economic Entomology 86 11ndash19

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Syed T S amp Abro G H (2003) Effect of Brassica vegetable hosts on biology and life table par-ameters of Plutella xylostella under laboratory conditions Pakistan Journal of BiologicalSciences 6 1891ndash1896

Tabashnik B E Finson N amp Johnson M W (1991) Managing resistance to Bacillus thuringien-sis Lessons from the diamondback moth (Lepidoptera Plutellidae) Journal of EconomicEntomology 84 49ndash55

Talekar N S amp Shelton A M (1993) Biology ecology and management of the diamondbackmoth Annual Review of Entomology 38 275ndash301 doi101146annureven38010193001423

Ulmer B Gillott C Woods D amp Erlandson M (2002) Diamondback moth Plutella xylostella(L) feeding and oviposition preferences on glossy and waxy Brassica rapa (L) lines CropProtection 21 327ndash331 doi101016S0261-2194(02)00014-5

Verkerk R H J Leather S R amp Wright D J (1998) The potential for manipulating cropndashpestnatural enemy interactions for improved insect pest management Bulletin of EntomologicalResearch 88 493ndash501 doi101017S0007485300026018

Verkerk R H J amp Wright D J (1997) Field-based studies with the diamondback moth tritrophicsystem in Cameron Highlands of Malaysia Implications for pest management InternationalJournal of Pest Management 43 27ndash33 doi101080096708797228942

Williams J L Ellers-Kirk C Orth R G Gassmann A J Head G Tabashnik B E amp CarriegravereY (2011) Fitness cost of resistance to Bt cotton linked with increased gossypol content in pinkbollworm larvae PLoS One 6 e21863ndashe21863 doi101371journalpone0021863

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