5 18 b In a 19 , E. eremi- 18 . However, control. eremicus . E T. vaporariorum and Nicolas Desneux Until now, it was unknown whether IGP a 22 , performed IGP on engages in intraguild (IGP), the (Hymenoptera: Aphelinidae) are whitefly 21 on the whitefly decreases when IGP takes a* Trialeurodes prey upon nymphs and adults of the wasp punctipes punctipes . . G G G. punctipes This kind of trophic interaction, in which one natural enemy 20 Correspondence to: Ricardo Ramirez-Romero,Agrícola, Departamento CUCBA, de Universidad Producción deZapopan, Jalisco, Guadalajara, Mexico. E-mail: Apartado [email protected] Postal 139, 45110 Departamento de Producción Agrícola, CUCBA,Zapopan, Jalisco, Universidad Mexico de Guadalajara, French National Institute forAntipolis, Agricultural Institut Research Sophia Agrobiotech, (INRA), Sophia-Antipolis, France Univ. Nice Sophia . and its influence ∗ a b on the whitefly was nevertheless higher when both natural This polyphagous predator has a nymphal developmentdays of and 23–36 a subsequent adult stageAdults than can of last up this to 108can days. species start can oviposition after mate 5 3 days following days emergence. after emergence and between these two species tooknarios, place such under as more field complexthe sce- or effect semi-field of IGP conditions. occurrence Also on unknown was of a target pest preys onis another known natural as enemy intraguild of predation the (IGP) and sameious can pest, natural take enemies. place with var- companion study, we foundG. punctipes that, under laboratory conditions, cus Eretmocerus eremicus 17 – This 6 Rose , does occur under semi-field conditions, it does not adversely affect 14 5 2 , , 2 . However, it is unknown whether this IGP interaction takes place under 1 G. punctipes This solitary José Sánchez-Martínez 9 a – eremicus 7 . E. eremicus Bemisia argentifolii E Its hemimetabolous on 4 – Ricardo Ramirez-Romero, 2 (: ) is (Hemiptera: Aleyrodidae) a Eretmocerus eremicus (Hemiptera: Lygaeidae) and 13 in tomato. G. punctipes Its pre-imaginal developmental period can Geocoris punctipes : 1110–1116 www.soci.org © 2015 Society of Chemical Industry 12 72 – 10 T. vaporariorum Geocoris punctipes The whole life cycle can last up to 30–80 days 2 2016; Trialeurodes vaporariorum Lygaeidae; Aphelinidae; Aleyrodidae; intraguild predation Eretmocerus eremicus

The rates of oviposition and infestation are influenced by 2

In turn, the predator One of the whitefly natural enemies used successfully as a factors such as environmentalintraspecific conditions, competition and host presence of plant, natural inter- enemies. and and Zolnerowich (Hymenoptera: Aphelinidae). biocontrol agent is the parasitoid Pest Manag Sci is a sucking pest, native to Central and South America. 1 INTRODUCTIONThe whitefly Abstract BACKGROUND: natural enemies. Previously, under laboratory conditions, we showed that Carla V Sánchez-Hernández, Lourdes Bao-Fundora, Intraguild predation of (wileyonlinelibrary.com) DOI 10.1002/ps.4163 Research Article Received: 17 July 2015 Revised: 29 September 2015 Accepted article published: 5 October 2015 Published online in Wiley Online Library: 27 October 201 on (depending upon temperature),year. with multiple generations per life cycle includes cylindrical eggs, fourdevelopment. nymphal instars and adult whitefly is a cosmopolitan species consideredpest, to as be an it important crops, can such lead as to tomato, cotton substantial and economic beans. losses in different last from 16 to 32 days,oviposit and on females average can about live five for eggs up per day to on 11 days and Bellows & Perring nymphs as hosts. endoparasitoid prefers towhitefly oviposit nymphs. on second- and third-instar another common natural enemy of this pest in the Americas. attack of one natural enemy by another, on

more complex scenarios, such asthe semi-field prey conditions. population Even requires investigation. more Therefore, importantly,semi-field the the present conditions study effect and aimed of to to this establish determineplace. interaction whether whether on this the IGP the takes predation density place rate of under of RESULTS: Molecular analysis showed that,although under IGP semi-field did conditions, take place, the predation rate by on the control of the whitefly vaporariorum enemies were present together than when the predator was present alone. CONCLUSION: While IGP of whitefly control. The concomitantprogrammes of use of these two natural enemies seems a valid option for inundative biological control Keywords: © 2015 Society of Chemical Industry

1110 1111 ), ′′ 2 43 ′ 30 Canda ∘ ∘ 20 18 5 g of artifi- ≈ 10.8 ’), a microcosm N, 103 Parasitoids were ± and can live up to Gp ′′ 22 with 35 + 47 ′ 28.16% were recorded Tv ± 44 ∘ , Mexico City, Mexico). Any ad libitum ® SD) of 25.31 ± wileyonlinelibrary.com/journal/ps Instruments, Waltham, MA, USA). SD) of 55.48 ® ± Female predators were used in experiments 20 63 cm) and fed × 1.8 m) with sides containing anti-aphid mesh, placed 63 × . pollen (5 g; Apiarios Rancaño, Mexico City, Mexico) and × 3 45.0 cm) and inspected daily to determine adult emer- × 20 13 × magnifying glass (Victorinox × 30.0 Within the field cages we set up microcosms containing the We established five treatments: (1) control (only whitefly Treatment 1 (hereafter referred to as the ‘control’) consisted In treatment 2 (hereafter referred to as ‘ containing whitefly nymphs wastors set were up, released andpreliminary within observations, six the we female used microcosm. six preda- females Taking in each into microcosm account first-stage nymphs thatremoved from were the plants. Thus, present the experimental at set-up200–230 contained this nymphs at the time second or point third nymphal were stage. (Datalogger RHT10; Extech tested treatments. Each microcosmenclosed consisted in of a plastic a cylinder tomatowith (28 plant cm six high holes and (each 18 9.5 cmmesh cm in for diameter) in ventilation. diameter) covered Beforemicrocosms with was use anti-aphid infested in with experiments,allowed 150 each to adult of oviposit whiteflies, these were for which removed were 48 from the h. microcosms,to and After laid develop this eggs for were period, allowed 14the whitefly days. number adults After of this nymphs40 period at of the time, second we and recorded third stage using a in campus experimental grounds (20 cial diet, gence date. Upon emergence,(7:3 adults mL, were honey:water), which fed was offered a on a honey paper solution towel (5 cm 2.2.2 Parasitoid Eretmocerus eremicus Parasitoids were provided by Koppertqués, Querétaro, Mexico) México as parasitised SA nymphs in de cardboardping CV ship- containers. The (El nymphs were placed Mar- inside acrylic cages× (38.5 sorghum seeds (10 g, var.Artificial UDG-110; Universidad diet de was Guadalajara). replacedseeds once every a day, week. and pollen and sorghum nymphs); (2) whitefly nymphs and predators;predators (3) and whitefly nymphs, parasitoids, introduced concomitantly;nymphs, (4) parasitoids whitefly and predators, introducedwhitefly consecutively; nymphs (5) and parasitoids. of microcosms containingthe whitefly same nymphs environmental andother treatments, and submitted but without experimental to naturaltrol enemy conditions exposure. allowed This as con- us the G. punctipes to establish a benchmark predation rate for mean relative humidity ( 2.3 Experimental set-up Bioassays were carried out under field conditions within woodcages field (3 W) (CUCBA, Universidad de Guadalajara). During theperiod, experimental a mean temperature ( 2.2.3 Predator GeocorisPredators punctipes were provided by Organismos Benéficos paratura la Agricul- (Autlán de Navarro,arrival Jalisco, in Mexico) our as laboratory, nymphs. nymphscages Upon were (40 placed their inside polystyrene when they were 8–20produce days fertile old eggs because and after they can 5 live days up females to 108 can days. and tap water; food was replaced every day. 11 days. used when they were 2–4can days mate and old oviposit because when it they are is 1 known day old that they 28 28 , 27 might ; CUCBA, ® G. punctipes Therefore, if is confronted 34 More specifically, 26 G. punctipes – 10% relative humidity 23 on the whitefly could be L. cv. ‘Saladette’) were 10% and a 14:10 h (light: ± G. punctipes ± The IG predator 45.0 cm) with sides covered 32 × C, 50 ∘ or maintaining the pest control 3 30.0 32 ± × G. punctipes found that the rate and direction of 27 : 1110–1116 © 2015 Society of Chemical Industry ; Germinaza SA de CV, Guadalajara, Jalisco, et al. decreases when IGP is taking place. ® 72 increasing Solanum lycopersicum 31 – For example, it has been proposed that the prefer- 2016; 29 33 C, a relative humidity of 50 ∘ 3 G. punctipes ± Indeed, it has been shown that IGP can influence pest control Complementary studies under more natural conditions are preferably prey upon adult waspstion (i.e. in exhibit the IGP). predation rate If of expected so, (relative to a conditions in reduc- which with whitefly nymphs only).this Therefore, study, we as aimed to a determine second whetherrate the by objective whitefly predation of IGP was influenced byis the important pubescence to ofmodifies the the determine IGP leaves. observed whether under Clearly, laboratory a it importantly, conditions the and, potential more more effect of this complex interaction on pest scenario control. by reducing, important because factorscosystems, related such as environmental to variations, plant size the or structure and complexity leaf properties of (e.g. epicuticular waxes, agroe- trichomes orcan domatia), influence interactions among . Pest Manag Sci 2.2.1 Whitefly Trialeurodes vaporariorum Whiteflies used infounded by the individuals provided by experiments(Universidad Dr Carla de came Sanchez-Hernández Guadalajara) from andAleyrodidae specialist taxonomically our Dr verified Vicente colonies Carapia by (Universidaddel Autónoma the Estado de Morelos, Cuernavaca, Morelos,virus-free Mexico). whiteflies. These These were colonies were rearedplaced on tomato in plants acrylic cages (38.5 bought at La CasaSeeds del were Hortelano planted (Guadalajara,ronmental on Jalisco, conditions Mexico). of plastic 24 germinating trays under envi- dark) photoperiod. with anti-aphid mesh. 2.1 Plants Tomato seeds ( 2 MATERIALS AND METHODS For example, the IGP ratebioassays, was compared with reduced bioassays when using arenas plants without were plants. Moreover, used Seelman in Intraguild predation and its influence on whitefly control www.soci.org ence of IG predators can playtion a rate of role the in IG the predator on net pests. effect of the preda- unchanged. is known to prefer moving prey to immobile prey. this IG predator were confrontedversus with mobile immobile prey (adult prey wasps) (whitefly nymphs), these properties of environmental complexity can affect IGP. 2.2 Insects All insects were reared in acclimatisedof chambers 24 at a temperature Mexico). Plants were grownimental under cages natural (see conditions below)they in and had were exper- reached used theprotected in fourth from experiments leaf exposure once containing of to anti-aphid development. herbivores mesh-covered Plants using windows were type of plastic (see pesticide application below). cylinders was strictly Any avoided. and a 12:12 h (light:dark)third photoperiod. leaf When plants of reachedplastic the development, pots (16 they cm were high,a 18 transferred cm mixture to in diameter). individual consisting Each pot of contained vermicompost (Lombrifert Universidad de Guadalajara,and Zapopan, coir Jalisco, (Germinza Mexico), pumice C 44 or ∘ Lof ,0.5 et al. μ 2 45 (sequen- CCCGC on white- PCR buffer C for 3 min, : 1110–1116 Gp ∘ × 100, and the in treatments 72 The mean per- ⇒ × 43 -specific primers also engaging 100, among treat- Ee T. vaporariorum 143 bp amplicon. 2016; 100, were also sub- ∼ 1) transformations × + C for 40 s and a final ∘ G. punctipes × + (individual release). detection using previ- Tv x C until required. For PCR G. punctipes Gp ∘ E. eremicus + 20 -ATACTCAAAATCCTT 42 ′ − Tv G. punctipes /5 Pest Manag Sci ′ DNA or autoclaved distilled water T. vaporariorum L containing 500 ng of DNA, 1 M of each primer and 2 U of Invitrogen Taq C for 10 min. Prey DNA ( μ μ ∘ C for 30 s, extension at 72 G. punctipies ∘ (simultaneous release) and All analyses were performed using R, v.3.1.1. , i.e. [number of whitefly nymphs preyed upon by Ee )and 43 + tests were performed, with contrasts derived from the lin- Gp + ) were designed from the internal transcribed spacer (ITS-1) -TTGGTGTCTCAATTTTATATC-3 100, among all treatments using a generalised linear model ′ ′ TE buffer (10 mM of Tris-HCl, 1was mM checked of EDTA, pH by 8.0). DNA agarosea integrity gel Q5000 Quawell electrophoresis spectrophotometer andJose, (Quawell CA, quantified USA). Technology, by San DNA was stored at tial release) and compared thesenymphs with preyed the upon in percentage treatment of whitefly another tube, and the DNA was precipitated withpellet isopropanol. was The washed with 70% ethanol and resuspended in 35 analysis, the mitochondrial cytochromegene oxidase was subunit targeted I for (COI) ously reported Tv1F/Tv1R primers. jected to a one-way ANOVA, but after log ( E. eremicus were included as positive and negativeproducts controls were respectively. separated PCR by electrophoresisstained in 1.5% with agarose gels ethidiumA bromide predator and was visualised consideredDNA under to was not be UV detected negative after light. two forreported separate analyses. prey as The DNA results the are proportion ifdetected of prey (i.e. predators the in number which ofthe prey predators total with DNA number prey of was analysed DNA predators). divided by 2.5 Whitefly predation rate by predator/initial number of whitefly nymphs] ments, we used ahomoscedasticity one-way requirements. ANOVA, For aspared data whitefly the mean met density, percentage of normality emerged we whiteflyber and of adults, com- emerged i.e. whitefly [num- adults/initial number of× whitefly nymphs] (GLM) with a gamma error and a log link function. 2.6 Data analysis To compare the meanG. percentage punctipes of nymphs preyed upon by region (Genbank AB662973) to generate a (50mMofKCl,20mMofTris-HCl,pH8.4),1.5mMofMgCl to fit normality and homoscedasticity requirements. For all models, the block was included as anPost hoc explanatory variable in eachear model. model. mean percentage ofwasps/initial emerged number wasps, of i.e. whitefly [number nymphs] of emerged centage of parasitised nymphs, i.e.fly [number of nymphs/initial parasitised number white- of whitefly nymphs] (5 mM of each dNTP,0.5 DNA polymerase (Life Technologies, Sao Paulo, Brazil).conditions The cycling were set as follows:for 3 initial min, denaturation followed by step 45 cycles atannealing of at 95 denaturation 63 at 95 extension step at 72 in IGP To determine whether the predation rate of flies decreased under IGP scenarios,age of we whitefly nymphs focused preyed on upon by theTv percent- Primers were tested for cross-reactivityPCR and amplifications performance were performed in in PCR. (ESCO, a Philadelphia, Swift PA, maxi USA). thermo Reactions cycler reaction were volume prepared of in 25 a total -3 E. ). In Cfor ’), we ∘ Gp Gp Both nat- ⇒ www.soci.org L Bao-Fundora 13 ) six female ⇒ ’),wesimul- Ee C freezer for 38 ∘ Ee + © 2015 Society of Chemical Industry Lofextraction Ee Briefly, individ- μ + ’) consisted of a 20 Tv 41 + 37 Ee − Gp Tv + + et al. 19 males) into a micro- .Forthesetreatments, Tv Tv + )and4( Ee and host density. Lof3Msodiumacetate(pH μ + Atthesametime,waspswere C until further analysis (prey DNA Gp ∘ 37 The number of parasitised nymphs G. punctipes + 39 , 2 C for subsequent analysis for whitefly Tv E. eremicus ∘ ), 3 ( Gp + 19 males) into a microcosm containing whitefly We followed a randomised block design, with time Tv 40 + , 38 , After this period of time, predators were removed from 20 . 36 In treatment 3 (hereafter referred to as ‘ In treatment 4 (hereafter referred to as ‘ For treatments 2, 3 and 4, we recorded the number of white- Treatment 5 (hereafter referred to as ‘ these analyses, DNA (includingDNA) possible was extracted whitefly from and predatorsfollowing parasitoid using the whole protocol predator described bodies by Cenis was recorded 18 days following thenumber parasitism of period. Finally, emerged the waspsparasitism was period. recorded These 25 time daysnymphs points and following adult for wasps the were counting determined in of accordancelier with observations ear- parasitised and previous literature on the development of eremicus buffer (200 mM ofEDTA, 0.5% Tris-HCl, SDS). pH A 8.5, quantity of5.2) 250 100 was mM of added, NaCl, and 25 tubes mM were of placed in a 10 min. After centrifugation, the supernatant was transferred to wileyonlinelibrary.com/journal/ps to determine nymph consumption ratean per initial female number per of day, availablethe with female nymphs predators were of allowed to 200–230. forage within thefor After microcosm 48 release, h. microcosms, preserved in 70% ethanol (v:v) and stored at 4 subsequent analysis for whitefly DNA detection. also removed from microcosms and preserved in ethanol. 2.4 IGP assessmentTo by molecular determine analysis whether IGPlooked occurs for under traces naturaltreatments of conditions, 2 we prey ( DNA in predator homogenates from as the blocking factor. Each treatment was replicated 11 times. and parasitoid DNA detection. ural enemies were allowed toAfter forage this during period of 48 time, hin predators concomitantly. were 70% captured ethanol and (v:v) preserved at 4 microcosm with whitefly nymphs and 19 pairs of parasitoids.parasitoids These were allowed to forage for 48 h andfrom were then removed the microcosm.microcosms After were promptly removing put back the into field natural cages. enemies, the fly nymphs preyed upon by detection; see below). predators were introduced into the microcosm andage allowed to for for- 48 h. Theserved female in 70% predators ethanol were (v:v) at then 4 recovered and pre- nymphs. This wasp numberdaily was rate of chosen oviposition of in accordance with the taneously released six female(19 predators females and 19 parasitoid pairs ual insects werehomogenised crushed with in a 2.0 Kontes pellet mL pestle microcentrifuge in 100 tubes and released 19 parasitoids pairs (19 females cosm containing whitefly nymphs. After introducing the wasps, we let them forage for 48 h,previous a treatment. After similar this time period to of time, thatremoved the for adult predators from wasps in were the the microcosm,developing and wasps after had 18–20 reached the days last (when larval the stage the counting of nymphsday preyed that upon was predators performed wereeach the plant extracted. were same For scrutinised under thisZeiss a count, de stereomicroscope all (DV4; Mexico Carl leavesments, SA of the de number of CV, emergeddays Mexico adult following the whiteflies City, whitefly was oviposition Mexico). recorded period,whitefly in 30 development For consideration time. of all treat-

1112 1113 T. E. ± punc- ), the . G. punc- E. eremi- Ee G However, punctipes nymphs, + As a result, and 20 ), the preda- 28 T. vaporariorum , nymphs preyed ( Gp Gp 27 Ee + ⇒ + nymphs and Tv Ee Tv under semi-field con- G. punctipes + T. vaporariorum ( Tv T. vaporariorum Gp ⇒ nymphs and adults. nymphs, T. vaporariorum ( E. eremicus Ee In contrast, in the treatment with wileyonlinelibrary.com/journal/ps SEM) of + Gp 50 , ± + Tv 49 Tv eremicus . 0.05). released consecutively); E adults emerged. Analysed treatments: control ( < ). Columns bearing different letters represent sig- For IGP specifically, it is known that the use P T. vaporariorum under semi-field conditions. (b) Mean percentage ( ( 47 , Some of the factors that could be related to these 46 Ee , 48 26 + – – nymphs only); G. punctipes E. eremicus 46 23 Gp (a) Mean percentage ( + and G. punctipes T. vaporariorum Tv exhibited IGP on ); released simultaneously); eremicus nymphs and nificant differences (at SEM) of vaporariorum cus tipes tipes upon by 4.1 Intraguild predationPreviously, assessment under laboratory conditions, we found that Figure 1. of plants, as opposed to bare artificialof arenas, leaves and can the modify pubescence the rate at which IGP occurs. the complexity of analysedof systems interactions can and influence particularlyfirst the interested outcome that in determining of whetherexhibited IGP. the Therefore, IGP predator on we G. the were parasitoid ditions. Our results showed thatin the IGP predator on the did parasitoid. incontained High wasp fact DNA percentages when engage the of two analysed natural enemies predators into were released a microcosmthe together treatment (89.7%) with or concomitant sequentially (90.7%). release In ( differential results includement experimental complexity (e.g. conditions climate, plant structure, or leaf properties,or light environ- season). sequential release of natural enemiestors ( were confronted withthe parasitised wasp nymphs DNA only. In detectedture this in parasitoids case, the developing predators in was the from host. these These imma- results are in line it was unknown whether IGPditions. occurred This under is more important complex because con- tory effects conditions observed will under not necessarily labora- takeconditions. place in field or semi-field predators remained with the adultthe wasp DNA wasps detected in for predators was 48 more likely h.adult obtained from wasps At than this from point, immature wasps.sitoid This egg is is because oviposited the externally para- the under invasion the of whitefly nymph the and hostparasitoid nymph larvae can hatching. take two or more days after G. G. on Gp Gp T. E. and + + = 0.001). Ee 18.574; Tv and Ee .Those Tv G. punc- < = + + Ee P E. eremicus Gp 4,48 + Gp F (Fig. 2b). + (Table 1). High : 89.7%) and in adults released Tv + G. punctipes Tv Ee Ee ; also engaging in engages in IGP on 27.328; : 90.7%). 0.001) (Fig. 2a). The + + Tv nymphs, = < and Gp T. vaporariorum Gp Gp P 2,28 ⇒ + + , molecular assessment Gp F Individuals in which DNA was detected (%) E. eremicus E. eremicus Ee Tv Tv + punctipes G. punctipes T. vaporariorum E. eremicus . + 39.585; G and Tv G. punctipes and Tv = T. vaporariorum , followed by the treatment Gp 2,28 = E. eremicus F Gp ⇒ Gp nymphs and on ⇒ Ee 0.001) (Fig. 1a). Unexpectedly, the highest 54 * 90.7 6358 38.1 55.2 89.7 ⇒ + G. punctipes Ee )(Fig.1a). a < : 1110–1116 © 2015 Society of Chemical Industry Ee under natural conditions (Table 1). However, P + Tv Gp Number of 72 + Tv ⇒ released consecutively. Tv analysed predators )andthesequentialintroductionofbothnatural nymphs, Ee and 2016; (Fig. 1b). 97.273; G. punctipes + Gp G. punctipes T. vaporariorum eremicus Ee = Molecular detection percentages of Gp Ee . Gp = engages in IGP on the wasp in was released alone (Fig. 1a). + E Tv + + ⇒ 2,28 ⇒ Gp , followed by Tv F Tv Gp Gp Ee G. punctipes + (Fig. 2a). A similar trend was found when the mean percent- was compared among treatments, we found significant differ- Ee Ee ), followed in descending order by the predator-only treat- + + + 0.001) (Fig. 1b). The treatments with the highest rate of Tv + + Ee Ee The mean percentage of parasitised nymphs was significantly vaporariorum simultaneously; a Treatment Tv Table 1. Tv Tv eremicus and *At this timewhitefly point, nymphs. predators were confronted only to parasitised < Tv different among treatments ( with the lowest rate of emerged flies were + age of emerged wasps was compared ( emerged flies were the control, Our results show that, under semi-field conditions,punctipes the predator percentages of predators containing waspin DNA the were concomitant found release both treatment ( number of preyed uponwhere nymphs both was natural enemies recorded were in concomitantly present the ( treatment highest number of parasitised nymphsments was recorded in the treat- P whitefly nymphs wasconcomitantly higher released when (i.e. both underpunctipes natural IGP conditions) enemies than were when Pest Manag Sci 4Our DISCUSSION results show that the predator although IGP occurred, the predation rate of the wasp 3.1 IGP of 3RESULTS the sequential release treatment ( Intraguild predation and its influence on whitefly control www.soci.org + The treatment with the highest percentage of emergedTv wasps was 3.2 Whitefly predation rate by enemies ( ment ( IGP When the mean percentage of nymphs preyed upon by tipes ences ( 3.3 Emergedemerged adult wasps whiteflies, parasitised nymphs and As for the mean percentage of emerged whiteflies, weicant found signif- differences when treatments were compared ( 32 Gp and et al. + ) rela- 54 – Ee Tv )resulted 52 treatment Pronkelisia + E. eremicus Movement : 1110–1116 (Hemiptera: Ee Gp 58 72 Gp 63 + , because some – ⇒ + 55 , Gp For example, IGP of 19 Ee 2016; ). Nevertheless, our Tv on adult + 31 + Gp – Tv exhibits a preference for Tyttus vagus 29 Tv + That is to say, we expected G. punctipes Tv 34 (Fig. 1a). This indicates that, in G. punctipes ) increase kills when prey density Pest Manag Sci ), we observed that the predator Gp Ee + G. punctipes The perception of wasps could then has been reported to be positively + These heterogeneous outcomes indi- Tv 34 33 was confronted with both options (adult Gp + G. punctipes Tv or as a response to competition represented by (Araneae: Lycosidae) on However, in other cases it has been documented 60 , G. punctipes 30 59 , Further experiments are required for a better assess- 36 G. punctipes , 34 62 , 61 treatment relative to Ee One final point, from the perspective of applied entomology, is spite of the consumption ofsome the reason parasitoids the predator (i.e. increases IGP) the (Table rate 1),relative of consumed for to nymphs conditions in whichreason it is is likely the lone relatedproximal natural to response enemy. of the That the perception predatorWasp of to presence the adult can detection wasps be ofor and revealed that movements. a through prey. Semiochemical semiochemical signals could signals by be wasps those while traces walking, left parasitising or feeding hosts, ment of the reason foroutcomes this on predator’s the prey–predator–parasitoid response and long-term the population potential dynamics. related to the rate of emergence ofthe adult lowest whiteflies. We rates found of that whitefly emergencewith were joint found release in of treatments naturalpest enemies control (Fig. with 1b). the This joint indicatesIGP release that occurrence) of is natural more enemies effectivesingle (in than spite natural that of enemy. with the Thisare release inducing suggests pest of that kills a additively. bothcomitant Indeed, when natural release we ( enemies analysed con- in the lowest rateof of pest whitefly emergence emergence was (Fig. obtained 1b). in A the similar rate exhibited a highersitoids, rate meanwhile, of nymph parasitisedtreatment, consumption fewer but, (Fig. 1a). regardless, nymphs joint Para- (Fig. 2a) action ( in that wasps. or remains unchanged. cate the variability ofon the pest control. influence In ofmodel, the interactions we specific expected such case that of as IGP our IGP of short-term biological would reduce nymph whitefly predation and consequentlyreduce would pest control efficacy. Thising hypothesis into account was the postulated fact that tak- mobile prey over non-mobile targets. Pardosa littoralis Miridae) resulted in an increase in theirplanthoppers. shared prey, the results showed that, contrary to oursumed expectations, the whitefly rate nymphs of con- was+ significantly higher in the that when wasps versus whitefly nymphs),wasps, it reducing would its preferably rate of attack predationquently, adult the on whitefly rates nymphs. of Conse- consumedin whitefly nymphs the would treatment be with lower concomitant release ( that, in spite of the presence of IGP, control of pests increases could be the other signal revealing the presencethe of wasps, because predator attracted to mobile prey. (Fig. 1b), in which the predatorbut the consumed wasps fewer parasitised nymphs more (Fig. nymphs 1a) (Fig.in 2a). line These with results other are studies thatthat have participate reported in that IGP natural act enemies additively in pest control. these signals can be detected by predators. trigger an increase in predation rate by predators (including increases on the pest and consequentlytrol. the efficacy Previous of literature biological reported pestcould con- that, result in in a reduction fact, in pest occurrence control. of IGP tive to that with the predator alone ( ); ± E. G. and T. vapo- released www.soci.org L Bao-Fundora nymphs and G. punctipes G. punctipes nymphs para- E. eremicus © 2015 Society of Chemical Industry E. eremicus also engaging in and If what is sought is the nymphs, nymphs and 51 T. vaporariorum ( T. vaporariorum Ee + G. punctipes G. punctipes Tv SEM) of 31 ± T. vaporariorum T. vaporariorum ( ( , our results suggest that an individual nymphs, Gp Gp could be much more successful than indi- + ⇒ Tv Ee under semi-field conditions. (b) Mean percentage ( + can prey upon adult and immature stages of E. eremicus adults emerged. Analysed treatments: control ( Tv E.eremicus T. vaporariorum 0.05). This could be relevant in terms of planned biological ( released consecutively); < and ). Columns bearing different letters represent significant differ- 20 (a) Mean percentage ( E. eremicus Ee . P nymphs only); E. eremicus + G. punctipes Gp + eremicus SEM) of rariorum Tv wileyonlinelibrary.com/journal/ps 4.2 Whitefly predation rate by with previous observations under laboratory conditions indicating that Figure 2. sitised by G. punctipes simultaneously); control programmes. For example, if a joint(concomitant release or were intended sequential), our(immature results or indicate adults) that would be parasitoids preyedrate upon and, of as a parasitism result, (Fig. a 2a)arise. low Therefore, and the wasp joint emergencecurrent release (Fig. or 2b) of sequential) would seems both not naturalthe to wasp) favour enemies an (at inoculative (con- least biological on controlreproduction the programme of where side natural the enemies of is sought. establishment of E. eremicus ences (at IGP The other important point wewhether analysed IGP occurrence in reduced the the predation rate present of study was release (without predators) would be morecontrast, favourable if (Fig. 2b). what is In planned isgoal inundative releases is (where the the control main of theof pest, natural without enemies), the the needpunctipes for concomitant reproduction or sequential releasevidual of releases (Fig. 1b). These resultsanalysing different point combinations to of the natural importancebined enemies of releases before are com- implemented, to optimise thebiological effectiveness of control a programme.

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