Biological Control 51 (2009) 34–41

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Biological Control

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Host plant nutritional quality affects the performance of the parasitoidDiadegma insulare

M. Sarfraz a,*, L.M. Dosdall b, B.A. Keddie a

a Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9b Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada T6G 2P5

a r t i c l e i n f o

Article history:Received 13 August 2008Accepted 2 July 2009Available online 8 July 2009

Keywords:Diamondback mothPlutella xylostellaBottom-up forcesSoil fertilityInsect–plant interactions

1049-9644/$ - see front matter � 2009 Elsevier Inc. Adoi:10.1016/j.biocontrol.2009.07.004

* Corresponding author. Address: CW-405 Biologicof Alberta, Edmonton, Alberta, Canada T6G 2E9. Fax:

E-mail addresses: rsarfraz@ualberta.ca, sarfrazrana

a b s t r a c t

The well documented biochemical profile of Brassicaceae, oligophagy of the herbivore Plutella xylostella(L.) (Lepidoptera: Plutellidae), and host specialization of the parasitoid Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae) provide an ideal system for investigating tritrophic interactions medi-ated by nutritional quality of plants. We evaluated the bottom-up effects of five soil fertility regimeson nutritional quality of canola (Brassica napus L.) and then on several fitness correlates of female andmale D. insulare as mediated through P. xylostella. Variation in soil fertility influenced the nutritionalquality of host plants and this in turn affected the performance of D. insulare. In general, D. insulare per-formed best on plants grown with 3.0 g fertilizer pot�1; these plants had 2.06-, 3.77-, and 1.02-fold morenitrogen, phosphorous and potassium, respectively than ones grown without any added fertilizer.P. xylostella escape from D. insulare was highest (32%) on plants grown at 1.0 g fertilizer, and this couldbe attributed to both physical and physiological defense mechanisms mediated by host plant nutritionalquality. Plant stress and plant vigor are competing paradigms pertaining to the performance of herbivo-rous insects on their host plants. These hypotheses were originally proposed to predict responses ofherbivores, but may also explain the effects of plant quality on koinobiont parasitoids, such as D. insulare.

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1. Introduction

In terrestrial systems where herbivory is common, bottom-upeffects of plants may be of crucial importance (Price et al., 1980;Polis and Strong, 1996; Ode, 2006). The interactions between her-bivorous insects and their host plants are undoubtedly influencedby host plant quality that can be determined largely by variationin certain abiotic (Hunter and Price, 1992; Moon et al., 2000) andbiotic factors (Masters et al., 2001; Soler et al., 2007a,b; Sarfrazet al., in press). Perhaps one of the most important abiotic factorsthat shapes these interactions is nutrient availability and the sub-sequent nutrient contents of host plant tissues. Hypotheses of‘plant stress’ and ‘plant vigor’ have been proposed to predict the re-sponse of insect herbivores to soil nutrients, as mediated by hostplant quality. Some studies have shown that insects perform betteron vigorous plants than on their stressed counterparts (e.g., Foxet al., 1990; Price, 1991; Meyer and Root, 1996; Craig and Ohgushi,2002; Dosdall et al., 2004), while others indicate that stressedplants frequently support higher densities of insect herbivores(e.g., White, 1969; Mattson, 1980; Jones and Coleman, 1988).

ll rights reserved.

al Sciences Centre, University+1 780 492 9234.pk@yahoo.com (M. Sarfraz).

The effects of soil nutrient regimes are relatively well studiedfor herbivores, but studies focusing on the effects of plant fertiliza-tion on parasitoids are rare. A parasitoid has to deal with a varietyof challenges for its success, including host habitat identification,host location, host acceptance, host suitability and host regulation.Nutritional quality of host plants can be important at every stepaffecting parasitoid preference and performance indirectly ordirectly. Plants are known to indirectly influence the foraging effi-ciency of parasitoids, while plants directly influence hostacceptance, host suitability and host regulation (Tumlinson et al.,1992; Poppy, 1997; Turlings and Benrey, 1998). A few experimen-tal studies have indicated that abiotically induced changes in hostplant quality can have strong effects on the performance of parasit-oids. For example, Anagrus armatus (Ashmead) (Hymenoptera:Mymaridae) parasitized significantly more eggs of the salt marshplanthopper, Pissonotus quadripustulatus van Duzee (Homoptera:Delphacidae) on fertilized than on unfertilized plants (Moonet al., 2000). Plant nutritional quality can influence host-size andmost host-size models assume that larger hosts are superior tosmaller hosts in terms of parasitoid fitness. The evidence in sup-port of such host-size models comes mainly from studies of non-feeding hosts (e.g., eggs and pupae) that contain a fixed quantityof resources for idiobiont parasitoids (Salt, 1940; Arthur and Wylie,1959; Charnov et al., 1981; King, 1989; Corrigan and Lashomb,1990; Moon et al., 2000; Moreau et al., 2009). In contrast to

M. Sarfraz et al. / Biological Control 51 (2009) 34–41 35

non-feeding hosts, insect herbivores continue to feed and developafter parasitization by koinobiont parasitoids until destructive con-sumption of their host (Jowyk and Smilowitz, 1978; Beckage andRiddiford, 1983; Sequeira and Mackauer, 1992; Harvey et al.,1995; Fox et al., 1996). Therefore, the quality of plant tissue con-sumed by herbivore hosts after parasitization may have strongerbottom-up influences on the performance of koinobionts than onidiobionts.

The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plu-tellidae), is a specialist on Brassicaceae (Talekar and Shelton, 1993;Idris and Grafius, 1996; Sarfraz et al., 2006), a family of plants char-acterized by the presence of sulfur-containing secondary plantcompounds, the glucosinolates (Mithen, 1992). Diadegma insulare(Cresson) (Hymenoptera: Ichneumonidae) is a solitary koinobiont,host-specific larval endoparasitoid of P. xylostella and is one of itsmost important biological control agents in North America (Sarfrazet al., 2005b). It parasitizes all four larval instars of P. xylostella. Itkills and emerges from the pre-pupal stage of its host and spinsits own cocoon inside the loosely woven cocoon of its host (Har-court, 1960). Like other parasitoid species of herbivores, D. insulareutilizes plant cues to locate its P. xylostella hosts (Tumlinson et al.,1992; Turlings and Benrey, 1998; Ohara et al., 2003). The uniquebiochemistry of Brassicaceae, the oligophagous habit of P. xylostella,and host specialization of D. insulare provide an excellent model toinvestigate tritrophic interactions based on the nutritional qualityof plants, but to our knowledge studies focusing on such interac-tions are uncommon (Fox et al., 1990, 1996; Bentz et al., 1996).

In view of the extensive worldwide economic importance ofP. xylostella, and the vast areas of the planet seeded annually tobrassicaceous crops (e.g., approximately 5 million ha devoted tocanola production in western Canada alone), the question arisesof whether soil fertility levels can be manipulated for enhancedbiological control of this herbivore with D. insulare. In this study,the effects of different soil fertility regimes were examined, viz.no added fertility, two levels of intermediate fertility and two lev-els of high fertility on Brassica napus L. (Brassicaceae), and on per-formance parameters of the parasitoid, D. insulare, developingwithin larvae of P. xylostella that were feeding upon leaf tissuesof B. napus. Several fitness correlates directly related to parasitoidpopulation dynamics (e.g., level of parasitism, survival, pre-imagi-nal developmental time, larval herbivory, pupal weight, adult bodyweight, longevity without food, forewing area, and hindwing area)were investigated on P. xylostella feeding on plants grown underfive soil fertility regimes. A further objective of this study was toinvestigate how male and female D. insulare respond to bottom-up forces when its P. xylostella host larvae were reared on hostplants grown under different soil fertility treatments.

2. Materials and methods

2.1. Insects and plants

Laboratory colonies of P. xylostella and D. insulare were main-tained on potted B. napus cv. Q2 plants at 22 ± 0.5 �C with 16 hL:8 h D. Moths and wasps collected from commercial fields ofB. napus in Alberta, Canada were added to the culture every sum-mer to maintain genetic diversity.

Brassica napus plants were grown individually in 15.2-cm-diam-eter pots using sterile Metromix-220 (W.R. Grace & Co., Ajax,Ontario, Canada) as a potting medium. Treatment plants weregrown under four soil fertility regimes viz. 0.5, 1.0, 3.0 and 5.0 gpot�1 of 20:20:20 (nitrogen:phosphorous:potassium) (Plant Prod-ucts Co. Ltd., Brampton, Ontario, Canada), whereas control plantswere grown without any added fertilizer. Fertilizer treatmentswere applied in two split applications to avoid any phytotoxic

effects of higher concentrations: the first application was madeafter the second week of seed germination and the second applica-tion was made when plants were 3 weeks old. Each fertilizer treat-ment was applied after dissolving concentrate in 100 ml of tapwater while control plants received 100 ml water only. Four-week-old plants were used for all experiments.

2.2. Intact plant study

2.2.1. Tissue nutrient analysisLeaves from each replicate uninfested control plant were col-

lected at the end of the larval development experiment (15–17 days, Section 2.2.2), air-dried at room temperature, groundand subjected to nutrient analysis. The combustion method(AOAC-990.03) was followed for determination of total nitrogenand sulfur (AOAC International, 2003a), whereas calcium, phos-phorous, potassium, magnesium and sodium were assessed byusing the inductively coupled plasma spectroscopic method(AOAC-985.01) in Norwest Labs, Lethbridge, Canada (AOAC Inter-national, 2003b).

2.2.2. D. insulare: parasitism, escape and survivalOver 500 newly emerged P. xylostella were allowed to oviposit

on tinfoil sheets treated with an extract of B. napus leaves (Sheltonet al., 1991). After 24 h, egg sheets were collected, excised in pieceseach containing about 15–20 eggs, and incubated in individualplastic cups. Parasitism, escape and survival were assessed inscreened cages (40 � 40 � 80 cm), arranged on greenhousebenches in a completely randomized design with each cage consid-ered one replicate. Each cage contained a single plant; the entireexperiment used 75 cages with 15 plants from each treatment.Ten plants from each treatment were infested with first-instarP. xylostella larvae from incubation cups at 10 larvae per plant byholding neonates carefully from their silk to avoid handling dam-age, while the remaining plants served as uninfested controls fortissue nutrient analysis (Section 2.2.1). Larvae were observed dailyuntil they molted to second instars. Five plants of each soil fertilitytreatment received two female and two male wasps (63 days old)whereas the remaining five plants of each soil fertility served ascontrols infested with P. xylostella only (see Sarfraz et al., 2005a);wasps were allowed to parasitize P. xylostella larvae for 24 h andwere then removed from the cages. Larvae were kept on the sameplants to complete development and observed every 48 h; thenumbers of surviving larvae were recorded, but daily observationswere made when pupation began. Pupae were harvested, weighedwithin 24 h of pupation and kept individually in labeled transpar-ent plastic cups in a growth chamber at 22 ± 0.5 �C with 16 h L:8 hD until adult emergence. The numbers of individuals that success-fully developed into P. xylostella pupae despite being exposed to D.insulare were considered to have escaped parasitism.

It was assumed that mortality of P. xylostella larvae other thancontrol mortality was caused by parasitoids and the percent para-sitism was calculated using the following equation:

Parasitism ð%Þ ¼ ½ðPdi � LtÞ � 100� þMc

where Pdi is the numbers of D. insulare pupae that developed, Lt thetotal numbers of P. xylostella larvae introduced to each cage, and Mc

the percent corrected mortality determined by Schneider-Orelli’sformula (Schneider-Orelli, 1947).

2.3. Leaf tissue study: pre-imaginal and imaginal parameters

This study was conducted in controlled environmentalconditions in a growth chamber (22 ± 0.5 �C with 16 h L:8 h D).Excised leaves taken from uninfested plants were placed on moistfilter papers (9-cm-diameter) in plastic containers covered with

36 M. Sarfraz et al. / Biological Control 51 (2009) 34–41

transparent ventilated lids. For each soil fertility treatment, 100newly molted second-instar larvae (624 h old) taken from the lab-oratory colony were parasitized (each larva was offered to femalewasps individually and observed until parasitized) and introducedinto individual plastic containers in completely randomized designwith subsampling; a total of 500 larvae were used (10 replicatesper fertility treatment). Larvae were provided with fresh leaf tissueof their respective treatment plants every 24 h until pupation.Developmental times from egg to pre-pupa and from pre-pupa topupa were recorded. Pupae were harvested, weighed within 24 hof pupation, returned to their respective containers and develop-mental times from pupa to adult emergence were recorded. Afteradult eclosion, the silk cocoons were also weighed using a SartoriusSupermicro� Scale (Sartorius Inc., Edgewood, NY, USA). Adultswere separated by sex and used in the longevity (without food),body weight, and forewing and hindwing area experiments.

To quantify levels of larval feeding, all leaves damaged by par-asitized P. xylostella larvae were scanned daily into a digital formatusing a desktop scanner (Umax Powerlook 2100XL Flatbed Scan-ner, UMAX Technologies Inc., Dallas, TX, USA). Image J (NationalInstitutes of Health, Bethesda, MD, USA) was used to quantify theamount of leaf area removed due to larval herbivory.

Twenty females and 20 males of D. insulare (<1 day old) rearedfrom each treatment were used to determine their longevitieswithout food. Specimens were placed in individual plastic contain-ers in a growth chamber (22 ± 0.5 �C with 16 h L:8 h D) and exam-ined daily for survival or mortality. In a separate experiment, 20females and 20 males (61 day old) of D. insulare reared from eachtreatment were killed and their wet body masses were determinedusing a Sartorius Supermicro� Scale (Sartorius Inc.). Forewings andhindwings were carefully removed, glued onto paper, scannedusing a desktop scanner (Umax Powerlook 2100XL Flatbed Scan-ner), and their areas were measured using Image J as describedby Sarfraz et al. (2007).

2.4. Statistical analyses

Transformations ((x + 0.5)0.5, ln(x + 1)) were used as necessary toachieve normality and homoscedasticity before analysis (Steel et al.,1997), but untransformed means are presented graphically and intables. Analyses of variance (ANOVA) (PROC GLM) for a completelyrandomized design were performed to assess the differences amongtreatments, and means were compared at the 5% level of significanceusing Tukey’s studentized range test (Littell et al., 2002; SAS Insti-tute, 2004). Pearson correlation coefficients (PROC CORR) weredetermined between pre-pupal development time and silk weight,pupal weight and silk weight, pupal weight and adult weight, pupalweight and longevity without food, herbivory and adult weight,adult weight and longevity, pupal weight and forewing area, adultweight and forewing area, and forewing area and hindwing areafor both female and male specimens. T-tests (PROC TTEST) were per-formed for pair-wise comparisons between female and male insects

Table 1Mean (±SE) nutrients in leaf tissue of intact Brassica napus plants grown under different f

Leaf tissue nutrients (%) Fertilizer application rate (g pot�1)

0.0 0.5 1.0

Nitrogen 4.2 ± 0.1e 6.5 ± 0.0d 7.1 ± 0.0c

Phosphorous 0.2 ± 0.0c 0.8 ± 0.0b 1.1 ± 0.1a

Potassium 6.1 ± 0.0b 6.7 ± 0.0a 6.2 ± 0.0b

Sulfur 2.1 ± 0.0b 1.9 ± 0.0c 2.4 ± 0.0a

Calcium 2.2 ± 0.1b 1.9 ± 0.0c 2.6 ± 0.0a

Magnesium 0.9 ± 0.0a 0.6 ± 0.0c 0.7 ± 0.0b

Sodium 0.3 ± 0.0a 0.3 ± 0.0a 0.3 ± 0.0a

Means in a row followed by the same letter do not differ significantly (P = 0.05) using a

for their developmental times, larval herbivory, pupal weights, silkweights, adult body weights, longevity (without food), forewingand hindwing areas when they were reared on plants grown withvarious fertilizer applications.

3. Results

3.1. Intact plant study

3.1.1. Tissue nutrient analysisSoil fertility levels strongly influenced foliar nutrients in B. napus

(Table 1). Leaf nitrogen content increased with fertilizer applicationrate, with highest levels observed in plants grown at 5.0 g fertilizerand lowest levels in unfertilized plants. The highest levels of phos-phorous occurred in plants grown under 1.0 g, and these differedsignificantly from the controls and the other treatment plants. Phos-phorous contents did not differ in plants grown under 0.5, 3.0 and5.0 g fertilizer. The highest potassium contents occurred in plantsgrown at 0.5 g, and lowest in plants grown at 5.0 g. Leaf sulfur con-tents declined with an increase in fertilizer application rate, with thehighest levels found in plants grown at 1.0 g fertilizer while the low-est contents were in plants fertilized at 5.0 g pot�1. Calcium washighest in plants grown at 1.0 g and lowest in plants grown with5.0 g; calcium contents did not differ in plants grown at 0.5 and3.0 g fertilizer. The highest magnesium contents were present inunfertilized plants while plants treated with 5.0 g had the lowestconcentrations; magnesium contents did not differ in plants grownat 0.5 and 3.0 g fertilizer. Sodium concentration in plants fertilized at0.0, 0.5, 1.0 and 3.0 g were not significantly different; however,plants fertilized at 5.0 g had significantly less sodium comparedwith unfertilized plants (Table 1).

3.1.2. D. insulare: parasitism, escape and survivalBrassica napus nutrient regimes significantly affected mean per-

cent parasitism (F4,36 = 3.67, P = 0.01). Parasitism occurrence wasgreatest when host larvae were reared on plants grown with3.0 g fertilizer pot�1 (57.4 ± 5.8%), and this significantly exceededthat for hosts reared on plants grown with 0.0 and 5.0 g fertilizerpot�1, but not for hosts reared on plants grown with 0.5 and1.0 g fertilizer pot�1 (Fig. 1).

Host plant quality had a significant effect on avoidance/escapeof P. xylostella from D. insulare (F4,36 = 5.41, P = 0.002). P. xylostellaescape percentage was highest on plants fertilized at 1.0 g(32.0 ± 8.3%), but it did not differ among plants grown with 0.0,0.5, 3.0 and 5.0 g fertilizer (Fig. 1).

Plant nutrient regime on which host P. xylostella were rearedhad significant effects on survival of D. insulare from egg to pupa(F4,36 = 3.35, P = 0.02), but non-significant effects on survival frompupa to adult (F4,36 = 1.77, P = 0.16) (Table 2). Survival from eggto pupa on plants grown with 3.0 g fertilizer pot�1 was signifi-cantly greater than on plants grown without any added fertilizer,

ertilizer regimes.

F4,16 P

3.0 5.0

8.7 ± 0.2b 10.4 ± 0.1a 586.49 <0.0010.9 ± 0.0b 0.8 ± 0.0b 122.84 <0.0016.2 ± 0.0b 5.3 ± 0.0c 1081.75 <0.0011.4 ± 0.0d 1.2 ± 0.0e 667.07 <0.0012.0 ± 0.0c 1.1 ± 0.1d 292.30 <0.0010.6 ± 0.0c 0.4 ± 0.0d 88.58 <0.0010.3 ± 0.0a 0.2 ± 0.0b 51.33 <0.001

nalysis of variance and Tukey’s studentized range test.

20

30

40

50

60

70Parasitism %Escape %

0

10Mea

n Pa

rasi

tism

and

Esc

ape

(%)

0.0 0.5 1.0 3.0 5.0

Fertilizer Application Rate (g pot-1)

Fig. 1. Parasitism and escape (means ± SE) of Plutella xylostella larvae on intact plants in no-choice tests.

M. Sarfraz et al. / Biological Control 51 (2009) 34–41 37

but survival did not differ significantly among the other plantnutrient regimes (Table 2).

3.2. Leaf tissue study: pre-imaginal and imaginal parameters

Host plant nutrient quality on which P. xylostella larvae werereared significantly affected developmental times of D. insularefrom egg to pre-pupa, pupa to adult, and egg to adult for both fe-males (F4,76 = 12.52, P < 0.001; F4,76 = 12.74, P < 0.001 andF4,76 = 9.98, P < 0.001, respectively) and males (F4,76 = 24.35,P < 0.001; F4,76 = 66.29, P < 0.001 and F4,76 = 22.81, P < 0.001,respectively) (Table 3). Host plants grown with different soil fertil-ity regimes significantly affected developmental times from pre-pupa to pupa for females (F4,76 = 3.05, P = 0.02), but not for males(F4,76 = 0.04, P = 0.99) (Table 3). Foliage consumption by P. xylostellalarvae varied significantly when parasitized by female and malelarvae of D. insulare (F4,76 = 16.68, P < 0.001 and F4,76 = 10.90,P < 0.001, respectively), and pupal weights differed significantlyfor females and males (F4,76 = 4.25, P = 0.004 and F4,76 = 3.07,P = 0.02, respectively) (Table 4). Silk weight of D. insulare speci-

Table 2Mean percent survival (±SE) of Diadegma insulare from egg to pupa and from pupa to aduplants grown under various fertility regimes.

Developmental stages Fertilizer application rate (g pot�1)

0.0 0.5

Egg to Pupa 32.0 ± 4.9b 42.0 ± 4.4ab

Pupa to Adult 64.0 ± 8.3a 68.5 ± 7.4a

Means in a row followed by the same letter do not differ significantly (P = 0.05) using a

Table 3Mean (±SE) developmental times in days of Diadegma insulare female and male specimensnapus plants grown under five different soil fertility regimes.

Biological parameters Fertilizer application rate (g

0.0 0.5

Egg to pre-pupa (days) Female 7.9 ± 0.2a 6.4Male 8.3 ± 0.3a 6.1

Pre-pupa to pupa (days) Female 1.6 ± 0.2ab 1.2Male 1.4 ± 0.1a 1.4

Pupa to adult (days) Female 7.2 ± 0.3b 8.7Male 7.0 ± 0.2bc 9.2

Egg to adult (days) Female 16.7 ± 0.3a 16.3Male 16.7 ± 0.3a 16.7

Means in a row followed by the same letter do not differ significantly (P = 0.05) using a

mens was significantly affected by plant quality on which theirhosts were reared for both females (F4,76 = 9.98, P < 0.001) andmales (F4,76 = 5.97, P < 0.001) (Table 4). Host plant quality signifi-cantly affected adult body weight of females but not of males(F4,76 = 23.26, P < 0.001 and F4,76 = 2.26, P = 0.07, respectively).Adult longevity without food differed significantly for both femalesand males (F4,76 = 37.73, P < 0.001 and F4,76 = 59.66, P < 0.001,respectively) (Table 5). Forewing areas varied significantly for fe-males (F4,76 = 7.48, P < 0.001) and males (F4,76 = 2.71, P = 0.04).Plant quality strongly affected hindwing areas of males but notof females (F4,76 = 6.04, P < 0.001 and F4,76 = 1.55, P = 0.20 respec-tively) (Table 5).

Female and male development of D. insulare from egg to pre-pupa was fastest when hosts were reared on plants grown with0.5 and 3.0 g fertilizer pot�1. Both female and male pupae devel-oped slowest on plants grown under 0.5 g soil fertility. Egg to adultdevelopment was faster on plants grown with 5.0 g fertilizer thanon plants grown with 0.0, 0.5 and 1.0 g fertilizer (Table 3). P. xylo-stella larvae harboring female D. insulare consumed the largest leafarea when no fertilizer additions were made, whereas least foliage

lt when parasitized host Plutella xylostella larvae were reared on intact Brassica napus

1.0 3.0 5.0

42.0 ± 1.3ab 58.0 ± 6.5a 56.0 ± 5.8a

77.3 ± 6.3a 72.9 ± 5.9a 52.5 ± 8.1a

nalysis of variance and Tukey’s studentized range test.

when parasitized host Plutella xylostella larvae were reared on leaf tissue of Brassica

pot�1)

1.0 3.0 5.0

± 0.2c 7.3 ± 0.1ab 6.4 ± 0.2c 6.7 ± 0.2b

± 0.1c 7.2 ± 0.1b 6.4 ± 0.1c 6.6 ± 0.2bc

± 0.1b 1.7 ± 0.1ab 1.9 ± 0.2a 1.6 ± 0.1ab

± 0.1a 1.4 ± 0.1a 1.4 ± 0.2a 1.4 ± 0.2a

± 0.2a 7.7 ± 0.1b 7.3 ± 0.1b 7.0 ± 0.1b

± 0.2a 7.2 ± 0.1b 6.7 ± 0.2bc 6.6 ± 0.1c

± 0.2ab 16.7 ± 0.1a 15.6 ± 0.2bc 15.3 ± 0.2c

± 0.3a 15.8 ± 0.2a 14.5 ± 0.2b 14.6 ± 0.1b

nalysis of variance and Tukey’s studentized range test.

Table 5Mean (±SE) adult body weights, longevity without food, forewing and hindwing areas of Diadegma insulare female and male specimens when parasitized Plutella xylostella hostlarvae were reared on leaf tissue of Brassica napus plants grown under five different soil fertility regimes.

Biological parameters Fertilizer application rate (g pot�1)

0.0 0.5 1.0 3.0 5.0

Adult body weight (mg) Female 0.7 ± 0.0c 1.1 ± 0.0ab 1.0 ± 0.0b 1.3 ± 0.1a 0.7 ± 0.0c

Male 0.8 ± 0.1a 1.0 ± 0.0a 1.0 ± 0.1a 1.0 ± 0.1a 1.0 ± 0.1a

Longevity without food (days) Female 2.0 ± 0.2b 3.5 ± 0.1a 3.7 ± 0.1a 3.7 ± 0.1a 3.7 ± 0.1a

Male 3.0 ± 0.1c 1.7 ± 0.2d 3.6 ± 0.1b 4.4 ± 0.2a 3.6 ± 0.1b

Forewing area (mm2) Female 4.8 ± 0.1b 4.8 ± 0.1b 5.3 ± 0.2ab 5.7 ± 0.1a 5.1 ± 0.1b

Male 4.9 ± 0.2ab 4.4 ± 0.1b 4.3 ± 0.2b 4.7 ± 0.3ab 5.2 ± 0.2a

Hindwing area (mm2) Female 2.9 ± 0.6a 2.0 ± 0.0a 2.3 ± 0.1a 2.9 ± 0.1a 2.6 ± 0.1a

Male 2.1 ± 0.2ab 1.7 ± 0.1b 2.2 ± 0.1ab 2.2 ± 0.1ab 2.6 ± 0.1a

Means in a row followed by the same letter do not differ significantly (P = 0.05) using analysis of variance and Tukey’s studentized range test.

Table 4Mean (±SE) foliage consumption, pupal weights and silk weights of Diadegma insulare female and male specimens when parasitized Plutella xylostella host larvae were reared onleaf tissue of Brassica napus plants grown under five different soil fertility regimes.

Biological parameters Fertilizer application rate (g pot�1)

0.0 0.5 1.0 3.0 5.0

Foliage consumed (cm2) Female 3.0 ± 0.2a 2.8 ± 0.2a 2.4 ± 0.1ab 1.8 ± 0.1bc 1.4 ± 0.0c

Male 2.7 ± 0.1a 2.5 ± 0.2ab 1.9 ± 0.1bc 1.6 ± 0.1c 1.2 ± 0.0c

Pupal weight (mg) Female 3.9 ± 0.2b 4.1 ± 0.1ab 4.4 ± 0.1a 4.4 ± 0.1a 3.9 ± 0.1b

Male 4.1 ± 0.1a 3.9 ± 0.1ab 3.6 ± 0.1b 4.2 ± 0.1a 4.2 ± 0.1a

Silk weight (mg) Female 0.5 ± 0.0b 0.5 ± 0.0b 0.6 ± 0.0a 0.6 ± 0.0a 0.6 ± 0.0a

Male 0.6 ± 0.0b 0.7 ± 0.1a 0.6 ± 0.0b 0.7 ± 0.0a 0.7 ± 0.0a

Means in a row followed by the same letter do not differ significantly (P = 0.05) using analysis of variance and Tukey’s studentized range test.

38 M. Sarfraz et al. / Biological Control 51 (2009) 34–41

consumption occurred on plants grown with 5.0 g fertilizer pot�1

(Table 4). Female pupae were heavier when their P. xylostella hostswere reared on plants grown with 1.0 and 3.0 g fertilizer than onplants grown with 0.0 and 5.0 g fertilizer, but weights of male pu-pae were significantly lighter when host larvae were reared onplants fertilized at 1.0 than at 3.0 g pot�1 (Table 4). Female speci-mens reared on P. xylostella hosts that consumed plants fertilizedat 1.0, 3.0 and 5.0 g pot�1 produced significantly more silk thanthose from hosts that consumed plants grown with 0.0 and 0.5 gfertilizer pot�1. Males produced more silk when parasitizedP. xylostella larvae were fed on plants grown with 0.5, 3.0 and5.0 g fertilizer than on plants grown without any added fertilizer(Table 4).

Heaviest females of D. insulare were produced on P. xylostellahosts reared on plants fertilized at 3.0 g pot�1; however, bodyweights of males did not differ significantly when reared on plantsgrown under various soil fertility regimes (Table 5). Female waspsreared on P. xylostella hosts that consumed unfertilized plants livedfor the shortest time in the absence of food whereas males rearedon plants grown at 1.0, 3.0 and 5.0 g fertilizer pot�1 lived the lon-gest time. Female and male wasps reared on larvae that fed onplants grown with 3.0 and 5.0 g fertilizer had the largest forewings,respectively. Regardless of fertilizer treatments, hindwing areas forfemales did not differ significantly; males with largest hindwingswere from larvae reared on plants grown at 5.0 g fertilizer pot�1

(Table 5).For female specimens reared on P. xylostella hosts that con-

sumed host plants varying in quality, significant correlations werefound between pre-pupal development time and silk weight(r = 0.31, P = 0.002), pupal weight and silk weight (r = 0.39,P < 0.001), pupal weight and longevity (r = 0.21, P = 0.04), pupalweight and forewing area (r = 0.41, P < 0.001), adult weight andlongevity (r = 0.23, P = 0.02), adult weight and forewing area(r = 0.25, P = 0.01), and forewing area and hindwing area (r = 0.25,P = 0.01), but no correlations existed between herbivory and adultweight (r = �0.07, P = 0.52), and pupal weight and adult weight

(r = 0.16, P = 0.10). For males, significant correlations were foundbetween pupal weight and adult weight (r = 0.29, P = 0.003), pupalweight and forewing area (r = 0.37, P < 0.001), forewing area andhindwing area (r = 0.42, P < 0.001), but no correlations existed be-tween pre-pupal development time and silk weight (r = 0.12,P = 0.24), pupal weight and silk weight (r = �0.01, P = 0.94), pupalweight and longevity (r = 0.12, P = 0.23), adult weight and longev-ity (r = 0.05, P = 0.64), adult weight and forewing area (r = 0.10,P = 0.32), and herbivory and adult weight (r = 0.11, P = 0.28).

Female and male D. insulare exhibited significant differences inonly a few life-history traits when reared on plants receiving thesame treatment. Pupa to adult development was slower for fe-males than their male counterparts when parasitized P. xylostellalarvae were reared on plants treated at 1.0, 3.0 and 5.0 g fertilizerpot�1 (t = 3.58, df = 1, 37, P < 0.001; t = 2.89, df = 1, 31, P = 0.01, andt = 2.63, df = 1, 38, P = 0.01, respectively). Female pupae were hea-vier than male pupae when parasitized host larvae were reared onplants grown with 1.0 g fertilizer whereas male pupae were hea-vier than female pupae when reared on plants fertilized at 5.0 g(t = 5.02, df = 1, 29, P < 0.001, and t = 2.61, df = 1, 35, P = 0.01,respectively). Females were heavier with larger forewings andhindwings than their male counterparts when parasitized P. xylo-stella larvae were reared on plants grown with 3.0 g fertilizer perpot. Males reared on plants grown with 0.0 and 3.0 g fertilizer livedlonger without food than females, but females from 0.5 g soil fer-tility plants were more long lived than their male counterparts(t = 4.25, df = 1, 26, P < 0.001; t = 3.31, df = 1, 30, P < 0.01, andt = 9.80, df = 1, 36, P < 0.001, respectively).

4. Discussion

Variation in soil fertility influenced the nutritional quality ofhost plants and this in turn affected the performance of D. insulare.In general, D. insulare performed best on P. xylostella larvae thatdeveloped on plants grown with 3.0 g fertilizer; these plants had2.06-, 3.77-, and 1.02-fold more nitrogen, phosphorous and

M. Sarfraz et al. / Biological Control 51 (2009) 34–41 39

potassium, respectively than plants grown without any addedfertilizer. By contrast, our earlier research indicated that overallperformance of non-parasitized P. xylostella hosts was better onplants grown at 1.0 g fertilizer than on other treatment plants(Sarfraz et al., 2005a). Parasitism and survival of D. insulare variedconsiderably among the tested soil fertility regimes on which hostP. xylostella larvae were reared with most on plants grown with3.0 g fertilizer and least on unfertilized plants. Some previousevidence exists that parasitism rates by D. insulare were signifi-cantly higher on high-nitrogen collard plants (Brassica oleraceaL. var. acephala) than on low-nitrogen plants (Fox et al., 1990). Con-trary to the present findings, Fox et al. (1996) found that D. insularesurvival/adult emergence was higher on ‘‘low-fertilizer” collardplants than on ‘‘high-fertilizer” plants. However, we were unableto determine how much fertilizer was actually used to grow‘‘low-fertilizer” and ‘‘high-fertilizer” plants in their study, and theauthors did not provide data on tissue nutrient contents of theirtreatment plants.

Our study suggested a complex interaction of the soil matrix(which might have had traces of nutrients) with the added fertil-izer: soil fertility treatments led to increased foliar nitrogen con-tent, while phosphorous and potassium contents peaked andthen decreased, and magnesium and sodium contents decreasedas well (Table 1). This might be due to direct impact on the siteof ion uptake in the roots (competition) and/or indirect effectscaused by changes in soil pH. Nevertheless, soil fertilization influ-enced the nutritional quality of B. napus plants which in turn af-fected performance of the parasitoid.

Plutella xylostella escape from D. insulare was highest on plantsgrown at 1.0 g fertilizer. This could be attributed to plant physiol-ogy, and both physical and physiological defensive mechanisms ofthe herbivores mediated by host plant quality. Plant physiologycan affect the parasitoid foraging, for instance by changing volatilecues upon herbivory or via influences on the epicuticular waxes(Tumlinson et al., 1992; Eigenbrode, 2004; Gentry and Barbosa,2006). Herbivore hosts can sometimes physically deter parasitoidssuccessfully, for instance by wriggling, walking away, jumping,kicking, dropping off the plant or secreting defensive chemicals(Godfray, 1994). P. xylostella larvae can deter parasitism primarilyby wriggling and dropping off the plant, where they can hang sus-pended on silken threads until the parasitoid departs (Sarfraz, per-sonal observation). Similarly, Myzus persicae (Sulzer) (Homoptera:Aphididae) successfully escaped from Aphelinus flavus Nees (Hyme-noptera: Aphelinidae) in 58% of oviposition attacks by walkingaway and dropping off the plant (Wilbert, 1967; Jansson, 2003).The immune systems of herbivore hosts can also defend againstparasitism (e.g., through encapsulation), and kill the parasitoideggs or larvae. Plant quality can affect the ability of a herbivoreto encapsulate parasitoid eggs (Cheng, 1970; Benrey and Denno,1997); the success of encapsulation depends on the vigor of theherbivore, and this can be influenced by host plant nutritionalquality and suitability (Muldrew, 1953; van den Bosch, 1964; Vin-son and Barbosa, 1987). A plant with toxins or low nutritionalquality that renders the herbivore host weakened may suppressits immune system and thereby benefit the parasitoid. In thisstudy, physiological mechanisms were also likely involved becauserelatively high numbers (ca. 8–10%) of P. xylostella larvae that wereindividually parasitized for life-history trait experiments devel-oped into P. xylostella pupae instead of D. insulare when rearedon plants grown at 1.0 g fertilizer. By contrast, larvae of P. xylostellareared on plants subjected to other soil fertility treatments escapedparasitism by D. insulare less frequently (ca. 0–4%) (Sarfraz, unpub-lished data).

Sarfraz et al. (2005a) determined that among these soil fertilitytreatments, the application rate of 1.0 g pot�1 was optimal forP. xylostella. Mean numbers of P. xylostella eggs per plant and percent

survival from neonate to pupa were greatest on plants fertilized at1.0 g pot�1. In addition, larval and pupal development rates werefastest when plants were fertilized at this rate. Here, we report thatthis rate is also optimal for enabling P. xylostella to escape parasitismby D. insulare. Evidently the ability of P. xylostella females to selecthost plants with optimal nutrient levels confers benefits that extendbeyond merely rapid developmental rates of their offspring; optimalplant nutrients enhance survival of their offspring whether or nottheir larvae are under attack by D. insulare.

Plant quality on which P. xylostella hosts were reared signifi-cantly affected developmental times of both female and maleD. insulare. Nutritional sufficiency and quality of the plant canaffect parasitoid development (Vinson and Iwantsch, 1980). Forinstance, performance of the parasitoid Venturia canescens (Graven-horst) (Hymenoptera: Ichneumonidae) varied when parasitizedPlodia interpunctella (Hübner) (Lepidoptera: Pyralidae) hosts werereared on artificial diets of different quality; parasitoids took longerto develop and experienced higher mortality when reared in hoststhat were fed on low-quality diet (Harvey et al., 1995). For femalespecimens of D. insulare, slowest development from egg to pre-pupa and from pupa to adult occurred on host larvae reared onplants grown with 0.0 and 0.5 g fertilizer, respectively. Accordingto the ‘‘Slow Growth-High Mortality Hypothesis”, individuals feed-ing on larvae reared on these treatment plants may have an ex-tended window of vulnerability to natural enemies (Benrey andDenno, 1997). On the other hand, D. insulare egg to adult develop-ment was shorter (about 1 day) when parasitized P. xylostella hostswere reared on plants grown with high soil fertility than on plantsgrown with no or intermediate soil fertility. Development ofP. xylostella from egg to adult is more rapid in tropical than in tem-perate regions, with as many as 20 generations per year possible inthe tropics (Sarfraz et al., 2005b). The 1-day difference in develop-ment time of D. insulare at higher levels of soil fertility may result inan additional generation per year in tropics, and thereby enhancethe biological control of P. xylostella in those regions.

Increased nitrogen and other nutrients can lead to unbalancedamino acid profiles and large concentrations of organic acids inplant tissues; consequently, such diets can be detrimental andeven toxic to insects (Brodbeck et al., 1990). Parasitized P. xylostellalarvae consumed more foliage of plants grown at low and interme-diate soil fertility levels than at high fertility. Substantial evidenceexists that insects need to compensate for lowered concentrationsof nitrogen (and possibly other nutrients) by increasing food intake(Slansky and Feeny, 1977; Berner et al., 2005). The plants grown atdifferent soil fertility regimes influenced the pupal weights, silkweights, adult body weights, longevities, and sizes of forewingsand hindwings of D. insulare when parasitized P. xylostella hostswere reared on plants subjected to various soil fertility treatments.Growth is governed by the rate of biomass gain, the efficiency ofconversion of food into tissue, and the metabolic costs of mainte-nance (Calow, 1977; Sequeira and Mackauer, 1992). For a givenset of environmental conditions, efficient growth should yieldmaximum biomass at minimum metabolic cost in the shortestdevelopmental time. Parasitoid larval growth provides a directmeasure of host quality because it reflects the nutritional interac-tions between the two species throughout the course of parasitism.Because nutrient reserves accumulated by larvae feeding on differ-ent quality plants may not be the same, these differences can haveconsequences on adult life-history parameters, including fecun-dity, longevity (Boggs, 1981; Sequeira and Mackauer, 1992) andbody size. Body size is an important fitness index because it oftenaffects reproductive success through variations in fecundity, lon-gevity, dispersal, searching efficiency, and host handling strategies(Charnov and Skinner, 1984; Visser, 1994; Kazmer and Luck, 1995).Reduced wing areas can also affect parasitoid fitness by affectingits dispersal and foraging efficiency.

40 M. Sarfraz et al. / Biological Control 51 (2009) 34–41

Investigation of tritrophic interactions involving canola sub-jected to varying levels of nutrient stress and vigor, being fed uponby P. xylostella larvae under attack by D. insulare parasitoids, hasuncovered a complex series of bottom-up effects influencing alltrophic levels. As expected, soil fertility inputs were reflected inleaf tissue nutrient contents, and as a consequence, developmentof the herbivore was slowed at low soil fertility levels and occurredmore rapidly at intermediate levels (Sarfraz et al., 2005a). At lowsoil fertility levels, P. xylostella adults deposited fewest eggs, andeven though their larvae consumed more leaf tissue when nutri-ents were limiting, development progressed more slowly thanwhen fertility was intermediate. Here, we found that most param-eters of the parasitoid indicated optimal fitness when D. insularewere reared on P. xylostella larvae that fed on plants fertilized atthe high rates. Canola stressed by low nutrient levels has poor seedyields, even in the absence of insect herbivory (Thomas, 1990), andalthough higher levels of soil fertility can predispose plants to in-creased infestations of P. xylostella, increased fertility also enhancesdevelopment and survival of D. insulare. Vigorous, well nourishedplants can better compensate for insect attack than plants undernutrient stress (Dosdall et al., 2004; Sarfraz et al., 2005a), so main-taining relatively high levels of soil fertility seems appropriate forintegrated management of P. xylostella in canola. It is probable thatthis recommendation also applies to other brassicaceous crops un-der attack by P. xylostella.

Acknowledgments

This research was funded by the University of Alberta F.S. ChiaScholarship, the Queen Elizabeth-II Scholarship, the Alberta Societyof Professional Biologists Scholarship, and the Canadian Society ofAgronomy Pest Management Research Award to the senior author.In addition, funding support from grants to LMD provided by theCanola Council of Canada, the canola producer commissions ofAlberta, Saskatchewan and Manitoba and the Natural Sciences andEngineering Research Council of Canada are gratefully acknowl-edged. We also thank B. Laxton and G. Hilchie for technical support.

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