POPULATION ECOLOGY

Wind-Borne Dispersal of a Parasitoid: the Process, the Model, andits Validation

NADIAH P. KRISTENSEN,1,2 NANCY A. SCHELLHORN,1 ANDREW D. HULTHEN,1

LYNITA J. HOWIE,1 AND PAUL J. DE BARRO1

Environ. Entomol. 42(6): 1137Ð1148 (2013); DOI: http://dx.doi.org/10.1603/EN12243

ABSTRACT The aphelinid parasitoid Eretmocerus hayati Zolnerowich & Rose (Hymenoptera:Aphelinidae) was recently released in Australia as a biocontrol agent against the crop pest Bemisiatabaci Gennadius (Hemiptera: Aleyrodidae). It was found that the parasitoid can spread over severalkilometers ina singlegenerationandcontinue layingeggs forovera fortnight.A simplewind-advectionmodel was Þtted to emergence data from a Þrst release between Fassifern and Kalbar, Queensland,and its predictive abilitywas tested against the second release nearCarnarvon,WesternAustralia. TheÞtting of the model was used to develop several hypotheses about the dispersal of E. hayati, whichwere validated by the second release: E. hayati ßies in the same direction as the wind to a distanceproportional to the wind speed; this wind-borne ßight takes place at any time during daylight hours;a ßight is attempted every day after emergence unless there are high wind conditions during that day;and the high wind condition that will delay ßight is wind speeds in excess of �2 m/s. This model ofE. hayati dispersal may be contrasted with previous models Þtted for Eretmocerus species, for whichdispersal was dominated by diffusion processes, and parasitoid spread was constrained to the scalesof tens and hundreds of meters.

KEY WORDS Eretmocerus hayati, Bemisia tabaci, advection, spread, landscape scale

Despite the potential importance of the wind-bornecomponent to small parasitoid dispersal (Pasek 1988,Chapman et al. 2004), the literature in this area islimited, and no validated wind-advection model onthe kilometers scale exists. This has bearing on theassessment of the potential efÞcacy of biocontrolagents like Eretmocerus species. Its host Bemisia tabaciGennadius (Hemiptera: Aleyrodidae) is known to dis-perse long distances (Blackmer and Byrne 1993), dis-persing �2.7 km within a morning (Byrne et al. 1996),and it has been suggested that the relatively poordispersal capability of one of its natural enemies, Er-etmocerus eremicus (Hymenoptera: Aphelinidae)Rose and Zolnerowich, was responsible for its weakperformance (Bellamy et al. 2004).

The linear parasitoid dispersal distances that havebeen observed in the literature are meters (KöllikerÐOtt et al. 2004, Takasu et al. 2004, DarrouzetÐNardi etal. 2006, Ayvaz et al. 2008, Suverkropp et al. 2009), tensof meters (Sallam et al. 2001, Langhof et al. 2005,Paranhos et al. 2007, Scarratt et al. 2008, Chapman etal. 2009), hundreds of meters (Wright et al. 2001,Schellhorn et al. 2008), and kilometers (Doutt andNakata 1973, McKenzie and Beirne 1973, Williams1984, Antolin and Strong 1987, Smith 1988). With theexceptions of Antolin and Strong (1987) and Grillen-

berger et al. (2009), previous studies only consider asingle scale per investigation. SigniÞcantly, the excep-tions revealed much longer distance dispersal thanwould have been estimated using a single smallerscale, raising the possibility that longer-distance dis-persal has been overlooked.

Studies of long-distance dispersal may be compro-mised by the constraints of the methods used. MarkÐreleaseÐrecapture methods or markÐcapture methods(Antolin and Strong 1987, Corbett and Rosenheim1996, Wright et al. 2001, Desouhant et al. 2003, Takasuet al. 2004, Paranhos et al. 2007, Scarratt et al. 2008,Schellhorn et al. 2008, Chapman et al. 2009, Grillen-berger et al. 2009, Suverkropp et al. 2009) or baitingwith sentinel hosts (Sallam et al. 2001, KöllikerÐOtt etal. 2004, Langhof et al. 2005, DarrouzetÐNardi et al.2006, Ayvaz et al. 2008, Chapman et al. 2009) maychange the insectÕs behavior. Direct methods are alsounable to provide critical information about the lo-cation of egg-laying (Hastings 2000). The Þrst-timerelease of a biocontrol agent offers an excellentopportunity to monitor dispersal without these short-comings (Petit et al. 2008).

Dispersal data can be inferred fromemergence dataunder certain conditions (e.g., the univoltine Torymussinensis Kamijo in Moriya et al. 1989). Therefore, weused the release (De Barro and Coombs 2009) of abiocontrol agent, Eretmocerus hayati Zolnerowich &Rose(Hymenoptera:Aphelinidae), and its emergencefrom its host the silverleaf whiteßy, B. tabaci Middle

1 CSIROEcosystemSciences,GPOBox2583,Brisbane,Queensland4001, Australia.

2 Corresponding author, e-mail: nadiah.kristensen@gmail.com.

0046-225X/13/1137Ð1148$04.00/0 � 2013 Entomological Society of America

East-Asia Minor 1 (also commonly known as the Bbiotype Gennadius [Hemiptera: Aleyrodidae]), to in-fer parasitoid dispersal.

Parasitoid dispersal studies may be used to deriveand Þt a dispersal model. With a few exceptions (Cor-bett and Rosenheim 1996, Brewster et al. 1997), themodels Þtted for parasitoid dispersal have been dif-fusion models (Simmons 2000, Desouhant et al. 2003,DarrouzetÐNardi et al. 2006,Chapmanet al. 2009), andthe authors knowofno study inwhichwind-advectionalone was modeled. Wind is known to inßuence para-sitoid dispersal (Hendricks 1967, Chapman 1982,Keller andLewis 1985, Smith1988,Corbett andRosen-heim 1996, Sallam et al. 2001, Wright et al. 2001, De-souhant et al. 2003, Langhof et al. 2005, Grillenbergeret al. 2009); however, theobjectiveofmost studieswastodeterminewhether andwhenparasitoids are able todisperse up- and down-wind (Chapman 1982), ratherthan investigatingwind-advectionas adispersalmech-anism speciÞcally.

For Eretmocerus species, diffusion kernel Þtting hasonly been undertaken for scales �1 km (Brewster etal. 1997, Simmons 2000). In light of the observationthat E. hayati can disperse several kilometers (Kris-tensen et al. 2013), both the mechanism and dispersalscale of most models in the literature appear unsuitedto this species. Further, none of the models developedwere validated against a second independent data set.Such model validation is necessary to avoid over-Þt-

ting, to test the robustness of the model, and to im-prove conÞdence in the dispersal mechanisms iden-tiÞed by the model Þtting.

In this study, we used a Þrst-time biocontrol release(Kristensen et al. 2013) to develop a hypothesis of E.hayati wind-borne dispersal via a model-Þtting pro-cedure. The model was validated using independentdata from a second Þrst-time release.

Materials and Methods

Study Site. Fassifern. The Þrst release occurred be-tween Fassifern and Kalbar, southÐeastern Queens-land, Australia, 27.945752� S, 152.58474� E (Fig. 1). Adetailed account may be found in Kristensen et al.(2013), but an abbreviated description is providedhere. At the time of release (12 March 2005), sunrisewas at 5:49 a.m. and sunset at 6:10p.m.The site consistsof one release Þeld, Field 0, and six sentinel Þelds fromwhich leaves containing hosts were collected to esti-mate emergence.

Field 0 is a 17-haÞeldßankedbya two-lanehighwayon the northwest edge, a tree-lined creek on thesoutheast, and a bare Þeld on the northeast. The bot-tomedge of the Field 0 runs 32 east of the northÐsouthalignment, and the release point was placed near thecenter of the Þeld, where there is a bare patch ofground that is used as a tractor turning circle. At the

Fig. 1. The ÔFassifernÕ site is situated in southÐeastern Queensland, Australia, near the townships of Fassifern and Kalbar.The sentinel collection Þelds were located at increasing distances from the release Þeld in a northeasterly direction.

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timeof release,Field0wasplantedwithbeans(varietyYates ÔStringless PioneerÕ).

The sentinel Þelds were located at increasing dis-tances fromthe releaseÞeld in thenortheastdirection.Table 1 lists the crops and locations of each Þeldrelative to the release Þeld (where coordinates aredeÞned by taking Field 0 as [0,0], north as positive y,and east as positive x).

Carnarvon. The second release occurred near Car-narvon, on the mid-west coast of Western Australia,Australia, at 24.851314�S, 113.731267�E(Fig. 2).At thetime of release (30 March 2008), sunrise was at 6:33a.m. and sunset at 6:26 p.m. The study area consists ofone release Þeld, Field 0, and 20 sentinel Þelds from

which leaves containing parasitized hosts were col-lected to estimate emergence.

The Carnarvon irrigation area is surrounded to thenorth, south, and east by desert vegetation, and to thewest by the Indian Ocean. It consists of a series ofirrigated blocks that ßank the Gascoyne River. Blocksextend no further than 1.5 km from the river. Field 0is on the south bank of the Gascoyne River, on thecorner of South River Road and Research road. At thetime of release, Field 0 was planted with rockmelons;however, the crophad started todiebefore the secondcollection on the 26 April.

The sentinel Þelds were located to the northeastand west of the release Þeld, on both sides of theGascoyne River. Table 2 lists the crops and locationsof each Þeld from which emergence was recordedrelative to the release Þeld (where coordinates aredeÞned by taking Field 0 as [0,0], north as positive y,and east as positive x).

The Release, Collection of Emergence Data, andRecordingofWeatherConditions.Fassifern.Acenter-point release of E. hayati was conducted in Field 0 at8:30 a.m. on 12 March 2005. Four mesh bags (1 by 1cm) measuring 35 by 15 by 10 cm were Þlled withsoybean leaves infestedwithB. tabaciparasitizedbyE.hayati. Approximately 130,000 wasps emerged (esti-mated from sample density per leaf and number ofleaves).At the timeof release, allB. tabacihadreached

Table 1. Coordinates of sentinel plots, in meters, used formonitoring dispersal on the landscape scale

Namex-coordinate y-coordinate

Crop(m) (m)

Field 0 0 0 Green beansField 300-NW �175 300 Green beansField 700-N �75 675 SoybeansField 700-E 700 0 Green beansField 2000-NE 1500 1375 Green beansField 2900-NE 2375 1675 Green beansField 3600-NE 2750 2375 Green beans

The release Þeld, Field 0, is taken as (0,0), North as positive y, andEast as positive x. Fields are named by their radial distance andcompass direction from the release Þeld.

Fig. 2. The ÔCarnarvonÕ site is situated on the mid-west coast of Western Australia, Australia, to the east of the town ofCarnarvon.

December 2013 KRISTENSEN ET AL.: WIND-BORNE DISPERSAL OF A PARASITOID 1139

pupal stage and 5% of E. hayati had just begun toemerge.

To evaluate long distance dispersal, on 31 March2005, 270 leaves were collected from each sentinelÞeld, and placed in containers so that parasitoid andhost emergence could be measured. Encarsia weredifferentiated from E. hayati by visual inspection. Fe-males of Eretmocerus mundus (Mercet), a species thatis known to attack B. tabaci at very low levels (DeBarro et al. 2000), look similar to females of E. hayati.There is no confusion between males of the two spe-cies because E. mundus only produces females (DeBarro and Hart 2001). Therefore, DNA analysis wasused to verify that all emerged female Eretmoceruswere E. hayati.

Weather data were collected from 12:00 a.m. on 13March to 11:30 p.m. on 30 March 2005 in 30-min in-tervals using a Vantage Pro2 from Davis Instruments.The weather station was placed in the center of theÞeld next to the release cage, on the standard tripod1.8 m tall. Recordings included temperature, hu-midity, precipitation, wind speed, and wind direc-tion. Wind velocity was averaged over each 30-mininterval. Wind direction was recorded in 1 of 16compass directions.

Carnarvon. On 30 March 2008, �40,000 parasitizedhosts were released into Field Ô0� (Fig. 2). In contrastwith the Fassifern release, the emergence of E. hayatireleased at Carnarvon was spread over �12 d.

To determine the spread of E. hayati, collections ofleaveswithhostsweremadeateachof18pointswithinthe release Þeld and at each sentinel Þeld on threeoccasions, 23, 27, and 31 d post release. The Þrst col-lectionwasmade 23 d postrelease (22April 2008), anda minimum of 30 nymphs were collected at all points.The second collection was made 27 d postrelease (26April 2008). Owing to death of the crop in the releaseÞeld, the minimum of 30 nymphs could not be ob-tained for 8 of the 18 points within the release Þeld.The Þnal collection was made 31 d postrelease (30April 2008).No leaveswere collected from the releaseÞeld for the Þnal collection.

Weather data were collected in 30-min intervalsfrom 5:30 p.m. on 30 March to 4:00 p.m. on 30 April2008, again using the Vantage Pro2 from Davis Instru-ments. The weather station was located in the centerof the release Þeld. Wind speed was averaged over the30-min interval, and wind direction was recorded inone of 16 compass directions.

Modeling. Using Emergence to Infer the Presence ofFemales. It is assumed that the presence of releasedparasitoids may be Þtted to the emergence data withan appropriate time-shift. For example, if one parasi-toid emerges 3 d after another at a certain location,then it is assumed that itwas oviposited 3dearlier thanthe other, and therefore, the respective females werepresent at those times at that location.This assumptionmay be justiÞed by observing that the developmenttime for Eretmocerus spp. is neither sensitive to theinstar parasitized (17.6, 16.8, and 16.4 d for Þrstthrough third instars, respectively, at 27�C;McAuslaneand Nguyen 1996) nor to temperature variability forthe range over which temperature varied during theexperiment (Qiu et al. 2004). In this way, emergencedata canbeused to inferpresencedata for the releasedparasitoid females.

Flight Vector is Proportional to Wind Velocity. Thedispersal of theparasitoidswasmodeledusing a simpleadvection model. The model assumes that female E.hayati will undertake wind-borne ßights in the samedirection as the wind, to a distance proportional to thewindÕs speed by a factor f. Therefore,

flight distance � f � wind speed � ßight time,

[1]

Wind velocities are determined from the 30-minaverages recorded during the experiment. There aretwo major ways in which this assumption will intro-duceerrors into themodel: theuseof 30-min averages,and the use measurements that were made near theground level.

Wind speed and direction is highly variable, and soany temporal averaging of wind velocity loses infor-mation. However, what is critical is that the input dataare sufÞcient for the purposes of the model and theresolution of the empirical data to which it is Þtted.The purpose of the model is to demonstrate that, incontrast to previous models using diffusion kernels, E.hayati can disperse on the kilometers scale and thatthis dispersal is by advection. Female E. eremicus havebeen observed to ßy for up to 108 min in ßight cham-bers,withmeanßights of 10min formated females and34 min for unmated females (Bellamy and Byrne2001); therefore, wind data averaged over time inter-vals of the same order of magnitudeÑ30 minÑaremost suitable. Fitting such a model also offers theopportunity to identify environmental factors, such astime-of-day and weather conditions, that may inßu-ence ßight on this scale.

Owing to theboundary layer effect,wind speeds arelower when closer to the ground. It is not knownexactly howhighE. hayatißywhenundertakingwind-borne dispersal; however, it is possible that it is higher

Table 2. Coordinates of ‘Carnarvon’ sentinel plots fromwhich emergence was recorded, in meters, and the host in eachfield

Namex-coordinate y-coordinate

Crop(m) (m)

Field 0 0 0 ThistlesField 6300-NE 5100 3780 ThistlesField 3500-NE 1600 3090 ThistlesField 2800-NE 1810 2080 ThistlesField 1200-NE 1220 1510 ThistlesField 3200-W 3140 770 ThistlesField 1300-NE 1050 800 ThistlesField 300-E 50 �300 ThistlesField 700-SW �630 �340 ThistlesField 1600-W �1470 �560 ThistlesField 2300-W �2110 �790 ThistlesField 4000-W �3870 �950 Thistles

The release Þeld is taken as (0,0), North as positive y, and East aspositive x.

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than 1.8 m (Glick 1939, Freeman 1945, Elzinga et al.2007), and so the wind speeds measured by ourweather station will likely have underestimated thewind speedsE.hayatiuse.Thisdifference is accountedfor by the factor f such that an underestimate of thewind speed will be corrected by Þtting an f that is �1.In addition, the factor fcanaccount for errors thatmayreduce the distance traveled by E. hayati, such as thepossibility that the mean ßight time of 10 min takenfromßight-chamber experiments is an overestimate ofßight time (e.g., because of the harsher Þeld condi-tions).

The diffusion component of dispersal is not explic-itly included in the model for two reasons. First, be-cause the number of grid-points that would be re-quired to adequately represent both the diffusionscale (hundreds of meters) and the wind-borne ad-vection scale (on the order of kilometers) would notbe computationally feasible. Second, and more signif-icantly, because the Þeld data obtained are of such alow resolution that the detailed density-distributiondata required to Þt a diffusion model are not available.However, although there is no explicit diffusion com-ponent, the coarse grid used in the model in-effectsimulates the spread of insects over the area deÞnedby the grid-square. A grid size of 500 by 500 m wasused.

Female Flight Time. It is assumed that theßight timeis the same for all females. Using a single uniformßighttime simpliÞes the model; however, it ignores manyreal-world complicating factors, including depen-dence of ßight time on mating status (Bellamy andByrne 2001), increased patch-leaving tendency at lowhost density (Bellamy et al. 2004), a variety of re-sponses to visual plant cues (Blackmer and Cross2001), potential self-direction toward host cues(Guerrieri 1997, Hagler et al. 2002), relationships be-tween ßight-tendency and time-of-day and tempera-ture (Hagler et al. 2002), relationships between egg-load, weight, and host-feeding opportunities (Asplenet al. 2001), and the effects of dessication (Berlingeret al. 1996).

A ßight time of 10 min is used in the model, takenfrom the mean ßight time reported for mated E. er-emicus females in ßight-chamber experiments (Bel-lamy and Byrne 2001, Blackmer and Cross 2001). Itshould be noted that Bellamy and Byrne (2001) re-ported a signiÞcant difference in ßight time with re-spect tomating status,with unmated females ßying fora mean time of 34 min. Because E. hayati are arrhe-notokous, if thedependenceonmating status is similarin the E. hayati species, it will manifest as a spatial biasin the sex ratiowithmoremales emerging further fromthe release Þeld. However, no such bias is evident inthe Fassifern emergence data (Fig. 3).

It is unlikely that the E. hayati in our experimentßew for an average of exactly 10 min for a number ofreasons, including the difference in species and thedifference in conditions between the Þeld and theßight chamber. However, the estimate of 10 min pro-vides as reasonable a starting point as possible giventhe information available, and the error in it will be

accounted for during the Þtting process (see discus-sion of the coefÞcient f above).

Conditions for Wind Borne Flight. It is assumed thatall females modeled will undertake one wind-borneßight per day, unless certain conditions preventingthat ßight are met. Conditions identiÞed in the liter-ature under which females may choose not to under-take a wind-borne ßight include a high whiteßy den-sity in the femaleÕs current location (Hoddle et al.1998, Jones et al. 1999), time of day (Hagler et al.2002), and weather conditions that make ßight difÞ-cult or dangerous. For example, Walters and Dixon(1984) showed that the take-off time of cereal aphidscould be delayed by several hours if the wind speedwas high enough. Response to whiteßy density wasinvestigated in the initial exploratory model runs (seeSupp. Material [online only]), and both the maximumwind speed constraint and the time-of-day at whichßights occurred were used as genetic algorithm Þttingparameters in the Þnal models. Because our modelassumes that E. hayati will ßy in the same direction asthe prevailing wind at that time, the time of day wasused with the wind data collected to determine whenßights were undertaken, and to determine whetherthis was related to the time of day and the wind speedat that time.

Number and Distribution of Eggs Oviposited. It isassumed that the number of eggs oviposited per day isequal over the study period. VillanuevaÐJimenez et al.(2012) observed that E. hayati show parasitisation upto 25 d postemergence, with a peak in female progeny5 d postemergence and in male progeny 13 d poste-mergence, summing to a ßattened (though still dual-peaked)proÞleover 17d, tapering-off until 25dposte-mergence. For comparison, E. eremicus has beenobserved with two peaks in egg-laying, one on the dayof emergence and one �5 d after emergence (Head-rick et al. 1999), and E. mundus has been observedlaying eggs for �10 d after emergence (Qiu et al.2005). In contrast to E. hayati, both E. eremicus and E.mundus have been observed to lay most of their eggswithin a few (�3) days after emergence (Qiu et al.2004). Further, dispersal and the egg-laying proÞle arealso thought to be traded-off against one another (By-rne et al. 2001), and may further depend on the pro-tein-availability circumstances in which individualsÞnd themselves (Asplen et al. 2001). As no more de-tailed information about the egg-laying proÞle of E.hayati is available, assumingaßatproÞle is the simplestassumption that can be made, and is reasonable giventhe published data (VillanuevaÐJimenez et al. 2012).

It is also assumed that oviposition occurs on the Þrstday of emergence, in the Þeld of emergence. This isjustiÞed because Eretmocerus is synovogenic andtherefore oviposition begins soon after emergence.For example, preoviposition periods of 0.29 d 20�C, 0 dat 29�C (Powell and Bellows 1992), and 0.61 d at 28�C(Headrick et al. 1999) have been observed.

Fitting. After an initial manual Þtting process thatserved to familiarize uswith the behavior of themodel(Supp. Material [online only]), the key parameterswere selected for model Þtting: start and end time of

December 2013 KRISTENSEN ET AL.: WIND-BORNE DISPERSAL OF A PARASITOID 1141

ßights, maximum wind speed at which ßights occur,and coefÞcient f.

The model was Þtted using PyGene, the geneticalgorithm library for Python. A genetic algorithm(GA) is an algorithm that searches the parameterspace for values that optimize a Þtness function usinga process that mimics natural selection (Holland1975). Each individual or phenotype was one set ofpossible parameter values. Individualswere permittedto reproduce and produce mutations, and their sur-vival to thenext generationdependedonhowwell themodel with that set of parameter values predicted thedata. The code, together with input data, sample runs,and instructions and assistance on the codeÕs use, isavailable from the lead author.

Owing to the coarseness of the data and the uncer-tainties introduced by inferring presence from emer-gence, the GA was run with the objective of matchingthe presenceÐabsence data. The Þtness function F

applied a penalty for each incorrect prediction. F wasincreased from 0 by 2 for every 2 d in which noemergencewas observed, but themodel predicted thepresence of parasitoids on at least one of those days.Fwas increasedby4 forevery2d forwhichemergencewas observed, and the model predicted no parasitoidspresent on either of those days. Erroneously predict-ing that the parasitoids would be present when nonewere observed was less heavily penalized than thereverse error, to account for the variousways inwhichparasitoids may have been present without being de-tected (e.g., death of the offspring, not collectingenough leaves to detect low densities, etc.). Alterna-tive Þtness functions are explored in the Supp. Mate-rial (online only).

Validation. The best-Þtting model for the Fassiferndata set, as foundby theGA,was rerunusing the initialemergence and wind conditions for Carnarvon. Tocheck for over-Þtting, a best-Þtting model for the

Fig. 3. Number of (a) female E. hayati, (b) male E. hayati, and (c) host B. tabaci emerged over time (day/mo of 2005)from leaves sampled from ÔFassifernÕ site.

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Carnarvon data set was also rerun on Fassifern. Inboth cases, model performance was assessed interms of the GA Þtness function and the ability ofthe models to predict key qualitative features ofeach data set.

Results

Weather. Fassifern. The mean daily temperaturerecorded over the period was 22�C, and ranged from19 to 24�C. Rain was recorded during two 30-minintervals: 0.25 mm was recorded at 2.30 a.m., 14March, and 0.51 mm was recorded at 4:00 p.m., 28March.

The predominant wind direction during the ex-perimental period was from the south. Generally,faster winds came from the southeast and slowerwinds from the southwest. Morning wind speedstended to be slower than those later in the day. Aperiod of high wind speed occurred from 19 to 23March, with speeds frequently over 2 m/s in themornings.Days 16, 17, 22Ð25, and 29Marchhadwindfrom a northerly direction, usually occurring later inthe day.

Carnarvon. The average temperature over thestudy period was 23.8�C, ranging between a minimumof12.6�Candamaximumof35.4�C.Therewere severalrain days during the experimental period: 9.4 mm wasrecorded on 31March, 6.2mmon 03April, 53.4mmon4 April, and 16.8 mm on 29 April. The predominantwind direction was from the south and southeast, withthe highest winds tending to occur in the mid-after-noon.

E. hayati Emergence From Leaves From Releaseand Sentinel Fields. Fassifern. The emergence of maleE. hayati, female E. hayati, and B. tabaci from leavescollected from the sentinel Þelds is presented in Fig.3.E.hayatiemerges fromthe fourth instar, sowechoseleaves infested with these.

The start and peak of E. hayati emergence is later inÞelds further from the release Þeld. This pattern is notevident in the emergence of B. tabaci, which peaksnear the start of the period regardless of the ÞeldÕsdistance. Therefore, the pattern of E. hayati emer-gence is suggestive of the dispersal of females.

Carnarvon. The emergence of the host and of E.hayati from leaves collected at sentinel Þelds is pre-sented in Fig. 4.

In contrastwith theFassifern release, leaf collectionwas made at three different times for the Carnarvonrelease, allowing for the possibility of collectingsecond-generation parasitoids. The parasitoids thatemerged late in the experiment from Fields 3500-NEand 2300-W were most likely second generation, asthey only emerged from leaves that were collected31 d postrelease, and emerged �24 d after the bulk ofthe emergence from the release Þeld.

Although no time-to-emergence relationships arepublished for the E. hayati species speciÞcally, usingrelationships derived for related E. eremicus and E.mundus species (Greenberget al. 2000,Qiuet al. 2004)emergence time should be between 18 and 22 d

(Greenberg et al. 2000, Qiu et al. 2004). Therefore, itis likely that all late emergence from Fields 3500-NE,1600-W, and 2300-W after 12 May were second gen-eration. In light of this, for the model Þtting, theseparasitoid emergence data points were shifted intime to approximate when their female parentswould have emerged in the same Þelds. This is inkeeping with the assumption that the synovogenicEretmocerus will oviposit on the Þrst day of emer-gence in the Þeld of emergence, as is observed forrelease generation.

Modeling. Using Emergence to Infer Presence of Re-lease Females. The rearing of the E. hayati was timedsuch that most emergence would occur on 13 March,so this was set as the start date for the model. Initialmanual exploration of the model revealed that keyfeatures of the empirical data could be reproducedby changing the maximum wind speed at whichßightwould occur and the time-of-day duringwhichßights were undertaken. Reducing the maximumwind speed to �2 m/s prevented the E. hayati frombeing blown out of the study area altogether by thefast winds that occurred from 19 March onwards.When combined with extending the time-of-day atwhich ßights occurred to include the afternoon (c.f.Hagler et al. 2002, who found that most E. emiratuswere captured between 6:00 a.m. and 10:00 a.m.),the bimodal shape of emergence in Fields 0, 300-NW, and 700-NW could be reproduced (Supp. Ma-terial [online only]).

The GA was then used to Þnd the maximum windspeed, ßight period, and f, which provided the best Þtto the empirical data. A Þtness F 52 was obtainedwhen the maximum wind speed was 2.2 m/s, f 1, theßight period start time was 6:30 a.m., and the end timewas 5:00 p.m. (Fig. 5a).

Fassifern Model’s Performance on Carnarvon. Themodel Þtted for Fassifern was rerun using the windconditions recorded for Carnarvon, with the addi-tional assumption that emergence was spread uni-formly over 12 d to reßect the change in the hostnymph stages released. The Fassifern model hadmixedsuccesspredicting theCarnarvondata(Fig. 6a).The model did correctly predict an increase in para-sitoidconcentrations in the releaseÞeld�7dafterÞrstemergence,whichcorresponded todays forwhich thewind velocities were above 2.2 m/s, preventing theparasitoids from ßying. This result gives weight tothe hypothesis that E. hayati will delay ßight duringhigh-wind conditions. The model also correctly pre-dicted the presence of parasitoids in Fields 1600-Wand 2300-W soon after the release, matching our de-duction that the late emergence in those Þelds weresecond-generation parasitoids. However, the predic-tions for NE Fields, 3200-W, and 300-E are poor, andthe model parasitoids did not reach Field 6300-NE atall.

Fitting the Carnarvon Model. The GA was used toÞnd the parameter values that led to the best-Þttingmodel, where the maximum wind speed at whichparasitoids would ßy was held at 2.2 m/s (Fig. 6). AÞtness F 82 was obtained when f 2.02, the ßight

December 2013 KRISTENSEN ET AL.: WIND-BORNE DISPERSAL OF A PARASITOID 1143

period start time was 5:00 a.m., and the end time was7:00 p.m. So the GA extended the ßight time slightlycompared with the best-Þt for Fassifern; however, themost signiÞcant difference was the doubling of thefactor f, which effectively doubles the distance thatthe parasitoids traveled.

The model found by the GA was better able topredict parasitoid presence for NE Fields, 3200-W,and300-E;however, it still couldnotpredict thearrivalof parasitoids at Þeld 6300-NE in comparably highnumbers.Onepossible reason for this failure is that themodel makes the simplifying assumption that all para-sitoids remain airborne for the average length of time.However, Bellamy and Byrne (2001) also observed a

wide range of ßight times for E. eremicus, from 2 s forone mated male to �108 min for one unmated female,so it is possible the emergence at this Þeld was fromrare parasitoids that ßew further than the average.

CarnarvonModel’s Performance onFassifern. To testhow reasonable the model found by the GA for theCarnarvon data were, and to check for over-Þtting,the model was rerun on the Fassifern site (Fig. 5c).The Carnarvon model has a Þtness of F 82 on theFassifern data, as compared with 52 from the best-Þtting model. However, comparing FassifernÕs best Þtto CarnarvonÕs best Þt (Fig. 5a and b), it can be seenthat the difference between the two model predic-tions is small. The new Carnarvon-Þtted parameter

Fig. 4. Number of (a) female E. hayati, (b) male E. hayati, and (c) host B. tabaci emerged over time (day/mo of 2008)from leaves sampled from ÔCarnarvonÕ site.

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values make predictions that still retain key featuresfrom the Fassifern-Þtted values, namely, the return ofparasitoids to Fields 0, 300-NW, and 700-NW afterdispersal, and the general tendency for parasitoids toarrive at further Þelds later in the experiment.

Discussion

This study provides evidence that supports the viewexpressed in Petit et al. (2008) that a Þrst-time releaseof a biological control agent is an excellent opportu-nity with which to study dispersal. Without the meth-odological limitations of direct marking and recapturestudies, Þrst-generation emergence data providedenough information to infer the presence of femalesreleased, to test thehypothesis ofwind-advection, andto identify the broad factors governing it.

This study also supports the authorsÕ previous rec-ommendation (Kristensen et al. 2013) that a hierar-chical sampling design be used for measuring disper-

sal. The model Þtted and tested here presents aradically different perspective on parasitoid and Er-etmocerus dispersal compared with that presented inthe literature so far. While this may be a result of realdifferences in the dispersal mechanism between thespecies consideredÑthat is, wind-advection may bepeculiar to E. hayati as compared with other Eret-mocerus for which diffusion dispersal models havebeen used (Brewster et al. 1997, Simmons 2000)Ñthis studyÕs result raises the possibility that the pre-ponderance of such models may be an artifact of thesampling methodology used, rather than a true rep-resentation of parasitoid dispersal mechanisms.

To the speciÞc question of E. hayati as an effectivebiocontrol agent for Bemisia, the results of this studyare encouraging. Bemisia is known to travel on thewind for long times over longdistances (Blackmer andByrne 1993, Byrne et al. 1996), and so an effectivebiocontrol agent will need to have dispersal capabil-ities to match that. Evidence of wind-borne dispersal

Fig. 5. The relative density of female E. hayati parasitoids through time (d/mo of 2005, solid) as predicted by (a) thebest-Þtting model (F 52) for Fassifern, and (b) the best-Þtting model (F 82) for Carnarvon, and (c) the observedemergence of E. hayati from sites at Fassifern.

December 2013 KRISTENSEN ET AL.: WIND-BORNE DISPERSAL OF A PARASITOID 1145

over several kilometers suggests that E. hayati will bea more successful B. tabaci biocontrol agent than E.eremicus. The relatively poor dispersal capability of E.eremicus has been cited as a key reason behind itsfailure (Bellamy et al. 2004).

The model validation step used increases our con-Þdence thatwinddispersal is an important componentof E. hayati dispersal. Our model also suggests that theßights take place at any time during daylight hours;that a ßight is attempted every day after emergenceunless there are high wind conditions during that day;and that the ßight will be delayed for wind speedsabove �2 m/s. However, as only one additional sitewas available for model validation, we recommend

that the speciÞcs of this description be treated withcaution. We hope that this preliminary description ofE. hayati dispersal can provide a basis from whichfurther work on parasitoid dispersal using E. hayati asa model species may be performed.

Acknowledgments

We thank Gregory Simmons for his comments and pro-viding us with an early version of his manuscript. Thisproject has been funded in part by Horticulture AustraliaLimited using the AUSVEG Levy and matched funds fromthe Australian Government, and by the Plant BiosecurityCRC.

Fig. 6. The relative density of femaleE. hayatiparasitoids through time (d/moof 2008) as predicted by (a) the best-Þttingmodel for Fassifern (Fig. 3) applied to the Carnarvon (F 114), and (b) the best-Þtting model for Carnarvon (F 82), andthe (c) observed emergence of E. hayati, including a time-shifted second-generation emergence. The assumption thatparasitoids will not ßy above 2.2 m/s led to a predicted increase in parasitoid concentrations in Field 0 corresponding to 1May 2008 and 2 May 2008 in the observed data.

1146 ENVIRONMENTAL ENTOMOLOGY Vol. 42, no. 6

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Received 25 August 2012; accepted 30 July 2013.

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