rizvi_et_al-2015-insect_science

Insect Science (2015) 00, 1–13, DOI 10.1111/1744-7917.12191

ORIGINAL ARTICLE

Oviposition preference and larval performance of Epiphyaspostvittana (Lepidoptera: Tortricidae) on Botrytis cinerea(Helotiales: Sclerotiniaceae) infected berries of Vitis vinifera(Vitales: Vitaceae)

Syed Z. M. Rizvi1,2, Anantanarayanan Raman1,2, Warwick M. Wheatley1 and Geoffrey Cook1

1School of Agricultural & Wine Sciences and 2Graham Centre for Agricultural Innovation, Charles Sturt University, Orange, NSW 2800,

Australia

Abstract In this paper we tested the behavior of gravid Epiphyas postvittana in select-ing the most-appropriate site for oviposition thus benefitting offspring performance. Ourhypothesis was built on Jaenike’s preference–performance hypothesis (also referred to asthe “mother-knows-the-best” hypothesis). To test this, we used the interacting Epiphyaspostvittana, its host Vitis vinifera, and the pathogenic microbe Botrytis cinerea system.Populations of E. postvittana and B. cinerea often exist concurrently on V. vinifera in Aus-tralasia and their interaction and mutual influence are currently being explored, althoughthe suggestion presently is that the relationship between E. postvittana and B. cinerea ismutualistic. We tested the effect of volatiles from B. cinerea-infected berries and unin-fected (control) berries of V. vinifera on the oviposition behavior of E. postvittana. Wealso characterized the effects of B. cinerea infection on the berries of V. vinifera on thegrowth and development of E. postvittana. Contrary to the preference–performance hy-pothesis, oviposition choices made by gravid E. postvittana did not result in the bestoffspring survival, development, and performance. The preference for oviposition byE. postvittana was strongly influenced by the olfactory and tactile cues. She laid fewer eggson B. cinerea-infected berries compared to uninfected berries of V. vinifera. The larvae ofE. postvittana showed no preference to uninfected berries of V. vinifera. The larvae fedon B. cinerea-infected berries of V. vinifera showing greater survival rate, shorter time topupation, greater pupal mass, and on becoming adults they laid more numbers of eggs thanthe larvae that were enabled to feed on uninfected berries. The larvae of E. postvittanatransport the conidia of B. cinerea and transmit grey-mould disease to uninfected berriesof V. vinifera.

Key words larval development; life-history performance; light-brown apple moth; ovipo-sition preference; preference–performance hypothesis; grapevine

Introduction

The link between host–plant preference and offspringperformance is central in insect–plant interaction stud-

Correspondence: Anantanarayanan Raman, Charles SturtUniversity, Orange, PO Box 883, NSW 2800, Australia.Tel: +61 02 6365 7833; email: [email protected]

ies (Thompson, 1988). The “decision” made on thesuitability of the host plant by a plant-feeding insect iscritical for its progeny (Gripenberg et al., 2010). Amongvarious plant-feeding insects, preadult mobile stageshave limited opportunities to explore newer food sites incase the oviposited sites were inappropriate. The gravidfemale, therefore, usually, selects a site that will servicethe nutritional needs of her offspring (Mayhew, 1997).

C© 2014 Institute of Zoology, Chinese Academy of Sciences1

2 S. Z. M. Rizvi et al.

The preference–performance hypothesis (also referred toas the “mother-knows-the-best” hypothesis) proposes thatoviposition preference should correspond with host suit-ability for offspring development; the adult females, thus,maximize the fitness of their offspring by ovipositing atthe most appropriate host sites (Jaenike, 1978). Energystored during preadult mobile (“larval” hereafter) stagesis utilized during nonfeeding pupal stages. The qualityof food consumed during larval stage also contributesto reproductive performance. Reproduction in severalplant-feeding taxa has been demonstrated to be closelylinked to feeding preferences during their larval stages(Awmack & Leather, 2002). For instance, oocyte pro-duction depends on the quality of food consumed duringlarval periods; bulk of nitrogen and carbon componentsof eggs is derived from the nutrients obtained duringlarval period (Boggs, 1997). Many mated females usuallyprefer either one or related few among diverse plants foroviposition. Nevertheless, that oviposition preference re-lates to offspring performance is currently being debated(Mayhew, 1997). For instance, a gravid female’s decisionin the choice of a plant could be based on reasons favoringher performance than that of her offspring (Valladares &Lawton, 1991; Mayhew, 1997). This selfish-motherhoodhypothesis has been reinforced by Scheirs and Bruyn(2002), and Scheirs et al. (2004). In such alternatescenarios, insects fail to make the seemingly optimalchoice and they oviposit on a plant, which will achievethe optimal growth and development of their offspring.

Among plant-feeding insects, chemical cues fromplants are vital for host selection. Female insects use dif-ferent sensory cues to locate and select the “most suitable”plant and the site for nourishment and/or oviposition (sev-eral examples cited in Schoonhoven et al., 2005; Bruceet al., 2010). Olfaction, contact chemoreception, and vi-sion play decisive roles in this process. From a dis-tance, in the specific instance of Epiphyas postvittana(Lepidoptera: Tortricidae) (Foster et al., 1997) and Lobe-sia botrana (Lepidoptera: Tortricidae) (Tasin et al., 2011),volatiles from the host enable insects to locate their hostsfor oviposition, but when at the correct host surface, con-tact cues influence their decision enabling them to eitherprogress with the oviposition or not (Rojas et al., 2003;Rizvi et al., 2014). Volatiles of host plants are influencedand modified by various factors, such as infection bymicrobes, which can alter host–plant quality. In the nat-ural environment and agricultural contexts, plants oftenencounter several organisms. Among these, insects andfungi concurrently attack plants, resulting in a three-wayinteraction among plants, plant-feeding arthropod, andplant-infecting microbe. In such 3-way interacting sys-tems, the fungi either influence the interaction between

the insect and the plant, or remain a mutualist or an antag-onist; occasionally these fungi can remain neutral as well(Hatcher, 1995; van Dam, 2009). The fungi, in such in-teracting systems, can induce multiple variations in plantchemistry (Cardoza et al., 2003b; Raman et al., 2012).Such variation in host quality alters volatile composition,which is recognized by plant-feeding insects by their ol-factory capacity, which, in turn, can change the preferencebehavior in insects (Najar-Rodriguez et al., 2010; Qawas-meh et al., 2012). The fungus-induced plant volatiles canact as either attractants or deterrents for plant-feedinginsects (Tack & Dicke, 2013; Qawasmeh et al., 2014).For example, Arachis hypogaea (Fabales: Fabaceae) wheninfected by Sclerotium rolfsii (Atheliales: Atheliaceae)releases specific terpenes, which act as attractants toSpodoptera exigua (Lepidoptera: Noctuidae) (Cardozaet al., 2002). Botrytis cinerea (Helotiales: Sclerotini-aceae), a necrotrophic pathogen degrades the host-plantcell-wall hydrocarbons and releases 3-methyl-1-butanol,which arises in plant tissues consequent to decay (Magan& Evans, 2000; Tasin et al., 2012). 3-methyl-1-butanol re-leased by Vitis vinifera (Vitales: Vitaceae) when infectedby B. cinerea deters oviposition by L. botrana (Tasin et al.,2012). On the other hand, fungal mycelia can be a sourceof nourishment for the lepidopteran larvae, enabling themto synthesize sterols and vitamins (Svoboda et al., 1994).

In Australian vineyards, the active adults of E. postvit-tana encounter B. cinerea during oviposition, whereastheir larvae cooccur with B. cinerea feeding on their hy-phae and spores (Bailey et al., 1996; Rizvi et al., 2014).Epiphyas postvittana is native to Australia, but its widehost range has enabled it to establish in New Zealand,England, Ireland, the Netherlands, and Sweden, and inHawaii and California of the United States of America(Wolschrijn & Kuchlein, 2006; Suckling & Brockerhoff,2010). Epiphyas postvittana has 3–4 generations a year.In Australia, spring (September to November) and sum-mer (December to February) generations of E. postvittanaoften coincide with berry production and nearly 65% ofE. postvittana larvae move to berries of V. vinifera inflict-ing intense productivity losses (Buchanan, 1977; Baileyet al., 1996).

Botrytis cinerea occurs worldwide and induces grey-mould disease on V. vinifera affecting leaves and fruits(Fournier et al., 2013). Botrytis cinerea–V. vinifera asso-ciation eventuates in the production of various volatiles,which have been shown to influence the ovipositionbehavior of E. postvittana (Rizvi et al., 2014) andL. botrana (Tasin et al., 2012). A mutualistic relationshipbetween L. botrana and B. cinerea has been shown: thelarvae of L. botrana benefit from B. cinerea because theirmycelia supply sterols such as ergosterol enabling the

C© 2014 Institute of Zoology, Chinese Academy of Sciences, 00, 1–13

Effect of B. cinerea on E. postvittana 3

metamorphosis of L. botrana, whereas L. botrana helpsB. cinerea dispersing its spores (Mondy & Corio-Costet,2000). Moreover, chewing of V. vinifera tissues by L. bo-trana larvae inflicts wounds facilitating the establishmentof the fungus (Fermaud & Lemenn, 1992).

Therefore, we propose that the gravid individuals ofE. postvittana recognize the volatiles from uninfected(control) and B. cinerea-infected berries of V. vinifera andchoose to oviposit at the most appropriate site enablingthe best performance of their offspring. This was testedby evaluating the relationship between ovipositionpreference and larval performance of E. postvittana onuninfected berries and infected berries of V. vinifera.In keeping with the above, we sought answers to thefollowing: (i) Do the females of E. postvittana prefer tooviposit on berries of V. vinifera infected by B. cinerea?(ii) Do the larvae of E. postvittana prefer to feed onberries of V. vinifera infected by B. cinerea? (iii) Dothe B. cinerea-infected berries affect the survival andlife-history performance of E. postvittana larvae?

Materials and methods

Insect culture

Fertile eggs of E. postvittana were obtained from de-termined stocks of E. postvittana maintained at CharlesSturt University, Orange Campus (CSU—O). The cultureswere maintained on a Phaseolus lunatus-based semisyn-thetic diet (Cunningham, 2007). The larvae were rearedin plastic boxes (35 cm × 20 cm × 4 cm) filled to abouta third with the synthetic diet and maintained at 21 ±1 °C, 60%–80% RH, and 16 L : 8 D regimen. On pu-pation, the insects were sexed and segregated consid-ering total-body length and numbers of abdominal seg-ments. A 24-h-old adult female was paired with a similaraged adult male in a corrugated-walled Dixie cup. Thesepairs were fed on cotton balls soaked in 10% aqueous-honey and 0.1% sorbic acid. Oviposition occurred on thewalls of cups, which were later cut into rafts bearing eggmasses, which consisted of eggs varying from 3 to 95.Some rafts were stored at 4–6 °C for future use, andthe remaining was used to raise adults. For all bioassaysin this study, a 24-h-old female was placed with sameage male for 24 h for mating and only those femaleswhich laid 5–10 eggs were used for oviposition bioassays.Adult males and females were not exposed to either unin-fected or B. cinerea-infected berries of V. vinifera, prior toexperimentation.

Fungus culture and preparation of conidial suspension

The fungus isolated from infected berries of V. viniferacv. Chardonnay from the CSU—O’s Chardonnay vine-yard in February 2013 were cultured on potato–dextroseagar (PDA) (Fisher Scientific, Inc., Scoresby, Victoria,Australia) at 22 °C and 12 L : 12 D in a horizontal lam-inar airflow (HWS120, Clyde–Apac, Sydney, Australia).Michael Priest (Mycologist–Plant Pathologist, NSW De-partment of Primary Industries, Orange, NSW, Australia)confirmed the cultured material as B. cinerea. The PDAcultures of B. cinerea bearing ca. 15-d-old conidia weregently rinsed in 5–10 mL of sterile water + Tween 80(0.01%) solution (Acros Organics, Geel, Belgium). Thedensity of the conidial suspension was adjusted to 106

conidia/mL. This conidial suspension was used for in-fecting berries of V. vinifera, in the laboratory, followingRizvi et al. (2014).

Infection of B. cinerea on V. vinifera berries

Berries of V. vinifera var. Chardonnay (hereafter,V. vinifera) of phenological stage 85 (Lorenz et al., 1994)were collected from CSU—O Chardonnay vineyard.Berries of V. vinifera were surface sterilized with 1%sodium hypochlorite (NaClO) solution for 5 min andwashed with sterile water (3×). Using a sterile scalpel,4 scars were scratched on the skins of each berry andwere sprayed immediately with the prepared conidialsuspension of B. cinerea in the horizontal-laminar airflowsystem. Uninfected berries were sprayed with sterilewater. The infected and the uninfected berries wereplaced in a zip-lock plastic bag (35 cm × 40 cm) andincubated at 22 °C and 12 L : 12 D. After 9–11 d, theberries that manifested infection symptoms were used indifferent bioassays. Following Mondy et al. (1998) andTasin et al. (2012), we used berries with visually evidentgrey-mould sporulation in the behavioral bioassays. Theberry clusters with varying numbers of berries wereused in the experiments, but were standardized by usingclusters of nearly the same mass (90 ± 8 g).

Oviposition behavior

Two-choice experiment The experiments wereconducted in glass devices assembled suiting the require-ments, using Pyrex glassware, at CSU—O research labo-ratory at 21 ± 1 °C, 60%–70% RH, and 16 L : 8 D (Rizviet al., 2014). The assembled glass device consisted of



Fig. 1 Custom-made glass device for the 2-choice experi-ment of adults of Epiphyas postvittana (not to scale). am, alu-minum mesh; gj, glass jar; hgt, horizontal-glass tube; ib, infectedberries; m, moth; pe, port of entry; ps, Parafilm seal; ub, unin-fected berries.

2 wide-mouth glass jars (10-cm Ø, 18-cm high) connectedto each other by a glass tube (3-cm Ø, 30-cm long).Each jar was lined with aluminum mesh screen (Fig. 1).The mouths of the jars were also covered with the samealuminum mesh screen and were further wrapped withParafilm, enabled with a hole to receive one end ofthe glass tube. The aluminum screen was necessary todistract females from ovipositing on the wall of the jar.This precaution was imperative because smooth-texturedsurfaces, similar to glass, stimulate oviposition byE. postvittana (Foster et al., 1997). Aluminum mesh hasbeen used in similar studies (Rojas & Cruz-Lopez, 2003)testing the oviposition behavior of Spodoptera frugiperda(Lepidoptera: Noctuidae), Mondy et al. (1998) usedlatticed cages while testing the oviposition behavior ofL. botrana. We used the same material in both jars thatincluded uninfected and B. cinerea-infected berries tominimize the effect of mesh in each treatment. Parafilm,an established odorless thermoplastic filmy material (Yoo& Nam, 2012), was used to prevent the interference ofany external volatiles. Clusters of uninfected and infectedberries (prepared for the experiment as described in thepreceding section) were placed at the bottom of the twowide-mouth jars. At the mid-point of the glass tube, acircular (2.0-cm Ø) port was cut for introducing gravidE. postvittana enabling them to choose either infected oruninfected berries. Five live adult females were gatheredin a clean glass test tube (2.0-cm Ø, 15-cm long).The diameter of this test tube was the same as that ofthe port in the horizontal glass tube. The port was set toface downwards. The test tube including the adult mothswas held tight to the port. By virtue of their vertical-climbing behavior, the adult moths crawled one afteranother into the horizontal tube, each taking about 2 minto achieve this task. The movement of moths from the ver-tical tube into the horizontal tube was individualistic andthey did not influence the other in any obvious manner. Inother words, ca. 2 min was adequate for each moth to crawlone after the other from the vertical tube into the horizon-

Fig. 2 Custom-made glass device used in the “no-choiceexperiment—rate of oviposition of Epiphyas postvittana” (not toscale). am, aluminum mesh; b, beaker; gj, glass jar; ib, infectedberries; m, moth; ps, Parafilm seal; ub, uninfected berries.

tal tube. By the time, the next one followed into the hori-zontal tube, the earlier crawled moth had adequate time tomake its choice of moving towards one of the “baits” (in-fected and uninfected berries) located at either end of thehorizontal tube. The port was sealed using Parafilm. After72 h, the introduced females were removed carefully fromthe jars. Choices made by the females were recorded bycounting the numbers of moths in each jar; the numbersof eggs laid on the infected and uninfected berries werecounted under a stereobinocular microscope (S–20,AIS Australian Instrument Services, Croydon, Victoria,Australia). This experiment was repeated 8 times usingfreshly assembled wide-mouth glass jars and the hori-zontal glass tube. In each replication, the infected anduninfected berries used as baits were randomly allocatedto the two jars.

No-choice experiment—rate of oviposition A no-choice experiment was done to determine the rate ofoviposition on infected and uninfected berries of V.vinifera, using glass jars (1000 mL). Clusters of infectedand uninfected berries of similar mass were hung in twoidentical jars from the aluminum mesh used to cover themouth of each jar, followed by a Parafilm wrapping. Agravid E. postvittana was introduced into the jar and themouth of jar was covered (Fig. 2). Each treatment wasrepeated 8 times. After 72 h, the moths introduced intothe jars were removed and the numbers of eggs laid onthe berries were counted, as described in the precedingparagraph.

No-choice experiment—effect of volatiles on oviposi-tion The rate of oviposition of E. postvittana in responseto the volatiles emitted from the infected and uninfected



Fig. 3 Custom-made device to test the effect of volatiles onoviposition behavior of Epiphyas postvittana (not to scale). b,beaker; d, Dixie cup; ib, infected berries; ub, uninfected berries;m, moth; pps, pierced Parafilm seal; ps, Parafilm seal.

berries was assayed following Rizvi et al. (2014). Briefly,the bottom of the corrugated wall Dixie cup (200 mL) wascut; the open end was wrapped with and pierced 30 timesusing a pin, enabling the movement of volatiles into thecup. This cup was then seated on a 250-mL beaker, whichcontained either a cluster of uninfected or B. cinerea-infected berries of V. vinifera of similar mass. The junc-tion point of the beaker with the Dixie cup was sealedwith Parafilm (Fig. 3). A 24-h-old mated E. postvittanafemale was introduced into the Dixie cup and the free endof cup was covered with Parafilm. After 72 h, the mothswere removed and eggs deposited on the wall of the cupcounted. Each treatment was replicated 10 times.

Olfactory response of adults of E. postvittana Theolfactory response of adult males of E. postvittana (24–48 h old) to B. cinerea-infected and uninfected berriesof V. vinifera were measured using a Y-tube olfactometer(OLFM–YT–2425F, Analytical Research Systems,Gainsville, Florida, USA) that has a stem (2.5-cm Ø, 15-cm long) and forked arms (each 2.5-cm Ø, 7.5-cm long)connected to 2 tubular glass containers by Teflon R© tubes(0.2-cm Ø, 25-cm long). Two clusters of volatile sources,namely, B. cinerea-infected and uninfected berries ofV. vinifera of similar mass were placed, one in each of thesource containers. Compressed air (flow rate 400 mL/min)was pumped into the source containers via the tube inlets(Fig. 4). Male moths were introduced individually throughthe downwind end of the Y-tube and their behavior wasobserved for 15 min. Moths that remained at the end of thestem of the Y-tube for 30 min were deemed unresponsiveand excluded from the tests. Females of E. postvittana

Fig. 4 Y-tube experiment to determine olfactory response ofadult E. postvittana (not to scale). ap, air pump; ib, infectedberries; ub, uninfected berries; m, moth; tp, Teflon plug; st,source tube; tt, Teflon tube; yt, Y tube.

Fig. 5 Custom-made glass device for the 2-choice experimentof larvae of Epiphyas postvittana (not to scale). hgt, horizontal-glass tube; ib, infected berries; ub, uninfected berries; pe, portof entry; ps, Parafilm seal.

have been shown to be less responsive and active than themales (Danthanarayana, 1976; Gu & Danthanarayana,1990). In the pilot trials made using the Y-tube (n =10), adult females showed no response in the nominated15-min time frame, and therefore they were excludedfrom Y-tube olfactometer trial.

Larval behavior

Two-choice experiment The preference of neonatelarvae (<2 h) of E. postvittana toward B. cinerea-infectedand uninfected berries was tested. Ten control and 10 B.cinerea-infected berries were inserted individually at eachend of the glass tube (3-cm Ø, 30-cm long) under “still-air” condition. The average distance of the berries fromthe center was 10 cm. Ten neonate larvae were introducedinside the tube through the circular port, which was im-mediately sealed with Parafilm (Fig. 5) and incubated at21 ± 1 °C, 60%–70% RH, and 16 L : 8 D. After 24 h,the position of the larvae was noted. This experiment wasrepeated 10 times.



Fig. 6 Petri dish test for the larval preference towards unin-fected and B. cinerea-infected berries of V. vinifera (not to scale).dfp, damp filter paper; ib, infected berries; l, larvae; pd, Petridish; ub, uninfected berries.

Larval behavior toward B. cinerea-infected and unin-fected berries of V. vinifera was further verified throughanother experiment. A Petri dish (90-mm Ø) was linedwith damp-filter paper. One B. cinerea-infected and 1 un-infected berry of V. vinifera were placed at the two oppositepoints, 5-mm away from the wall of Petri dish (Fig. 6).A neonate E. postvittana larva was placed at the centerof the Petri dish, the lid placed on top, and sealed withParafilm. After 24 h, the position of the larva was checkedin the Petri dish. This experiment was repeated 100 times.

Transmission of conidia of B. cinerea Transmissionof conidia from infected to uninfected berries of V. viniferawas evaluated. Thirty individuals of 4th-instar larvae of E.postvittana that were raised on the semisynthetic diet (seeSection “Insect culture”) ensuring that they were 100%clean, totally devoid of B. cinerea were fed on uninfectedor B. cinerea-infected berries of V. vinifera for 48 h. Eachlarva was then transferred using a sterile camel-hair brushonto a surface-sterilized berry in a Petri dish, under thesterile conditions of the horizontal-laminar airflow. Thelarvae were enabled to feed for 48 h on surface-sterilizedberries. The larvae were removed from the berries andthe berries were incubated individually in sterile Petridishes sealed with Parafilm and incubated at 21 °C for7 d. The number of berries with visible levels of B.cinerea-infection was recorded. Visible levels of infectionon berries were determined under the stereobinocular mi-croscope using sporulation of B. cinerea on the berries asa trait (Khazaeli et al., 2010).

Larval development This experiment was done to de-termine the effect of B. cinerea-infected berries on the life-history performance of E. postvittana. Botrytis cinerea-infected (9–11 d) and uninfected berries were placed onseparate Petri dishes. One <2-h-old larva was released oneach Petri dish and allowed to develop until pupation at

21 ± 1 °C, 60%–70% RH, and 16 L : 8 D. Every 7 d, thedehydrating berries in the Petri dishes were changed andfrass removed. Survival of the larvae was also checked.One hundred larvae were used in each treatment. The lar-vae were allowed to pupate. The dates of pupation, num-ber of pupae, and pupal mass were recorded. Becauseprecise measurements of the mass of active adults weredifficult to obtain, the mass of the pupa was used as anindicator of adult-body mass. Each pupa was isolated to astopper glass vial (2-cm Ø, 4-cm long) until emergence.Adult emergence and adult-sex ratio in percentage wererecorded. The adults were sexed and paired in a corrugate-walled Dixie cup enabling mating and oviposition. Theadults that were enabled to oviposit were subsequentlymeasured for their performance: fecundity rate, possibledelays in oviposition (measured in days), fertility (mea-sured as the number of emerged larvae; the eggs wereincubated for 15 d at 21 ± 1 °C, 60%–70% RH, and16 L : 8 D enabling larval emergence) and percentageof ovipositing females. Number of days from the date ofemergence of adults from the pupal stage to death was alsorecorded.

Statistical analysis

In the oviposition bioassay, the numbers of eggs laidon B. cinerea-infected and uninfected berries in the 2-choice experiment were analyzed using paired sample “t”test. Independent sample “t” test was applied to measurethe significant difference in the number of eggs laid onB. cinerea-infected and uninfected berries in the no-choiceexperiment and the experiments measuring the effect ofvolatiles. Data from the Y-tube olfactometer, choice of thefemale moths for B. cinerea-infected or control berries inoviposition bioassay and choice of larvae for B. cinerea-infected or control berries in larval bioassay were analyzedapplying χ2 test. Transmission of conidia from B. cinerea-infected berries to uninfected berries was analyzed by con-tingency table (χ2 test). Nonlinear regression was appliedto discriminate the significant difference in the mortalityrate of larvae between B. cinerea-infected and uninfectedberries of V. vinifera using the equation Y = A + B(Rx ),where x is the time (in days), y is mortality and A, B, andR (rate of curvature) are estimated parameters. A contin-gency table (χ2 test) was used to analyze female sex ratio,percentage of pupation, percentage of adult emergenceand percentage of egg-laying females whereas indepen-dent sample t-test was used in all other life-history traits(Tables 1–3). Analyses were conducted with SPSS statistic17.0 (2007) and GenStat (VSN International 2012) (Hert-fordshire, UK). Graphs were generated in MS Excel 2013.



Table 1 Larval developmental time, pupal duration and adult life span (mean ± SE) (sample size) of E. postvittana reared on B.cinerea-infected or uninfected berries of V. vinifera.

Larval developmental time (days) Pupal duration (days) Adult life span (days)Treatment

Male Female Male Female Male Female

Uninfectedberries

33.4 ± 0.6 (27) 41.2 ± 0.9 (24) 10.2 ± 0.2 (25) 10.4 ± 0.9 (19) 16.9 ± 0.7 (25) 15.6 ± 0.9 (19)

B. cinerea-infectedberries

27.9 ± 0.5 (36) 33.4 ± 0.8 (33) 9.7 ± 0.1 (35) 9.8 ± 0.11 (30) 17.2 ± 0.7 (35) 14.8 ± 0.7 (30)

Statistic(df) t = 6.6(61) t = 5.9(55) t = 1.7(58) t = 1.7(47) t = 0.7(58) t = 1.2(47)

P <0.001 <0.001 0.09 0.10 0.50 0.23

t, independent sample t-test.

Table 2 Pupal mass(mean ± SE) (sample size), percentage of larvae surviving from hating to pupae, percentage of larvae survivingfrom hating to adult, and female sex ratio of E. postvittana reared on B. cinerea-infected or uninfected berries of V. vinifera.

% surviving from % surviving from Female sexhatching to pupa hatching to adult ratio (%)

Pupal mass (mg)Treatment

Male Female

Uninfected berries 17.5 ± 0.5 (27) 23.1 ± 0.7 (24) 51 44 43.1B. cinerea-infected berries 21.4 ± 0.8 (36) 30.4 ± 1.6 (33) 69 65 45.9Statistic(df) t = 3.9(61) t = 6.0(55) χ 2 = 7.81 χ 2 = 8.9 χ 2 = 0.07P <0.001 <0.001 0.005 0.003 0.79

t, independent sample t-test; χ 2, contingency table (χ 2).

Table 3 Adult performance (mean ± SE) (sample size) of E. postvittana reared on B. cinerea-infected and uninfected berries ofV. vinifera.

Egg-laying Delay in egg No. of eggs per No. of larvaeTreatment

females (%) laying (days) female (days) emerged per female (days)

Uninfected berries 88 2.2 ± 0.1 (15) 246.1 ± 25.7 (15) 183.2 ± 27.9 (15)B. cinerea-infected berries 94 2.3 ± 0.2 (22) 326.8 ± 19.5 (22) 255.6 ± 18.1 (22)Statistic(df) χ 2 = 0.3 t = 0.175(35) t = 2.5(35) t = 2.3(35)

P 0.58 0.86 0.01 0.02

t, independent sample t-test; χ 2, contingency table (χ 2).

Results

Oviposition behavior

Two-choice experiment Gravid E. postvittana signif-icantly chose uninfected berries (70%) compared with B.cinerea-infected berries (30%, n = 40, χ2 = 6.40, P =0.011). Gravid E. postvittana laid significantly more num-ber of eggs on uninfected berries of V. vinifera than on B.cinerea-infected berries (uninfected vs. infected: 114 ±10.06 vs. 18 ± 2.7 [mean ± SE], df = 7, t = 9.13, P <

0.001, Fig. 7A).

No-choice experiment—rate of oviposition GravidE. postvittana laid significantly more number of eggson uninfected berries compared with B. cinerea-infectedberries of V. vinifera (uninfected vs. infected, 58 ± 7 vs.9 ± 1.5 [mean ± SE], df = 14, t = 8.51, P < 0.001,Fig. 7B).

No-choice experiment—effect of volatiles on ovipo-sition Gravid E. postvittana laid significantly more num-ber of eggs on the wall of the Dixie cup in the ambience ofvolatiles emitted from uninfected berries, compared withB. cinerea-infected berries of V. vinifera (uninfected vs.



Fig. 7 Mean number of eggs laid by E. postvittana in (A) 2-choice experiment, (B) no-choice experiment—rate of oviposition, (C)no-choice experiment—effect of volatiles on oviposition in response to uninfected ( ) and B. cinerea-infected ( � ) berries ofV. vinifera. Error bars denote SEM. **P < 0.01, ***P < 0.001.

infected, 347 ± 29 vs. 220 ± 30 [mean ± SE], df = 18,t = 3.03, P = 0.007, Fig. 7C).

Olfactory response of adults of E. postvittana Adult-male moths responded positively and significantly to thevolatiles from uninfected (control) berries compared withB. cinerea-infected berries (uninfected vs. infected, 70%vs. 30%, n = 40, χ2 = 6.4, P = 0.01). Female moths(n = 10) remained in the Y-tube stem and did not re-spond to volatiles from uninfected or B. cinerea-infectedberries.

Larval behavior

Two-choice experiment In glass tube experiment, theneonate larvae of E. postvittana (n = 100) moved to-wards uninfected and B. cinerea-infected berries (un-infected vs. infected, 43% vs. 57%, χ2 = 1.96,P = 0.161).

In Petri dish experiment, the neonate larvae of E.postvittana (n = 100) moved toward uninfected (control)berries and B. cinerea-infected berries (control vs. unin-fected, 55% vs. 45%, χ2 = 1, P = 0.317).

Transmission of conidia of B. cinerea The uninfectedberries, when fed upon by the larvae which were previ-ously fed on infected berries, manifested the grey-moulddisease (86.6%). On the contrary, those uninfected berrieswhen fed upon by the larvae which were previously fed onuninfected berries manifested the grey-mould disease ata low percentage (6.6%, n = 30, χ2 = 16.1, P < 0.001);even this low percentage of disease manifestation couldhave been possibly due to contamination.

Fig. 8 Mortality rate of larvae reared on B. cinerea-infected( � ) or uninfected ( ) berries of V. vinifera.

Larval development The larvae reared on B. cinerea-infected berries developed quicker (male P < 0.001;female P < 0.001) than the larvae raised on uninfectedberries of V. vinifera (Table 1). The mortality rate of larvaefed on uninfected berries (y = 48.91 − 49.18 × 0.89x)was significantly greater (P < 0.001) than those rearedon B. cinerea-infected berries of V. vinifera (y = 29.63− 29.45 × 0.85x, where x = day and y = mortality rate)(Fig. 8). Pupal mass of males and females of E. postvit-tana raised on B. cinerea-infected berries of V. viniferawere significantly greater (male P < 0.0001; female P< 0.001) than those of the larvae that were reared onuninfected berries (Table 2). Rate of pupation and adultemergence of larvae raised on B. cinerea-infected berries



were significantly higher (pupation P = 0.005; adultemergence P = 0.003) compared with those reared on un-infected berries. Botrytis cinerea infection did not affectthe sex ratio of adults, percentage of the gravid females,and the length of preoviposition period (Tables 2 and3). Botrytis cinerea-infected diet significantly increasedthe fecundity rates (P = 0.01) and larval emergence(P = 0.02) compared with control diet (Table 3).

Discussion

Gravid E. postvittana prefer to oviposit on uninfectedberries relative to B. cinerea-infected berries of V. vinifera.The larvae of E. postvittana show no significant prefer-ence for uninfected berries; they transmit the conidia ofB. cinerea to berries in the vicinity. The insects survivebetter, develop faster, attain a heavier pupal mass, andlay more numbers of eggs when reared on B. cinerea-infected berries than those reared on uninfected berries ofV. vinifera.

Females of E. postvittana are deterred from ovipositingon B. cinerea-infected berries of V. vinifera

Several factors affect host selection in generalist plant-feeding insects for feeding and oviposition. Among suchinsects, the preference for certain hosts, the preference tolay eggs on plants, and the numbers of eggs laid at specificlocations are essentially driven by an assessment of cuesfrom the host using visual, olfactory, and tactile stimuli.Botrytis cinerea-infected berries of V. vinifera evokedavoidance behavior in the gravid E. postvittana deterringoviposition. Fungi induce changes in the volatile profilesin plant systems, which in turn alter the behavior of theLepidoptera that interact with a fungus–plant system(Mondy et al., 1998; Cardoza et al., 2003b). In thethree-way interacting system involving Hadena bicruris(Lepidoptera: Noctuidae), Silene latifolia (Caryophyl-laceae), and Microbotryum violaceum (Microbotryales:Microbotryaceae) variations in the quantity of volatilecompounds produced in S. latifolia have been shown toalter the behavior of H. bicruris (Dotterl et al., 2009).On the other hand, in the three-way interacting systeminvolving L. botrana, V. vinifera, and B. cinerea, variationsin the quality of volatile compounds produced have beenshown to alter the behavior of L. botrana, in additionto variations in quantities of volatiles produced (Tasinet al., 2011). In the E. postvittana–V. vinifera–B. cinereasystem, B. cinerea is a necrotrophic mycobiont, which iscapable of killing V. vinifera in conducive environments(Fournier et al., 2013). During infection, B. cinerea

hyphae penetrate V. vinifera berry epidermis and degradethe carbohydrates such as pectin and cellulose andliberate hydrocarbons (Magya & Bene, 2006), which,in turn, transform and release behavior-modifying com-pounds such as 3-methyl-1-butanol and ethanol (Carlileet al., 2001; Jansen et al., 2009; Tasin et al., 2012). Forexample, gravid females of L. botrana were deterred fromovipositing in the presence of three-methyl-1-butanolreleased from B. cinerea-infected berries (Tasin et al.,2012). Such physiological changes and the consequentrelease of volatiles form B. cinerea-infected berries, inour study, may responsible for the deterrence behavior ingravid E. postvittana. Odours from the berries infectedwith B. cinerea also deterred the males, which couldinfluence the mating behavior, since the males use plantvolatiles to distinguish environments where the likelihoodof finding the females is higher (Ansebo et al., 2004).

Tactile stimuli play a key role in the choice of host foregg laying by plant-feeding insects (Rojas et al., 2003).That oviposition by E. postvittana is influenced by tactilecues has been shown by Foster & Howard (1999). Surfacetexture plays a role in the oviposition behavior of gravidE. postvittana, which prefers to lay eggs on smoothsurfaces of varicose texture, rather than on rough andhairy surfaces such as the abaxial sides of the leaves ofV. vinifera (Rizvi et al., 2014). This corroborates with thepattern of oviposition in E. postvittana noted in natural en-vironments on the leaves of V. vinifera (Danthanarayana,1975) and Malus domestica (Rosaceae) (Tomkins et al.,1991). The fungal mycelia growing on the surfaces of ei-ther leaves or berries of V. vinifera mimic hairiness, andpossibly that acts as a physical barrier in the preferenceof E. postvittana during oviposition (Rizvi et al., 2014).This explains why so few eggs of E. postvittana occur onthe berries of V. vinifera infected by B. cinerea as com-pared with the numbers of eggs laid on the corrugatedwalls of Dixie cups in the ambience of volatiles from B.cinerea-infected berries.

The larvae of E. postvittana show no significantpreference to B. cinerea-infected berries of V. vinifera

Botrytis cinerea-infected berries influence the behav-ior of E. postvittana developmental stages variously.The larvae of E. postvittana, unlike the adults, showno significant attraction to uninfected berries. These re-sults also match with our earlier findings (Rizvi et al.,2014), wherein we reported discordance in ovipositionbehavior versus larval-feeding behavior in E. postvit-tana, when tested on uninfected and B. cinerea-infectedleaves of V. vinifera. The larvae of E. postvittana do not



necessarily follow the choice made by their mother andmove to other sites on V. vinifera (Harris et al., 1997;Foster & Howard, 1999). Here, we cannot disregard thesuggestion made by Scheirs and De Bruyn (2002) thatoviposition occurs consequent to attraction of food sourceto adults. Adult plant-feeding insects often prefer to feedand oviposit on such sites, which favor their long-termfitness and in consequence, make poor choices for theirprogeny.

Botrytis cinerea-infected berries of V. vinifera affect thesurvival and life-history performance of E. postvittanalarvae

We aimed at verifying the preference–performance hy-pothesis (Jaenike, 1978) that plant-feeding insects suchas E. postvittana have evolved to choose the right hostfor oviposition that will enable the best performanceof the offspring. According to Jaenike, the oviposition-preference should match with host suitability for offspringdevelopment. Among polyphagous plant-feeding insects,mated females often exhibit a preference for ovipositionamong different host plants, the oviposition preferenceusually synchronizes with the best performance of off-spring, although evidences negating Jaenike (1978) alsoexist (Larsson & Ekbom, 1995; Mayhew, 1997; Leyvaet al., 2000; Gripenberg et al., 2010). The choice oflarvae for food may substantially differ from the adultsparticularly when the larvae and adults feed on differ-ent parts of a plant (Mayhew, 1997), for example, inE. postvittana. A poor relationship between preferenceof adults for oviposition and preference of larvae forfeeding by E. postvittana using V. vinifera and severalother plants without the involvement of B. cinerea hasbeen shown (Foster & Howard, 1999): gravid femalesof E. postvittana oviposited indiscriminately on host andnonhost plants; in contrast, the larvae of E. postvittanashowed a greater level of preference to V. vinifera than toother nonhost plants tested. The present work testing thepreference behavior of E. postvittana in the presence ofB. cinerea on V. vinifera during oviposition reinforces Fos-ter and Howard’s (1999) findings that gravid adults ofE. postvittana do not follow the preference–performancehypothesis. Among plant-feeding insects, optimal forag-ing and optimal oviposition are not independent; but opti-mal foraging influences host selection more than optimaloviposition in effect (Scheirs et al., 2004). This selfish-motherhood hypothesis was tested by Scheirs et al. (2000)who suggested that variation in the adult preference ishighly correlated with adult performance rather than withoffspring performance in host plant selection. Whether the

poor relationship between oviposition preference and theoffspring performance is due to this selfish-motherhoodbehavior of adult E. postvittana remain unknown. It thusappears that additional studies are needed to elucidatethe role of food sources on both the long-term fitness ofegg-laying females and the oviposition response in thepresence of these resources.

According to Yang et al. (2013) avoidance of fungus-infected tissue by gravid insects during oviposition couldbe an adaptive strategy for the fitness of the offspring.Biere & Tack (2013) also suggest a similar outcome thatthe level of fungal infection can influence the oviposi-tion preference of insects. In a specific context, Tasinet al. (2012) showed that L. botrana displayed significantlevel of deterrence of the 7–9-d-old B. cinerea-infectedV. vinifera berries, whereas no significant inhibition oc-curred when 1–3-d-old infected berries were supplied tothe gravid adults of L. botrana. On the other hand, thefungus associated with the plant could also facilitate thenutrition of the insect, either by breaking complex ma-terials into simpler forms or by decreasing the level ofdefense compounds in the plant (Cardoza et al. 2003a,b).In the present study, since we have used 9–11-d-old B.cinerea-infected berries of V. vinifera, it would be appro-priate to suggest that the difference between the time ofoviposition and that of egg hatch potentially enhancesthe level of infection of V. vinifera berries by B. cinerea.Therefore, the larval food quality could have potentiallydeteriorated with accelerated level of infection (Tasinet al., 2012). This possibly explains why gravid adultsavoid infected berries for oviposition.

Our results point to a mutualistic relationship betweenthe larvae of E. postvittana and B. cinerea. Although,adults of E. postvittana do not favor this relationship anddo not prefer to oviposit on B. cinerea-infected berries, theselection behavior of V. vinifera by the larvae differs fromthat of adults, either because they have different host re-quirements or because they feed on different plant organs.The larvae of E. postvittana vector the conidia trappedamong hairs on their body surfaces, in gut and faeces,and spread the conidia among susceptible berries (Baileyet al., 1997; Rizvi et al., 2014). In the present study, weshow that feeding on B. cinerea-infected berries of V.vinifera induce multiple physiological changes in the E.postvittana, such as an increase in fecundity, the emer-gence rate of larvae, a decrease in the total duration ofdevelopment and mortality. Larval diet plays an importantrole in determining the size and fecundity of most insects(Svoboda et al., 1994) and the Lepidoptera in particular(Mondy et al., 1998), because the energy required foroviposition and egg development is mainly derived fromreserves accumulated during their larval stages. Under



such a circumstance, the fungi possibly act as a source ofnutrition and food supplement to the larvae of E. postvit-tana. Mutualistic relationship between an insect and afungus is common among different insects (Svobodaet al., 1994; Mondy & Corio-Costet, 2000). Inability ofinsects to synthesize sterols constrains them to depend onexogenous sources such as plants and/or their symbionts.Working on the larvae of L. botrana Mondy et al. (1998)found that L. botrana larvae are mutualistically related toB. cinerea on V. vinifera for sterol source from the fungus.Based on this study, we propose that the relationship of E.postvittana with B. cinerea infected V. vinifera is driven bymutualism.

Conclusion

In this study, we show that the gravid females ofE. postvittana avoid and do not prefer to oviposit onB. cinerea-infected berries while the rate of ovipo-sition is significantly decreased in the ambiance ofvolatiles from B. cinerea-infected berries. The lar-vae of E. postvittana showed no preference for unin-fected berries. Larvae vector the conidia of B. cinereaand infect the healthy berries. Furthermore, the larvaewhich fed on B. cinerea-infected berries survived bet-ter, developed faster, attained a heavier pupal mass,and laid more eggs than those reared on uninfectedberries of V. vinifera. Gravid E. postvittana recognizethe volatiles arising from uninfected and B. cinerea-infected berries of V. vinifera but choose to oviposit atsites which need not lead to the best performance of theiroffspring.

Acknowledgments

We are grateful to Gadi V. P. Reddy and Brian Thompson(Western Ag Research Center, Montana State University,Conrad, Montana, USA) and Fazila Yousuf and AnamikaSharma (Charles Sturt University, Orange, NSW,Australia) for their insightful remarks on the draftmanuscript. We thank Helen Nicol for her advice onstatistical analysis.

Disclosure

All the authors of this manuscript declare that none ofthem has any conflict of interest. The manuscript is orig-inal and does not infringe any copyright issue.

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Accepted October 17, 2014


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