BIOLOGICAL AND MICROBIAL CONTROL

Reproduction and Feeding Behavior of Delphastus pusillus(Coleoptera Coccinellidae) a Predator of Bemisia tabaci

(Homoptera Aleyrodidae)

K A HOELMER L S OSBORNEl AND R K YOKOMI

Horticultural Research Laboratory USDA-ARS 2120 Camden Rd Orlando FL 32803

J Econ EntomoJ 86(2) 322--329(1993)ABSTRACT The development feeding behavior fecundity and longevity of Delphastuspusillus (LeConte) on the whitefly Bemisia tabaci (Gennadius) was studied in the labora-tory at 28 plusmn 3degC Developmental time from oviposition to eclosion was 210 d Longevityof adults was 605 d for females and 448 d for males Larval and adult beetles fed on allstages of whitefly The number of prey consumed by adult beetles decreased with increas-ing age and size of prey ie 1671 eggs or 116 early fourth instars per day Handling timeincreased with stage of whitefly from 313 s for eggs to 3777 s for early fourth instarsBeetle larvae began feeding upon hatching and consumed a mean of 9775 eggs beforepupating Mated females laid eggs only when reared on diets containing whitefly eggsWhen reared exclusively on a diet of eggs beetles laid 30 eggs per day Mean lifetime eggproduction was 1832 Predation on B tabaci eggs and beetle oviposition was also ob-served in a greenhouse mean prey consumption was 51 greater and mean daily ovipo-sition by females was 103 higher than in the laboratory Between 100 and 150 whiteflyeggs per day were required to initiate and sustain oviposition in the laboratory and thegreenhouse The need for large numbers of whitefly eggs in the diet suggests D pusilluswill maintain itself without augmentation only in large populations of B tabaci

KEY WORDS Delphastus pusillus Bemisia tabaci predation

SWEETPOTATO WHITEFLY Bemisia tabaci (Gen-nadius) is a worldwide tropical and subtropicalpest of many field crops (Anonymous 1986)middotespecially cotton and vegetables Damage toplants is caused by reduction in plant vigor andproduction of honeydew on which sooty moldsdevelop B tabaci also vectors many plantpathogenic viruses (Costa 1976) and recentlyhas been found to induce growth disorders insome ornamentals and vegetables (Schuster etaI 1990 1991 Yokomi et al 1990 Hoelmer et al1991) Although B tabaci was reported fromthe United States as early as 1894 (Russell 1975)it was seldom a serious problem in the UnitedStates until outbreaks began to occur in Ari-zona and California in 1981 (Johnson et al1982) and in Florida in 1986 (Hamon amp Salguero1987)

Numerous predators and parasitoids havebeen associated with B tabaci (Lopez Avila1986) but there are no published studies of itsnatural enemies in the southeastern United

This article reports the results of research only Mention of aproprietary product does not constitute an endorsement or arecommendation for its use by USDA or the University ofFloridaI University of Florida Department of Entomology

CFREC 2807 Binion Rd Apopka FL 32703

States Preliminary surveys indicate that somespecies indigenous to the region now attack Btabaci (Bennett et al 1990 Hoelmer amp Osborne1990) One native predator often found associ-ated with large populations of whiteflies in Flor-ida is Delphastus pusillus (LeConte) The adultD pusillus is a small shiny black beetle 13-14mm in length and the larva is pale yellowishwhite This coccinellid has been reported as apredator of various aleyrodids on citrus in Flor-ida (Muma 1956 Cherry amp Dowell 1979) of cit-rus blackfly Aleurocanthus woglumi Ashby inMexico (Smith et al 1964) and of Aleurotrache-Ius socialis Bondar and Trialeurodes variabilis(Quaintance) on cassava in Colombia (Gold ampAltieri 1989) All known members of the genusDelphastus Casey have been described from theNearctic and are known predators of whitefliesD pusillus is widely distributed across the cen-tral and southern United States and souththrough Central America into South America asfar as Peru (Gordon 1985)

The objectives of our study were to determinethe life history and basic rearing requirementsfor D pusillus on B tabaci and to provide apreliminary assessment of its potential as a bio-logical control agent of B tabaci

0022-0493930322-0329$02000copy 1993Entomological Society of America

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 323

Materials and Methods

Our insectary colonies of D pusillus werestarted with feral beetles collected from centralFlorida and maintained in a greenhouse and in alaboratory insectary room on B tabaci reared onPhaseolus limensis Macfady cv Henderson Eu-phorbia pulcherrima Willd ex Klotzsch Hibis-cus rosa-sinensis L and the whitefly Trialeu-rodes variabilis (Quaintance) (reared on Caricapapaya L) Voucher specimens have been placedin the Florida State Collection of ArthropodsGainesville

Laboratory studies were conducted at 28 plusmn 3degCwith a 1212 (LD) h photoperiod A stereomicro-scope was used to count whitefly eggs andnymphs (given to and consumed by beetles) andbeetle eggs laid

Developmental Studies Beetle eggs were ob-tained from the insectary colony or from femalesin the laboratory We initially tried to control thesupply of available eggs by storing them at lowtemperatures to slow their development buteggs were killed after storage overnight in a re-frigerator s6degC Even at 10degC viability of eggsstored was higher but still lower than that ofuncooled eggs Therefore all eggs used in exper-iments were fresh To minimize damage fromhandling beetle eggs were isolated on leaf disksand placed individually on moist filter paper oron 5 agar gel in petri plates kept on a bench inthe laboratory Methyl parabenzoate (methylP-hydroxy-benzoate) was added to the agar toretard growth of bacterial and fungal contami-nants Neonate beetle larvae were provideddaily with new leaf sections containing severalhundred B tabaci eggs (1-2 d old) Data on eggconsumption and molting were recorded dailyfor six males and six females throughout comple-tion of their larval and pupal development

Longevity Studies Beetle pupae were col-lected from the insectary colony and held in thelaboratory in petri dishes until emergenceNewly emerged adults were placed individuallyin plastic petri dishes containing moist filter pa-per and kept in the laboratory Females wereconfined with two or three males for 24 h formating after which males were removed Bee-tles were given leaf disks with 300 B tabacieggs every day Consumption of whitefly eggs bymale and female beetles and oviposition by fe-male beetles were recorded each day

Feeding Studies Whitefly death from preda-tion by beetles was readily distinguished fromother mortality factors thus allowing us to ac-curately count individuals consumed A high-resolution video camera with monitor was usedfor observations of feeding behavior Individualbeetles were studied in polystyrene petri plates(10 by 35 mm) with lids cut out and fitted withmesh screening to allow ventilation and preventcondensation Handling time and maximum

daily consumption of each stage was determinedby observing individual beetles in these experi-mental arenas Beetles were provided with oneof the following diets 200-300 eggs 200-300first instars 100-150 second instars 50-75 thirdinstars or 30-40 fourth instars (prepupae) Bee-tles were transferred daily to new plates contain-ing fresh leaf disks with whiteflies of the desiredstage Only female beetles observed feeding inlaboratory colonies were used for these studiesOviposition if any was recorded Egg consump-tion was recorded only from apparently healthyindividuals that fed consistently for at least 5consecutive d

Feeding studies were also done in the green-house for purposes of comparison with the re-sults of the laboratory studies Individual femaleadult beetles were confined to single hibiscusleaves with leaflet cages Leaves contained anabundant supply of whitefly eggs and nymphs ofall stages These leaves were examined with abinocular microscope while still attached to en-sure that only healthy whiteflies were initiallypresent The daily temperature range in thegreenhouse was 24-33degC during these studiesAfter feeding for 24 h the beetles were trans-ferred to a new leaf Prey consumption was eval-uated by clipping the leaf for examination with astereomicroscope and recording the number ofeach stage eaten

Oviposition Studies Oviposition by D pusil-lus fed to satiation with whitefly eggs was re-corded from the longevity studies conducted inthe laboratory The relation between quantity ofwhitefly eggs consumed and beetle fecunditywas examined by using petri dishes as experi-mental arenas as previously described Becauseunmated female beetles did not lay eggs newlyeclosed females were confined for 1-2 d withmales for mating Beetles taken from laboratorycolonies were assumed to have mated Femalesselected for these studies were given 350 eggsper day until oviposition was observed to con-firm their reproductive status Six to eight fe-males were then placed on each of five diets350 200 150 100 or 50 whitefly eggs per dayLeaf disks with whitefly eggs were changeddaily and the numbers of eggs consumed andbeetle eggs produced were recorded every dayfor 9 d Females that did not feed consistentlywere eliminated from the study leaving at leastfour to six females in each group This experi-ment was conducted in a greenhouse (tempera-ture and humidity range during the experimentwas 19-30degC and 60-95 RH daily)

To observe the effect of varying the diet of anindividual beetle on her fecundity a secondgroup of 19 females (six reared from pupae and13 collected from the insectary colony) were fedad lib until oviposition was observed They werethen given a diet of 50 eggs per day for 5 dNumbers of eggs were increased to 100 eggs per

324 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Table 1 Developmenlallime of D pusillus reared in Ihe laboralory al 28degC

ParameterDevelopmental time (d) at stage

Egg 2 3 4 4 (pupating) 5 Pupa

Mean 41 18 14 18 17 29 20 61SD 06 08 05 09 09 21 08 07Range 3-5 1-3 1-2 1-3 1-3 1-7 1-3 5-7n 16 16 14 12 3 4 3 16

day for the second 5 d then increased again to150 eggs per day for the finalS d Oviposition bybeetles was recorded each day Mean ovipositionon each diet in both experiments was comparedusing the multiple stage test (REGWF SAS In-stitute 1982) with the statistical software CRISP(Stegner amp Bostrom 1984)

The influence on beetle fecundity of mixingdifferent whitefly stages in the diet was investi-gated in the laboratory by comparing ovipositionof mated female beetles reared on four diets for21 consecutive days Diet regimes were (1)whitefly eggs only (n = 7) (2) eggs provided onlyuntil oviposition was noted after which onlyfourth instars were given (n = 8) (3) a combina-tion of 15 fourth instars and 25 eggs daily fromhatching (n = 8) and (4) a combination of 15fourth instars and 50 eggs daily from hatch (n =10) Other experimental procedures were doneas described above

Results

Developmental Biology At 28degC eggs hatchedin 3-5 d (Table 1) Instars lasted between 14 and30 d About half of the fourth instars molted to afifth instar This stadium lasted 20 d the restpupated without the extra instar The duration ofthe pupal stage was 61 d Development timewas 210 plusmn 15 d from egg to adult for femalesand 211 plusmn 15 d (mean plusmn SD) for males (n = 20for each)

Adult Longevity Newly emerged adult bee-tles are pale in color and remain inside theopened pupal cuticle for several hours Newlyemerged females did not mate as readily as those24 h or older When mated females were neededfor oviposition studies several males were con-fined for 16-24 h with each female to ensuremating Adult female longevity in laboratorystudies averaged 605 plusmn 243 d (range 26-93n = 15) Male survival averaged 448 plusmn 625 d(range 39-54 n = 6)

Feeding Behavior Beetles used their maxil-lary palpi to probe the leaf surface for prey whilewalking Detection of prey at short range ap-peared to require contact D pusillus was ob-served to walk past whiteflies if no actual contactoccurred Videocamera observations showed thatadult and larval D pusillus fed by biting throughthe whitefly integument and extracting the con-tents When feeding on older nymphs D pusil-

lus frequently regurgitated thereby reinflatingthe prey and introducing air bubbles The inter-nal contents of the whitefly were agitated duringthis process possibly helping to liquify or digestthem for extraction The oral morphology of Dpusillus was not studied but larvae of othersmall coccinellids have an internal duct withinthe mandibles for extraction and extraoral diges-tion of liquid food (Savoiskaya 1960)

Beetles generally fed only on the internal con-tents of their prey leaving the collapsed cuticleof eggs and immatures after feeding When bee-tles fed on whitefly eggs the entire shell exceptfor the base insertetl into the leaf was consumed10-15 of the time Nymphs that died fromcauses other than beetle predation left behinddried or discolored internal organs visiblethrough the cuticle Feces (watery or pasty yel-lowish deposits) were often deposited on or nearwhiteflies providing characteristic indirect evi-dence of beetle feeding activity Puncturewounds in the cuticle were not usually detect-able and therefore were not a reliable indicatorof predation Indirect evidence of predationcould be useful in evaluating the effect ofpreda-tion by D pusillus in the field We frequentlysaw such evidence of feeding activity on field-collected foliage

Consumption (prey-handling) time by firstsecond and fourth instars and adult female bee-tles generally increased within each beetle ageclass with increasing age and size of whiteflystage (Table 2) Handling times for whitefly eggsand early instars were similar for fourth instarand adult beetles but fourth instars required lesstime to consume older whitefly prey First andsecond instars expended more time than fourthinstars and adults in consuming whitefly eggsand immatures Older nymphs were seldom at-tacked however especially when yoftngerstages were available This preference may bebecause of the increased difficulty in penetrationof the cuticle which has been noted with othercoccinellid larvae (Drea 1956)

Delphastus pusillus larvae were often ob-served to congregate in the same area on thesame leaf disk even when several were availableLarvae occasionally competed with one anotherwhile feeding by bumping each other away fromprey Larval and adult beetles occasionally fedon beetle eggs and early instars this seldom oc-curred if whitefly prey was abundant

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 325

Table 2 Mean handling time in seconds (SD) by instars and adult females of D pusillus during consumption ofimmature stages of B tabaci

D pusillus B tabaci stagestage Egg 1 2 3 4 Pupa

lnstar1 4282 (873) 6910 (4343) 9225 (6014) 21783 (15227)2 2958 (ll54) 1135 (332) 2050 (1659) 5756 (5074)4 313 (112) 330 (91) 710 (210) 1001 (176) 2425 (1277)

Adult 295 (122) 277 (88) 802 (365) 2456 (761) 3777 (1584) 906 (1112)

n 10-18 observations per whitefly stage Handling time of fourth-instar whiteflies is shown only for fourth instar and adultbeetles and of pupal whiteflies only for adult beetles because of the reluctance of younger instars to feed on these prey stages

Consumption of prey began as soon as larvaehatched The mean number of whitefly eggseaten by larval D pusillus increased during thefirst three instars (Table 3) Daily consumption ofwhitefly eggs during third (mean 1491 CV922) fourth (mean 1788 CV 836) and fifthinstars (mean 1357 CV 440) was highly vari-able although the mean was similar among thethree instars The instar (third fourth or fifth) inwhich the greatest consumption occurred variedamong different beetles Total egg consumptionby third (mean 339 CV 865) fourth (mean469 CV 459) and fifth (407 n == 1) instars waspooled in Table 3 because of the high variabilitybetween daily observations the similarity ofmeans and the small number of beetles surviv-ing to complete successive older instars (n == 75and 1 respectively) in this study

The number of prey consumed per day byadult female D pusillus was highest when fed oneggs and first instars and decreased as size andage of whitefly increased (Table 4) The integerratio of eggs and first second third and earlyfourth instars consumed each day on stage-specific diets was 1412631 We assume thatthis ratio is determined by the biomass availablefor extraction from each stage of whitefly

Feeding was sometimes interrupted before thewhitefly was completely consumed neverthe-less resulting in death of the whitefly This oc-curred most frequently with fourth-instar preywhich required the most time to consume Be-cause prey were recorded as eaten only if con-sumption was complete our studies probablyprovide a conservative estimate of the mortality

Table 3 Consumption of whitefly eggs during larvaldevelopment of D pusillus

of older whitefly instars because of feeding by Dpusillus

In the comparative greenhouse feeding studybeetles were confined to single leaves on liveplants containing all stages of whitefly simulta-neously Because beetles fed on some of eachstage the ratio (determined as described above)was used to convert the numbers of whiteflieseaten in these experiments to equivalent num-bers of whitefly eggs for comparison with labo-ratory studies Based on this conversion adultbeetles in individual leaflet cages consumed70 of the food eaten in laboratory studies (ninetrials with five females)

Adult feeding activity remained high fromeclosion until death although variation from dayto day was typically high The number of white-fly eggs eaten each day was recorded over mostof the entire lifespan of five females (range39-91 d) for this group the mean number eateneach day during the first 10 d of adult life was1938 (CV 333) which was comparable withthe mean value of 1861 (CV 596) during thefinal 10 d The number of whiteflies eaten in 1 dwas sometimes as high as 4 times the meanvalue Individuals observed feeding heavily onone day often consumed relatively little the next

An estimate of the time allocated to feedingeach day was obtained by multiplying the meanhandling time with mean daily consumption ofeach whitefly stage The resulting values rangedfrom 11 to 36 hid when prey were abundanttherefore prey handling time should not be ex-pected to be a major limiting factor on predationof whiteflies by D pusillus

Table 4 Mean number of B tabaci eggs and imma-tures consumed per day by D pU8illus adult females whenfed exclusively on one stage

Instar StageTotal Parameter

Egg 2 Early 42 3-5 3

Mean 724 2174 6877 9775 Mean 1671 1381 713 352 116SD 409 1844 1681 1963 SD 770 449 254 158 64n 16 12 7 7

Total consumption during stadia 3 4 and 5 shown summedbecause of high variability within and between these instars(see text for discussion of variability)

n = 5-12 beetles and 44-58 total d obselved for each of firstsecond and third whitefly instars 4 beetles feeding for 8 deach on eggs 10 beetles for a total of 93 d feeding on fourthinstars

326 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Fig 2 Changes in oviposition by D pusillus inrelation to changes in quantity of whitefly eggs in dailydiet Mated females were fed to satiation on whiteflyeggs until egg production was noted then given dietsof 50 100 and 150 whitefly eggs per day sequentiallyfor 5 or 6 d each n = 19 beetles

Fig 1 Mean oviposition of D pusillus consumingdifferent quantities of whitefly eggs Mated femaleswere fed ad lib on whitefly eggs until egg productionwas noted then placed on one of the following diets50 100 150 200 and ~350 (abund) whitefly eggsper day (n = 566 5 4 females completed 9 d on eachdiet respectively) Mean number of whitefly eggs ac-tually consumed per day by females on each diet was50 100 133 171 and 254 respectively

1715

9

150

8

13

7

11

6

100

9

5

7

4

DAILY DIET OF BEMISIA EGGS

DAYS ON DIET

5

3

50

3

DAYS ON CONTROLLED DIET

2

EGG DIET GIVEN

50 1sect1000150 ~200 ABUND

o

o

25

ing in resumption of an occasional oviposition bya few individuals (3 of 19) most remained un-productive When diets were increased again to150 eggs per day oviposition by beetles in-creased again to levels at the beginning of theexperiment The mean number of D pusilluseggs laid each day while on the three diets isshown in Table 5 Mean daily oviposition waslowest during the 100 egg per day regime Weassume that oviposition lags behind changes infood intake by as much as several days

C 2

3enCJ 15CJW

~ 1I-WWm 05

Oviposition by D pusillus Mating was re-quired before oviposition occurred Followingmating 3-5 d elapsed before oviposition beganBeetle eggs were laid singly on their sides onleaf surfaces among whitefly eggs and nymphsEggs were sometimes deposited inside whiteflyexuviae In the laboratory eggs were laid on anysolid dry surface including the sides and lids of ~ 8

petri dishes fZOviposition by females fed ad lib on whitefly w 6

eggs in the laboratory studies averaged 30 plusmn 08 ~ 4

eggs per day (range 17-46 n = 15 beetles ~oviposition recorded for 8-64 d per individual) III 2Eggs were laid on about two-thirds of the daysdaily egg production ranged from 1 to as many as11 The mean lifetime egg production was1832 plusmn 889 with a maximum of 385 Althoughdaily oviposition by individual females typicallyvaried widely from day to day (CV 503-1593among 12 females) mean daily oviposition wasrelatively constant throughout life Of five fe-males for which oviposition was recordedthroughout most of their life in the laboratory(range 42-114 d) mean oviposition was 182eggs per day during the first half of life and 167eggs per day during the second half

No oviposition occurred in laboratory studieswhen beetles were fed exclusively on whiteflynymphs even though they were likely to havefed on eggs before being removed from the lab-oratory colony for feeding experiments Thenumber of consecutive days beetles were fed ondiets of immatures ranged from 5 to 22 (mean86)

The number of B tabaci eggs in the dietstrongly influenced the fecundity of the beetle(Fig 1) Beetle reproduction within each dietwas consistent over the 9 d of the study Femalesconsuming slOO eggs per day also produced vir-tually no progeny after being placed on reduceddiets (011 plusmn 052 on a diet of 50 whitefly eggsper day 013 plusmn 034 on a diet of 100 eggs perday) Six of the nine females on the diets with 50and 100 whitefly eggs per day deposited eggsonly on the first day after being placed on thereduced diets one individual laid a single egg 4and 5 d into the 100-egg diet Beetle fecundityincreased with whitefly egg consumption (139 plusmn157 on diet of 150 eggs per day 239 plusmn 211 ondiet of 200 eggs per day) Oviposition by femalesfed to satiation was higher under greenhouseconditions than in the laboratory averaging61 plusmn 403 eggs per day These females con-sumed a mean of 2514 plusmn 616 whitefly eggs perday 51 more than those eaten in the laboratorystudy Mean daily oviposition within each groupdiffered significantly (P lt 005)

When ovipositing beetles fed ad lib in the lab-oratory on whitefly eggs were placed on reduceddiets of 50 whitefly eggs per day ovipositiondropped to zero after 6 d (Fig 2) Their dietswere then increased to 100 eggs per day result-

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 323

Materials and Methods

Our insectary colonies of D pusillus werestarted with feral beetles collected from centralFlorida and maintained in a greenhouse and in alaboratory insectary room on B tabaci reared onPhaseolus limensis Macfady cv Henderson Eu-phorbia pulcherrima Willd ex Klotzsch Hibis-cus rosa-sinensis L and the whitefly Trialeu-rodes variabilis (Quaintance) (reared on Caricapapaya L) Voucher specimens have been placedin the Florida State Collection of ArthropodsGainesville

Laboratory studies were conducted at 28 plusmn 3degCwith a 1212 (LD) h photoperiod A stereomicro-scope was used to count whitefly eggs andnymphs (given to and consumed by beetles) andbeetle eggs laid

Developmental Studies Beetle eggs were ob-tained from the insectary colony or from femalesin the laboratory We initially tried to control thesupply of available eggs by storing them at lowtemperatures to slow their development buteggs were killed after storage overnight in a re-frigerator s6degC Even at 10degC viability of eggsstored was higher but still lower than that ofuncooled eggs Therefore all eggs used in exper-iments were fresh To minimize damage fromhandling beetle eggs were isolated on leaf disksand placed individually on moist filter paper oron 5 agar gel in petri plates kept on a bench inthe laboratory Methyl parabenzoate (methylP-hydroxy-benzoate) was added to the agar toretard growth of bacterial and fungal contami-nants Neonate beetle larvae were provideddaily with new leaf sections containing severalhundred B tabaci eggs (1-2 d old) Data on eggconsumption and molting were recorded dailyfor six males and six females throughout comple-tion of their larval and pupal development

Longevity Studies Beetle pupae were col-lected from the insectary colony and held in thelaboratory in petri dishes until emergenceNewly emerged adults were placed individuallyin plastic petri dishes containing moist filter pa-per and kept in the laboratory Females wereconfined with two or three males for 24 h formating after which males were removed Bee-tles were given leaf disks with 300 B tabacieggs every day Consumption of whitefly eggs bymale and female beetles and oviposition by fe-male beetles were recorded each day

Feeding Studies Whitefly death from preda-tion by beetles was readily distinguished fromother mortality factors thus allowing us to ac-curately count individuals consumed A high-resolution video camera with monitor was usedfor observations of feeding behavior Individualbeetles were studied in polystyrene petri plates(10 by 35 mm) with lids cut out and fitted withmesh screening to allow ventilation and preventcondensation Handling time and maximum

daily consumption of each stage was determinedby observing individual beetles in these experi-mental arenas Beetles were provided with oneof the following diets 200-300 eggs 200-300first instars 100-150 second instars 50-75 thirdinstars or 30-40 fourth instars (prepupae) Bee-tles were transferred daily to new plates contain-ing fresh leaf disks with whiteflies of the desiredstage Only female beetles observed feeding inlaboratory colonies were used for these studiesOviposition if any was recorded Egg consump-tion was recorded only from apparently healthyindividuals that fed consistently for at least 5consecutive d

Feeding studies were also done in the green-house for purposes of comparison with the re-sults of the laboratory studies Individual femaleadult beetles were confined to single hibiscusleaves with leaflet cages Leaves contained anabundant supply of whitefly eggs and nymphs ofall stages These leaves were examined with abinocular microscope while still attached to en-sure that only healthy whiteflies were initiallypresent The daily temperature range in thegreenhouse was 24-33degC during these studiesAfter feeding for 24 h the beetles were trans-ferred to a new leaf Prey consumption was eval-uated by clipping the leaf for examination with astereomicroscope and recording the number ofeach stage eaten

Oviposition Studies Oviposition by D pusil-lus fed to satiation with whitefly eggs was re-corded from the longevity studies conducted inthe laboratory The relation between quantity ofwhitefly eggs consumed and beetle fecunditywas examined by using petri dishes as experi-mental arenas as previously described Becauseunmated female beetles did not lay eggs newlyeclosed females were confined for 1-2 d withmales for mating Beetles taken from laboratorycolonies were assumed to have mated Femalesselected for these studies were given 350 eggsper day until oviposition was observed to con-firm their reproductive status Six to eight fe-males were then placed on each of five diets350 200 150 100 or 50 whitefly eggs per dayLeaf disks with whitefly eggs were changeddaily and the numbers of eggs consumed andbeetle eggs produced were recorded every dayfor 9 d Females that did not feed consistentlywere eliminated from the study leaving at leastfour to six females in each group This experi-ment was conducted in a greenhouse (tempera-ture and humidity range during the experimentwas 19-30degC and 60-95 RH daily)

To observe the effect of varying the diet of anindividual beetle on her fecundity a secondgroup of 19 females (six reared from pupae and13 collected from the insectary colony) were fedad lib until oviposition was observed They werethen given a diet of 50 eggs per day for 5 dNumbers of eggs were increased to 100 eggs per

324 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Table 1 Developmenlallime of D pusillus reared in Ihe laboralory al 28degC

ParameterDevelopmental time (d) at stage

Egg 2 3 4 4 (pupating) 5 Pupa

Mean 41 18 14 18 17 29 20 61SD 06 08 05 09 09 21 08 07Range 3-5 1-3 1-2 1-3 1-3 1-7 1-3 5-7n 16 16 14 12 3 4 3 16

day for the second 5 d then increased again to150 eggs per day for the finalS d Oviposition bybeetles was recorded each day Mean ovipositionon each diet in both experiments was comparedusing the multiple stage test (REGWF SAS In-stitute 1982) with the statistical software CRISP(Stegner amp Bostrom 1984)

The influence on beetle fecundity of mixingdifferent whitefly stages in the diet was investi-gated in the laboratory by comparing ovipositionof mated female beetles reared on four diets for21 consecutive days Diet regimes were (1)whitefly eggs only (n = 7) (2) eggs provided onlyuntil oviposition was noted after which onlyfourth instars were given (n = 8) (3) a combina-tion of 15 fourth instars and 25 eggs daily fromhatching (n = 8) and (4) a combination of 15fourth instars and 50 eggs daily from hatch (n =10) Other experimental procedures were doneas described above

Results

Developmental Biology At 28degC eggs hatchedin 3-5 d (Table 1) Instars lasted between 14 and30 d About half of the fourth instars molted to afifth instar This stadium lasted 20 d the restpupated without the extra instar The duration ofthe pupal stage was 61 d Development timewas 210 plusmn 15 d from egg to adult for femalesand 211 plusmn 15 d (mean plusmn SD) for males (n = 20for each)

Adult Longevity Newly emerged adult bee-tles are pale in color and remain inside theopened pupal cuticle for several hours Newlyemerged females did not mate as readily as those24 h or older When mated females were neededfor oviposition studies several males were con-fined for 16-24 h with each female to ensuremating Adult female longevity in laboratorystudies averaged 605 plusmn 243 d (range 26-93n = 15) Male survival averaged 448 plusmn 625 d(range 39-54 n = 6)

Feeding Behavior Beetles used their maxil-lary palpi to probe the leaf surface for prey whilewalking Detection of prey at short range ap-peared to require contact D pusillus was ob-served to walk past whiteflies if no actual contactoccurred Videocamera observations showed thatadult and larval D pusillus fed by biting throughthe whitefly integument and extracting the con-tents When feeding on older nymphs D pusil-

lus frequently regurgitated thereby reinflatingthe prey and introducing air bubbles The inter-nal contents of the whitefly were agitated duringthis process possibly helping to liquify or digestthem for extraction The oral morphology of Dpusillus was not studied but larvae of othersmall coccinellids have an internal duct withinthe mandibles for extraction and extraoral diges-tion of liquid food (Savoiskaya 1960)

Beetles generally fed only on the internal con-tents of their prey leaving the collapsed cuticleof eggs and immatures after feeding When bee-tles fed on whitefly eggs the entire shell exceptfor the base insertetl into the leaf was consumed10-15 of the time Nymphs that died fromcauses other than beetle predation left behinddried or discolored internal organs visiblethrough the cuticle Feces (watery or pasty yel-lowish deposits) were often deposited on or nearwhiteflies providing characteristic indirect evi-dence of beetle feeding activity Puncturewounds in the cuticle were not usually detect-able and therefore were not a reliable indicatorof predation Indirect evidence of predationcould be useful in evaluating the effect ofpreda-tion by D pusillus in the field We frequentlysaw such evidence of feeding activity on field-collected foliage

Consumption (prey-handling) time by firstsecond and fourth instars and adult female bee-tles generally increased within each beetle ageclass with increasing age and size of whiteflystage (Table 2) Handling times for whitefly eggsand early instars were similar for fourth instarand adult beetles but fourth instars required lesstime to consume older whitefly prey First andsecond instars expended more time than fourthinstars and adults in consuming whitefly eggsand immatures Older nymphs were seldom at-tacked however especially when yoftngerstages were available This preference may bebecause of the increased difficulty in penetrationof the cuticle which has been noted with othercoccinellid larvae (Drea 1956)

Delphastus pusillus larvae were often ob-served to congregate in the same area on thesame leaf disk even when several were availableLarvae occasionally competed with one anotherwhile feeding by bumping each other away fromprey Larval and adult beetles occasionally fedon beetle eggs and early instars this seldom oc-curred if whitefly prey was abundant

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 325

Table 2 Mean handling time in seconds (SD) by instars and adult females of D pusillus during consumption ofimmature stages of B tabaci

D pusillus B tabaci stagestage Egg 1 2 3 4 Pupa

lnstar1 4282 (873) 6910 (4343) 9225 (6014) 21783 (15227)2 2958 (ll54) 1135 (332) 2050 (1659) 5756 (5074)4 313 (112) 330 (91) 710 (210) 1001 (176) 2425 (1277)

Adult 295 (122) 277 (88) 802 (365) 2456 (761) 3777 (1584) 906 (1112)

n 10-18 observations per whitefly stage Handling time of fourth-instar whiteflies is shown only for fourth instar and adultbeetles and of pupal whiteflies only for adult beetles because of the reluctance of younger instars to feed on these prey stages

Consumption of prey began as soon as larvaehatched The mean number of whitefly eggseaten by larval D pusillus increased during thefirst three instars (Table 3) Daily consumption ofwhitefly eggs during third (mean 1491 CV922) fourth (mean 1788 CV 836) and fifthinstars (mean 1357 CV 440) was highly vari-able although the mean was similar among thethree instars The instar (third fourth or fifth) inwhich the greatest consumption occurred variedamong different beetles Total egg consumptionby third (mean 339 CV 865) fourth (mean469 CV 459) and fifth (407 n == 1) instars waspooled in Table 3 because of the high variabilitybetween daily observations the similarity ofmeans and the small number of beetles surviv-ing to complete successive older instars (n == 75and 1 respectively) in this study

The number of prey consumed per day byadult female D pusillus was highest when fed oneggs and first instars and decreased as size andage of whitefly increased (Table 4) The integerratio of eggs and first second third and earlyfourth instars consumed each day on stage-specific diets was 1412631 We assume thatthis ratio is determined by the biomass availablefor extraction from each stage of whitefly

Feeding was sometimes interrupted before thewhitefly was completely consumed neverthe-less resulting in death of the whitefly This oc-curred most frequently with fourth-instar preywhich required the most time to consume Be-cause prey were recorded as eaten only if con-sumption was complete our studies probablyprovide a conservative estimate of the mortality

Table 3 Consumption of whitefly eggs during larvaldevelopment of D pusillus

of older whitefly instars because of feeding by Dpusillus

In the comparative greenhouse feeding studybeetles were confined to single leaves on liveplants containing all stages of whitefly simulta-neously Because beetles fed on some of eachstage the ratio (determined as described above)was used to convert the numbers of whiteflieseaten in these experiments to equivalent num-bers of whitefly eggs for comparison with labo-ratory studies Based on this conversion adultbeetles in individual leaflet cages consumed70 of the food eaten in laboratory studies (ninetrials with five females)

Adult feeding activity remained high fromeclosion until death although variation from dayto day was typically high The number of white-fly eggs eaten each day was recorded over mostof the entire lifespan of five females (range39-91 d) for this group the mean number eateneach day during the first 10 d of adult life was1938 (CV 333) which was comparable withthe mean value of 1861 (CV 596) during thefinal 10 d The number of whiteflies eaten in 1 dwas sometimes as high as 4 times the meanvalue Individuals observed feeding heavily onone day often consumed relatively little the next

An estimate of the time allocated to feedingeach day was obtained by multiplying the meanhandling time with mean daily consumption ofeach whitefly stage The resulting values rangedfrom 11 to 36 hid when prey were abundanttherefore prey handling time should not be ex-pected to be a major limiting factor on predationof whiteflies by D pusillus

Table 4 Mean number of B tabaci eggs and imma-tures consumed per day by D pU8illus adult females whenfed exclusively on one stage

Instar StageTotal Parameter

Egg 2 Early 42 3-5 3

Mean 724 2174 6877 9775 Mean 1671 1381 713 352 116SD 409 1844 1681 1963 SD 770 449 254 158 64n 16 12 7 7

Total consumption during stadia 3 4 and 5 shown summedbecause of high variability within and between these instars(see text for discussion of variability)

n = 5-12 beetles and 44-58 total d obselved for each of firstsecond and third whitefly instars 4 beetles feeding for 8 deach on eggs 10 beetles for a total of 93 d feeding on fourthinstars

326 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Fig 2 Changes in oviposition by D pusillus inrelation to changes in quantity of whitefly eggs in dailydiet Mated females were fed to satiation on whiteflyeggs until egg production was noted then given dietsof 50 100 and 150 whitefly eggs per day sequentiallyfor 5 or 6 d each n = 19 beetles

Fig 1 Mean oviposition of D pusillus consumingdifferent quantities of whitefly eggs Mated femaleswere fed ad lib on whitefly eggs until egg productionwas noted then placed on one of the following diets50 100 150 200 and ~350 (abund) whitefly eggsper day (n = 566 5 4 females completed 9 d on eachdiet respectively) Mean number of whitefly eggs ac-tually consumed per day by females on each diet was50 100 133 171 and 254 respectively

1715

9

150

8

13

7

11

6

100

9

5

7

4

DAILY DIET OF BEMISIA EGGS

DAYS ON DIET

5

3

50

3

DAYS ON CONTROLLED DIET

2

EGG DIET GIVEN

50 1sect1000150 ~200 ABUND

o

o

25

ing in resumption of an occasional oviposition bya few individuals (3 of 19) most remained un-productive When diets were increased again to150 eggs per day oviposition by beetles in-creased again to levels at the beginning of theexperiment The mean number of D pusilluseggs laid each day while on the three diets isshown in Table 5 Mean daily oviposition waslowest during the 100 egg per day regime Weassume that oviposition lags behind changes infood intake by as much as several days

C 2

3enCJ 15CJW

~ 1I-WWm 05

Oviposition by D pusillus Mating was re-quired before oviposition occurred Followingmating 3-5 d elapsed before oviposition beganBeetle eggs were laid singly on their sides onleaf surfaces among whitefly eggs and nymphsEggs were sometimes deposited inside whiteflyexuviae In the laboratory eggs were laid on anysolid dry surface including the sides and lids of ~ 8

petri dishes fZOviposition by females fed ad lib on whitefly w 6

eggs in the laboratory studies averaged 30 plusmn 08 ~ 4

eggs per day (range 17-46 n = 15 beetles ~oviposition recorded for 8-64 d per individual) III 2Eggs were laid on about two-thirds of the daysdaily egg production ranged from 1 to as many as11 The mean lifetime egg production was1832 plusmn 889 with a maximum of 385 Althoughdaily oviposition by individual females typicallyvaried widely from day to day (CV 503-1593among 12 females) mean daily oviposition wasrelatively constant throughout life Of five fe-males for which oviposition was recordedthroughout most of their life in the laboratory(range 42-114 d) mean oviposition was 182eggs per day during the first half of life and 167eggs per day during the second half

No oviposition occurred in laboratory studieswhen beetles were fed exclusively on whiteflynymphs even though they were likely to havefed on eggs before being removed from the lab-oratory colony for feeding experiments Thenumber of consecutive days beetles were fed ondiets of immatures ranged from 5 to 22 (mean86)

The number of B tabaci eggs in the dietstrongly influenced the fecundity of the beetle(Fig 1) Beetle reproduction within each dietwas consistent over the 9 d of the study Femalesconsuming slOO eggs per day also produced vir-tually no progeny after being placed on reduceddiets (011 plusmn 052 on a diet of 50 whitefly eggsper day 013 plusmn 034 on a diet of 100 eggs perday) Six of the nine females on the diets with 50and 100 whitefly eggs per day deposited eggsonly on the first day after being placed on thereduced diets one individual laid a single egg 4and 5 d into the 100-egg diet Beetle fecundityincreased with whitefly egg consumption (139 plusmn157 on diet of 150 eggs per day 239 plusmn 211 ondiet of 200 eggs per day) Oviposition by femalesfed to satiation was higher under greenhouseconditions than in the laboratory averaging61 plusmn 403 eggs per day These females con-sumed a mean of 2514 plusmn 616 whitefly eggs perday 51 more than those eaten in the laboratorystudy Mean daily oviposition within each groupdiffered significantly (P lt 005)

When ovipositing beetles fed ad lib in the lab-oratory on whitefly eggs were placed on reduceddiets of 50 whitefly eggs per day ovipositiondropped to zero after 6 d (Fig 2) Their dietswere then increased to 100 eggs per day result-

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

324 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Table 1 Developmenlallime of D pusillus reared in Ihe laboralory al 28degC

ParameterDevelopmental time (d) at stage

Egg 2 3 4 4 (pupating) 5 Pupa

Mean 41 18 14 18 17 29 20 61SD 06 08 05 09 09 21 08 07Range 3-5 1-3 1-2 1-3 1-3 1-7 1-3 5-7n 16 16 14 12 3 4 3 16

day for the second 5 d then increased again to150 eggs per day for the finalS d Oviposition bybeetles was recorded each day Mean ovipositionon each diet in both experiments was comparedusing the multiple stage test (REGWF SAS In-stitute 1982) with the statistical software CRISP(Stegner amp Bostrom 1984)

The influence on beetle fecundity of mixingdifferent whitefly stages in the diet was investi-gated in the laboratory by comparing ovipositionof mated female beetles reared on four diets for21 consecutive days Diet regimes were (1)whitefly eggs only (n = 7) (2) eggs provided onlyuntil oviposition was noted after which onlyfourth instars were given (n = 8) (3) a combina-tion of 15 fourth instars and 25 eggs daily fromhatching (n = 8) and (4) a combination of 15fourth instars and 50 eggs daily from hatch (n =10) Other experimental procedures were doneas described above

Results

Developmental Biology At 28degC eggs hatchedin 3-5 d (Table 1) Instars lasted between 14 and30 d About half of the fourth instars molted to afifth instar This stadium lasted 20 d the restpupated without the extra instar The duration ofthe pupal stage was 61 d Development timewas 210 plusmn 15 d from egg to adult for femalesand 211 plusmn 15 d (mean plusmn SD) for males (n = 20for each)

Adult Longevity Newly emerged adult bee-tles are pale in color and remain inside theopened pupal cuticle for several hours Newlyemerged females did not mate as readily as those24 h or older When mated females were neededfor oviposition studies several males were con-fined for 16-24 h with each female to ensuremating Adult female longevity in laboratorystudies averaged 605 plusmn 243 d (range 26-93n = 15) Male survival averaged 448 plusmn 625 d(range 39-54 n = 6)

Feeding Behavior Beetles used their maxil-lary palpi to probe the leaf surface for prey whilewalking Detection of prey at short range ap-peared to require contact D pusillus was ob-served to walk past whiteflies if no actual contactoccurred Videocamera observations showed thatadult and larval D pusillus fed by biting throughthe whitefly integument and extracting the con-tents When feeding on older nymphs D pusil-

lus frequently regurgitated thereby reinflatingthe prey and introducing air bubbles The inter-nal contents of the whitefly were agitated duringthis process possibly helping to liquify or digestthem for extraction The oral morphology of Dpusillus was not studied but larvae of othersmall coccinellids have an internal duct withinthe mandibles for extraction and extraoral diges-tion of liquid food (Savoiskaya 1960)

Beetles generally fed only on the internal con-tents of their prey leaving the collapsed cuticleof eggs and immatures after feeding When bee-tles fed on whitefly eggs the entire shell exceptfor the base insertetl into the leaf was consumed10-15 of the time Nymphs that died fromcauses other than beetle predation left behinddried or discolored internal organs visiblethrough the cuticle Feces (watery or pasty yel-lowish deposits) were often deposited on or nearwhiteflies providing characteristic indirect evi-dence of beetle feeding activity Puncturewounds in the cuticle were not usually detect-able and therefore were not a reliable indicatorof predation Indirect evidence of predationcould be useful in evaluating the effect ofpreda-tion by D pusillus in the field We frequentlysaw such evidence of feeding activity on field-collected foliage

Consumption (prey-handling) time by firstsecond and fourth instars and adult female bee-tles generally increased within each beetle ageclass with increasing age and size of whiteflystage (Table 2) Handling times for whitefly eggsand early instars were similar for fourth instarand adult beetles but fourth instars required lesstime to consume older whitefly prey First andsecond instars expended more time than fourthinstars and adults in consuming whitefly eggsand immatures Older nymphs were seldom at-tacked however especially when yoftngerstages were available This preference may bebecause of the increased difficulty in penetrationof the cuticle which has been noted with othercoccinellid larvae (Drea 1956)

Delphastus pusillus larvae were often ob-served to congregate in the same area on thesame leaf disk even when several were availableLarvae occasionally competed with one anotherwhile feeding by bumping each other away fromprey Larval and adult beetles occasionally fedon beetle eggs and early instars this seldom oc-curred if whitefly prey was abundant

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 325

Table 2 Mean handling time in seconds (SD) by instars and adult females of D pusillus during consumption ofimmature stages of B tabaci

D pusillus B tabaci stagestage Egg 1 2 3 4 Pupa

lnstar1 4282 (873) 6910 (4343) 9225 (6014) 21783 (15227)2 2958 (ll54) 1135 (332) 2050 (1659) 5756 (5074)4 313 (112) 330 (91) 710 (210) 1001 (176) 2425 (1277)

Adult 295 (122) 277 (88) 802 (365) 2456 (761) 3777 (1584) 906 (1112)

n 10-18 observations per whitefly stage Handling time of fourth-instar whiteflies is shown only for fourth instar and adultbeetles and of pupal whiteflies only for adult beetles because of the reluctance of younger instars to feed on these prey stages

Consumption of prey began as soon as larvaehatched The mean number of whitefly eggseaten by larval D pusillus increased during thefirst three instars (Table 3) Daily consumption ofwhitefly eggs during third (mean 1491 CV922) fourth (mean 1788 CV 836) and fifthinstars (mean 1357 CV 440) was highly vari-able although the mean was similar among thethree instars The instar (third fourth or fifth) inwhich the greatest consumption occurred variedamong different beetles Total egg consumptionby third (mean 339 CV 865) fourth (mean469 CV 459) and fifth (407 n == 1) instars waspooled in Table 3 because of the high variabilitybetween daily observations the similarity ofmeans and the small number of beetles surviv-ing to complete successive older instars (n == 75and 1 respectively) in this study

The number of prey consumed per day byadult female D pusillus was highest when fed oneggs and first instars and decreased as size andage of whitefly increased (Table 4) The integerratio of eggs and first second third and earlyfourth instars consumed each day on stage-specific diets was 1412631 We assume thatthis ratio is determined by the biomass availablefor extraction from each stage of whitefly

Feeding was sometimes interrupted before thewhitefly was completely consumed neverthe-less resulting in death of the whitefly This oc-curred most frequently with fourth-instar preywhich required the most time to consume Be-cause prey were recorded as eaten only if con-sumption was complete our studies probablyprovide a conservative estimate of the mortality

Table 3 Consumption of whitefly eggs during larvaldevelopment of D pusillus

of older whitefly instars because of feeding by Dpusillus

In the comparative greenhouse feeding studybeetles were confined to single leaves on liveplants containing all stages of whitefly simulta-neously Because beetles fed on some of eachstage the ratio (determined as described above)was used to convert the numbers of whiteflieseaten in these experiments to equivalent num-bers of whitefly eggs for comparison with labo-ratory studies Based on this conversion adultbeetles in individual leaflet cages consumed70 of the food eaten in laboratory studies (ninetrials with five females)

Adult feeding activity remained high fromeclosion until death although variation from dayto day was typically high The number of white-fly eggs eaten each day was recorded over mostof the entire lifespan of five females (range39-91 d) for this group the mean number eateneach day during the first 10 d of adult life was1938 (CV 333) which was comparable withthe mean value of 1861 (CV 596) during thefinal 10 d The number of whiteflies eaten in 1 dwas sometimes as high as 4 times the meanvalue Individuals observed feeding heavily onone day often consumed relatively little the next

An estimate of the time allocated to feedingeach day was obtained by multiplying the meanhandling time with mean daily consumption ofeach whitefly stage The resulting values rangedfrom 11 to 36 hid when prey were abundanttherefore prey handling time should not be ex-pected to be a major limiting factor on predationof whiteflies by D pusillus

Table 4 Mean number of B tabaci eggs and imma-tures consumed per day by D pU8illus adult females whenfed exclusively on one stage

Instar StageTotal Parameter

Egg 2 Early 42 3-5 3

Mean 724 2174 6877 9775 Mean 1671 1381 713 352 116SD 409 1844 1681 1963 SD 770 449 254 158 64n 16 12 7 7

Total consumption during stadia 3 4 and 5 shown summedbecause of high variability within and between these instars(see text for discussion of variability)

n = 5-12 beetles and 44-58 total d obselved for each of firstsecond and third whitefly instars 4 beetles feeding for 8 deach on eggs 10 beetles for a total of 93 d feeding on fourthinstars

326 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Fig 2 Changes in oviposition by D pusillus inrelation to changes in quantity of whitefly eggs in dailydiet Mated females were fed to satiation on whiteflyeggs until egg production was noted then given dietsof 50 100 and 150 whitefly eggs per day sequentiallyfor 5 or 6 d each n = 19 beetles

Fig 1 Mean oviposition of D pusillus consumingdifferent quantities of whitefly eggs Mated femaleswere fed ad lib on whitefly eggs until egg productionwas noted then placed on one of the following diets50 100 150 200 and ~350 (abund) whitefly eggsper day (n = 566 5 4 females completed 9 d on eachdiet respectively) Mean number of whitefly eggs ac-tually consumed per day by females on each diet was50 100 133 171 and 254 respectively

1715

9

150

8

13

7

11

6

100

9

5

7

4

DAILY DIET OF BEMISIA EGGS

DAYS ON DIET

5

3

50

3

DAYS ON CONTROLLED DIET

2

EGG DIET GIVEN

50 1sect1000150 ~200 ABUND

o

o

25

ing in resumption of an occasional oviposition bya few individuals (3 of 19) most remained un-productive When diets were increased again to150 eggs per day oviposition by beetles in-creased again to levels at the beginning of theexperiment The mean number of D pusilluseggs laid each day while on the three diets isshown in Table 5 Mean daily oviposition waslowest during the 100 egg per day regime Weassume that oviposition lags behind changes infood intake by as much as several days

C 2

3enCJ 15CJW

~ 1I-WWm 05

Oviposition by D pusillus Mating was re-quired before oviposition occurred Followingmating 3-5 d elapsed before oviposition beganBeetle eggs were laid singly on their sides onleaf surfaces among whitefly eggs and nymphsEggs were sometimes deposited inside whiteflyexuviae In the laboratory eggs were laid on anysolid dry surface including the sides and lids of ~ 8

petri dishes fZOviposition by females fed ad lib on whitefly w 6

eggs in the laboratory studies averaged 30 plusmn 08 ~ 4

eggs per day (range 17-46 n = 15 beetles ~oviposition recorded for 8-64 d per individual) III 2Eggs were laid on about two-thirds of the daysdaily egg production ranged from 1 to as many as11 The mean lifetime egg production was1832 plusmn 889 with a maximum of 385 Althoughdaily oviposition by individual females typicallyvaried widely from day to day (CV 503-1593among 12 females) mean daily oviposition wasrelatively constant throughout life Of five fe-males for which oviposition was recordedthroughout most of their life in the laboratory(range 42-114 d) mean oviposition was 182eggs per day during the first half of life and 167eggs per day during the second half

No oviposition occurred in laboratory studieswhen beetles were fed exclusively on whiteflynymphs even though they were likely to havefed on eggs before being removed from the lab-oratory colony for feeding experiments Thenumber of consecutive days beetles were fed ondiets of immatures ranged from 5 to 22 (mean86)

The number of B tabaci eggs in the dietstrongly influenced the fecundity of the beetle(Fig 1) Beetle reproduction within each dietwas consistent over the 9 d of the study Femalesconsuming slOO eggs per day also produced vir-tually no progeny after being placed on reduceddiets (011 plusmn 052 on a diet of 50 whitefly eggsper day 013 plusmn 034 on a diet of 100 eggs perday) Six of the nine females on the diets with 50and 100 whitefly eggs per day deposited eggsonly on the first day after being placed on thereduced diets one individual laid a single egg 4and 5 d into the 100-egg diet Beetle fecundityincreased with whitefly egg consumption (139 plusmn157 on diet of 150 eggs per day 239 plusmn 211 ondiet of 200 eggs per day) Oviposition by femalesfed to satiation was higher under greenhouseconditions than in the laboratory averaging61 plusmn 403 eggs per day These females con-sumed a mean of 2514 plusmn 616 whitefly eggs perday 51 more than those eaten in the laboratorystudy Mean daily oviposition within each groupdiffered significantly (P lt 005)

When ovipositing beetles fed ad lib in the lab-oratory on whitefly eggs were placed on reduceddiets of 50 whitefly eggs per day ovipositiondropped to zero after 6 d (Fig 2) Their dietswere then increased to 100 eggs per day result-

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 325

Table 2 Mean handling time in seconds (SD) by instars and adult females of D pusillus during consumption ofimmature stages of B tabaci

D pusillus B tabaci stagestage Egg 1 2 3 4 Pupa

lnstar1 4282 (873) 6910 (4343) 9225 (6014) 21783 (15227)2 2958 (ll54) 1135 (332) 2050 (1659) 5756 (5074)4 313 (112) 330 (91) 710 (210) 1001 (176) 2425 (1277)

Adult 295 (122) 277 (88) 802 (365) 2456 (761) 3777 (1584) 906 (1112)

n 10-18 observations per whitefly stage Handling time of fourth-instar whiteflies is shown only for fourth instar and adultbeetles and of pupal whiteflies only for adult beetles because of the reluctance of younger instars to feed on these prey stages

Consumption of prey began as soon as larvaehatched The mean number of whitefly eggseaten by larval D pusillus increased during thefirst three instars (Table 3) Daily consumption ofwhitefly eggs during third (mean 1491 CV922) fourth (mean 1788 CV 836) and fifthinstars (mean 1357 CV 440) was highly vari-able although the mean was similar among thethree instars The instar (third fourth or fifth) inwhich the greatest consumption occurred variedamong different beetles Total egg consumptionby third (mean 339 CV 865) fourth (mean469 CV 459) and fifth (407 n == 1) instars waspooled in Table 3 because of the high variabilitybetween daily observations the similarity ofmeans and the small number of beetles surviv-ing to complete successive older instars (n == 75and 1 respectively) in this study

The number of prey consumed per day byadult female D pusillus was highest when fed oneggs and first instars and decreased as size andage of whitefly increased (Table 4) The integerratio of eggs and first second third and earlyfourth instars consumed each day on stage-specific diets was 1412631 We assume thatthis ratio is determined by the biomass availablefor extraction from each stage of whitefly

Feeding was sometimes interrupted before thewhitefly was completely consumed neverthe-less resulting in death of the whitefly This oc-curred most frequently with fourth-instar preywhich required the most time to consume Be-cause prey were recorded as eaten only if con-sumption was complete our studies probablyprovide a conservative estimate of the mortality

Table 3 Consumption of whitefly eggs during larvaldevelopment of D pusillus

of older whitefly instars because of feeding by Dpusillus

In the comparative greenhouse feeding studybeetles were confined to single leaves on liveplants containing all stages of whitefly simulta-neously Because beetles fed on some of eachstage the ratio (determined as described above)was used to convert the numbers of whiteflieseaten in these experiments to equivalent num-bers of whitefly eggs for comparison with labo-ratory studies Based on this conversion adultbeetles in individual leaflet cages consumed70 of the food eaten in laboratory studies (ninetrials with five females)

Adult feeding activity remained high fromeclosion until death although variation from dayto day was typically high The number of white-fly eggs eaten each day was recorded over mostof the entire lifespan of five females (range39-91 d) for this group the mean number eateneach day during the first 10 d of adult life was1938 (CV 333) which was comparable withthe mean value of 1861 (CV 596) during thefinal 10 d The number of whiteflies eaten in 1 dwas sometimes as high as 4 times the meanvalue Individuals observed feeding heavily onone day often consumed relatively little the next

An estimate of the time allocated to feedingeach day was obtained by multiplying the meanhandling time with mean daily consumption ofeach whitefly stage The resulting values rangedfrom 11 to 36 hid when prey were abundanttherefore prey handling time should not be ex-pected to be a major limiting factor on predationof whiteflies by D pusillus

Table 4 Mean number of B tabaci eggs and imma-tures consumed per day by D pU8illus adult females whenfed exclusively on one stage

Instar StageTotal Parameter

Egg 2 Early 42 3-5 3

Mean 724 2174 6877 9775 Mean 1671 1381 713 352 116SD 409 1844 1681 1963 SD 770 449 254 158 64n 16 12 7 7

Total consumption during stadia 3 4 and 5 shown summedbecause of high variability within and between these instars(see text for discussion of variability)

n = 5-12 beetles and 44-58 total d obselved for each of firstsecond and third whitefly instars 4 beetles feeding for 8 deach on eggs 10 beetles for a total of 93 d feeding on fourthinstars

326 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Fig 2 Changes in oviposition by D pusillus inrelation to changes in quantity of whitefly eggs in dailydiet Mated females were fed to satiation on whiteflyeggs until egg production was noted then given dietsof 50 100 and 150 whitefly eggs per day sequentiallyfor 5 or 6 d each n = 19 beetles

Fig 1 Mean oviposition of D pusillus consumingdifferent quantities of whitefly eggs Mated femaleswere fed ad lib on whitefly eggs until egg productionwas noted then placed on one of the following diets50 100 150 200 and ~350 (abund) whitefly eggsper day (n = 566 5 4 females completed 9 d on eachdiet respectively) Mean number of whitefly eggs ac-tually consumed per day by females on each diet was50 100 133 171 and 254 respectively

1715

9

150

8

13

7

11

6

100

9

5

7

4

DAILY DIET OF BEMISIA EGGS

DAYS ON DIET

5

3

50

3

DAYS ON CONTROLLED DIET

2

EGG DIET GIVEN

50 1sect1000150 ~200 ABUND

o

o

25

ing in resumption of an occasional oviposition bya few individuals (3 of 19) most remained un-productive When diets were increased again to150 eggs per day oviposition by beetles in-creased again to levels at the beginning of theexperiment The mean number of D pusilluseggs laid each day while on the three diets isshown in Table 5 Mean daily oviposition waslowest during the 100 egg per day regime Weassume that oviposition lags behind changes infood intake by as much as several days

C 2

3enCJ 15CJW

~ 1I-WWm 05

Oviposition by D pusillus Mating was re-quired before oviposition occurred Followingmating 3-5 d elapsed before oviposition beganBeetle eggs were laid singly on their sides onleaf surfaces among whitefly eggs and nymphsEggs were sometimes deposited inside whiteflyexuviae In the laboratory eggs were laid on anysolid dry surface including the sides and lids of ~ 8

petri dishes fZOviposition by females fed ad lib on whitefly w 6

eggs in the laboratory studies averaged 30 plusmn 08 ~ 4

eggs per day (range 17-46 n = 15 beetles ~oviposition recorded for 8-64 d per individual) III 2Eggs were laid on about two-thirds of the daysdaily egg production ranged from 1 to as many as11 The mean lifetime egg production was1832 plusmn 889 with a maximum of 385 Althoughdaily oviposition by individual females typicallyvaried widely from day to day (CV 503-1593among 12 females) mean daily oviposition wasrelatively constant throughout life Of five fe-males for which oviposition was recordedthroughout most of their life in the laboratory(range 42-114 d) mean oviposition was 182eggs per day during the first half of life and 167eggs per day during the second half

No oviposition occurred in laboratory studieswhen beetles were fed exclusively on whiteflynymphs even though they were likely to havefed on eggs before being removed from the lab-oratory colony for feeding experiments Thenumber of consecutive days beetles were fed ondiets of immatures ranged from 5 to 22 (mean86)

The number of B tabaci eggs in the dietstrongly influenced the fecundity of the beetle(Fig 1) Beetle reproduction within each dietwas consistent over the 9 d of the study Femalesconsuming slOO eggs per day also produced vir-tually no progeny after being placed on reduceddiets (011 plusmn 052 on a diet of 50 whitefly eggsper day 013 plusmn 034 on a diet of 100 eggs perday) Six of the nine females on the diets with 50and 100 whitefly eggs per day deposited eggsonly on the first day after being placed on thereduced diets one individual laid a single egg 4and 5 d into the 100-egg diet Beetle fecundityincreased with whitefly egg consumption (139 plusmn157 on diet of 150 eggs per day 239 plusmn 211 ondiet of 200 eggs per day) Oviposition by femalesfed to satiation was higher under greenhouseconditions than in the laboratory averaging61 plusmn 403 eggs per day These females con-sumed a mean of 2514 plusmn 616 whitefly eggs perday 51 more than those eaten in the laboratorystudy Mean daily oviposition within each groupdiffered significantly (P lt 005)

When ovipositing beetles fed ad lib in the lab-oratory on whitefly eggs were placed on reduceddiets of 50 whitefly eggs per day ovipositiondropped to zero after 6 d (Fig 2) Their dietswere then increased to 100 eggs per day result-

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

326 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

Fig 2 Changes in oviposition by D pusillus inrelation to changes in quantity of whitefly eggs in dailydiet Mated females were fed to satiation on whiteflyeggs until egg production was noted then given dietsof 50 100 and 150 whitefly eggs per day sequentiallyfor 5 or 6 d each n = 19 beetles

Fig 1 Mean oviposition of D pusillus consumingdifferent quantities of whitefly eggs Mated femaleswere fed ad lib on whitefly eggs until egg productionwas noted then placed on one of the following diets50 100 150 200 and ~350 (abund) whitefly eggsper day (n = 566 5 4 females completed 9 d on eachdiet respectively) Mean number of whitefly eggs ac-tually consumed per day by females on each diet was50 100 133 171 and 254 respectively

1715

9

150

8

13

7

11

6

100

9

5

7

4

DAILY DIET OF BEMISIA EGGS

DAYS ON DIET

5

3

50

3

DAYS ON CONTROLLED DIET

2

EGG DIET GIVEN

50 1sect1000150 ~200 ABUND

o

o

25

ing in resumption of an occasional oviposition bya few individuals (3 of 19) most remained un-productive When diets were increased again to150 eggs per day oviposition by beetles in-creased again to levels at the beginning of theexperiment The mean number of D pusilluseggs laid each day while on the three diets isshown in Table 5 Mean daily oviposition waslowest during the 100 egg per day regime Weassume that oviposition lags behind changes infood intake by as much as several days

C 2

3enCJ 15CJW

~ 1I-WWm 05

Oviposition by D pusillus Mating was re-quired before oviposition occurred Followingmating 3-5 d elapsed before oviposition beganBeetle eggs were laid singly on their sides onleaf surfaces among whitefly eggs and nymphsEggs were sometimes deposited inside whiteflyexuviae In the laboratory eggs were laid on anysolid dry surface including the sides and lids of ~ 8

petri dishes fZOviposition by females fed ad lib on whitefly w 6

eggs in the laboratory studies averaged 30 plusmn 08 ~ 4

eggs per day (range 17-46 n = 15 beetles ~oviposition recorded for 8-64 d per individual) III 2Eggs were laid on about two-thirds of the daysdaily egg production ranged from 1 to as many as11 The mean lifetime egg production was1832 plusmn 889 with a maximum of 385 Althoughdaily oviposition by individual females typicallyvaried widely from day to day (CV 503-1593among 12 females) mean daily oviposition wasrelatively constant throughout life Of five fe-males for which oviposition was recordedthroughout most of their life in the laboratory(range 42-114 d) mean oviposition was 182eggs per day during the first half of life and 167eggs per day during the second half

No oviposition occurred in laboratory studieswhen beetles were fed exclusively on whiteflynymphs even though they were likely to havefed on eggs before being removed from the lab-oratory colony for feeding experiments Thenumber of consecutive days beetles were fed ondiets of immatures ranged from 5 to 22 (mean86)

The number of B tabaci eggs in the dietstrongly influenced the fecundity of the beetle(Fig 1) Beetle reproduction within each dietwas consistent over the 9 d of the study Femalesconsuming slOO eggs per day also produced vir-tually no progeny after being placed on reduceddiets (011 plusmn 052 on a diet of 50 whitefly eggsper day 013 plusmn 034 on a diet of 100 eggs perday) Six of the nine females on the diets with 50and 100 whitefly eggs per day deposited eggsonly on the first day after being placed on thereduced diets one individual laid a single egg 4and 5 d into the 100-egg diet Beetle fecundityincreased with whitefly egg consumption (139 plusmn157 on diet of 150 eggs per day 239 plusmn 211 ondiet of 200 eggs per day) Oviposition by femalesfed to satiation was higher under greenhouseconditions than in the laboratory averaging61 plusmn 403 eggs per day These females con-sumed a mean of 2514 plusmn 616 whitefly eggs perday 51 more than those eaten in the laboratorystudy Mean daily oviposition within each groupdiffered significantly (P lt 005)

When ovipositing beetles fed ad lib in the lab-oratory on whitefly eggs were placed on reduceddiets of 50 whitefly eggs per day ovipositiondropped to zero after 6 d (Fig 2) Their dietswere then increased to 100 eggs per day result-

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 327

Table 5 Mean number of eggs (SD)laid per day by Dp~8illu8 fed ad lib until reproduction then placed ondiets of 50 100 and 150 eggs per day sequentially for 5 deach

Diet

50 eggsday100 eggsday150 eggsday

Group A

079 (095)ab003 (008)a109 (068)b

Group Bb

053 (108)ab005 (012)a076 (057)b

A + Be

061 (102)b004 (O11)a087 (061)b

and fourths only a few eggs were occasionallylaid Two of seven females placed on a diet offourth instars laid a total of 15 eggs over 21 d 5 of15 beetles reared on mixed diets laid a total of 19eggs over 21 d No eggs were produced by theremaining beetles on these diets In contrast allbeetles on the whitefly egg diet produced eggs

Means within columns followed by different letters are sigmiddotnificantly different (P lt 005 REGWF test [Stegner amp Bostrom1984])

Group A included 6 beetles reared from pupaeGroup B included 13 beetles from lab culture of unknown

age and ovipositional historye Because both groups responded similarly to diets means

for both groups pooled are also given

These results suggest consumption of between100 and 150 whitefly eggs per day is required toinitiate and maintain D pusillus ovipositionThis amount constitutes a large percentage of theaverage egg consumption by beetles each daywhen they are given unlimited food in the labo-ratory and about half of their consumption in thegreenhouse Because a relatively small part of abeetles time was spent feeding even when foodwas abundant and searching and handling timewas not limiting the capacity of D pusillus toprey on B tabaci does not appear to extend farbeyond the quantity needed to initiate reproduc-tion and reach maximum egg production

Mixed diets comprising fourth instars and sub-threshold levels of 25 or 50 eggs per day for 21 dwere not adequate to sustain beetle reproduc-tion Oviposition was highest when the diet wascomposed exclusively of eggs (Fig 3) Whenbeetles were switched from a diet of eggs tofourth instars or were given mixed diets of eggs

DIET GIVEN

4TH [g 4TH E25 D4TH E50 bull EGG

10C

~ BenCl 6ClWW 4tI-W 2WIII

03 5 7 9 11 13 15 17 19 21

DAYS AFTER ONSET OF OVIPOSITION

Fig 3 Mean daily oviposition by D pusillusreared on four different diets of B tabaci abundantfourth instars only 15 fourth instars and 25 eggs 15fourth instars and 50 eggs and abundant eggs only(control) n = 7-10 females per diet

Discussion

Delphastus pusillus is typically found feedingamong large populations of whiteflies usuallynear the top of the plant among the highest den-sities of whitefly eggs Older larvae graduallystop feeding and migrate down the plant insearch of protected places to pupate Pupae arefrequently found in aggregations on the under-sides oflower leaves These aggregations are notevenly distributed among all lower leaves butoccur only on certain leaves In the greenhousepupation also occurred underneath pots and inother cryptic locations In greenhouse and insec-tary culture Orius sp and various unidentifiedants and spiders sometimes preyed upon larvaland pupal beetles Predation of D pusillus wasnot observed in the field

When fed on B tabaci beetles feeding exclu-sively on abundant whitefly eggs were consider-ably more fecund than those feeding on lesserquantities of eggs or any other combinations ofinstars When diets consisted entirely of whiteflynymphs no beetle eggs were laid The compo-sition of diet is known to have a profound influ-ence on egg production by many species ofpolyphagous coccinellids (Hagen 1962) Duringt~e course of our study we noticed that D pu-s~llus also consumed eggs ofTetranychus urticaeKoch and Polyphagotarsonemus latus (Banks)Some coccinellids are known to feed on honey-dew produced by their prey (Hagen 1962) butwe did not observe this behavior However bee-tles were observed feeding on diluted honeyused in the laboratory as a feeding supplementfor parasitoids Although we did not investigatethe influence of alternate foods on the reproduc-tion of D pusillus such information would bevery useful in understanding the field ecology ofthis predator We also noticed that D pusillusadults avoided feeding on whitefly nymphs par-asitized by Encarsia transvena (Timberlake)this tendency was confirmed in further experi-ments to be described in detail elsewhere

Species in the coccinellid tribe Seranginiiwhich includes the genus Delphastus are rela-tively specific predators of whiteflies Conse-quently they would be expected to be welladapted as natural enemies of whitefly pestsHowever there are only a few examples of suc-cessful use of predators for biological control ofwhiteflies Gerling (1990) suggested that this isbecause of a relative lack of knowledge of pred-

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

328 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 86 no 2

ator ecology and the difficulty in obtaining dataon predator activity in field crops One docu-mented success involves Serangium parceseto-sum (Sicard) a coccinellid which has been intro-duced successfully against citrus whiteflyDialeurodes citrl (Ashmead) in Asian GeorgiaFrance and Corsica (Timofeeva amp Hoang DuikNyuan 1978 Malausa et aI 1988) and has com-plemented the action of the parasitoid Encarsialahorensis (Howard) (Malausa et aI 1988)

Although D pusillus did not significantly re-duce whitefly populations on cassava (Gold ampAltieri 1989) it was responsible for a significantproportion of mortality in citrus blackfly popula-tions (Smith et aI 1964 Cherry amp Dowell 1979)even though it could not be depended upon toregulate whitefly populations alone Our resultsand those of Smith et al (1964) suggest that itmay be most effective under warm and humidconditions Smith et aI (1964) also noted that Dpusillus appeared to be more effective in heavywhitefly populations The apparent reproductiverequirement for a diet high in eggs may explainthis observation Development of immatures alsorequired a large number of whiteflies Althoughadults are good fliers and can readily disperse tofind prey larvae are less mobile and are likely todevelop to maturity only when beetle eggs arelaid among large numbers of prey

Our studies suggest that D pusillus probablywill not maintain itself without augmentation inlow or highly dispersed populations of white-flies Based upon average consumption of preyand longevity in the laboratory individual bee-tles could consume as many as 10000 whiteflyeggs or 700 fourth instars during a lifetime Thebeetles effect on whiteflies under greenhouseconditions could be even higher although theirlongevity under these conditions is not knownBecause of its capacity to consume large num-bers of whiteflies or feed on alternate prey Dpusillus may be of value in helping to managepopulations of whitefly in conjunction with othermanagement methods as part of an integratedapproach

Acknowledgments

We thank BMcFall J Jeffers J Patton S Raaen MShaw and M Wettstein for technical assistance Wealso thank D Dean (University of Florida) F Petitt(EPCOTLand) J W Neal (USDA-ARS) D JSchuster (University of Florida) and M J Williams(Auburn University) for their helpful comments on ear-lier drafts of the manuscript Specimens of D pusilluswere determined by R D Gordon (USDA-ARSWash-ington DC)

References Cited

Anonymous 1986 Distribution pp 13-16 InMJWCock [ed] Bemisia tabaci-a literature sur-

vey on the cotton whitefly with an annotated bibli-ography FAO amp CAB Int Inst BioI Control

Bennett F D D J Schuster K A Hoelmer L SOsborne amp G Evans 1990 Survey of the sweet-potato whitefly parasitoids in cultivated and wildhosts in Florida and the Neotropics pp 75-76 InR K Yokomi et al [eds] Sweetpotato whitefly-mediated vegetable disorders in Florida Proc Uni-versity of Florida IFAS workshop Homestead FLFebruary 1990

Cherry Ramp RV Dowell 1979 Predators of citrusblackfly (Hom Aleyrodidae) Entomophaga 24385--391

Costa A C 1976 Whitefly-transmitted plant dis-eases Annu Rev Plant Pathol 14 429-449

Drea J J Jr 1956 A biological analysis of the Cal-ifornia Chilocorini (Coleoptera Coccinellidae)PhD dissertation University of California Berke-ley

Gerling D 1990 Natural enemies of whitefliespredators and parasitoids pp 147-185 In D Ger-ling [ed] Whiteflies their bionomics pest statusand management Intercept Andover UK

Gold C S amp M A Altieri 1989 The effects ofintercropping and mixed varieties of predators andparasitoids of cassava whiteflies (Hemiptera Aley-rodidae) in Colombia Bull Entomol Res 79 115-121

Gordon R D 1985 The Coccinellidae (Co-leoptera) of America north of Mexico J NYEntomol Soc 93 1-912

Hagen K 1962 Biology and ecology of predaceousCoccinellidae Annu Rev Entomol 7 289-326

Hamon A B amp V Salguero 1987 Bemisia tabacisweetpotato whitefly in Florida Div Plant IndFla Dept Agric Consumer Serv Entomol Circ292

Hoelmer K A amp L S Osborne 1990 Biologicalcontrol of sweetpotato whitefly in Florida withpredators and parasitoids pp 77-78 In R KYokomi et al [eds] Proceedings of a workshop onthe sweetpotato whitefly-mediated vegetable disor-ders in Florida Homestead FL Feb 1990 IFASUniv Florida Gainesville

Hoelmer K A L S Osborne amp R K Yokomi 1991Association of foliage disorders in Florida withfeeding by sweetpotato whitefly Bemisia tabaciFla Entomol 74 162-166

Johnson M W N C Toscano H T Reynolds E SSylvester K Kido amp E T Natwick 1982Whiteflies cause problems for southern Californiagrowers Calif Agric 36(910) 24-26

Lopez Avila A 1986 Natural enemies pp 27-35In MJW Cock [ed] Bemisia tabaci-a literaturesurvey on the cotton whitefly with an annotatedbibliography FAO amp CAB Int Inst BioI Control

Malausa J C E Franco amp P Brun 1988 Acclima-tation sur la Cote DAzur et en Corse de Serangiumparcesetosum (Col Coccinellidae) predateur deIaleurode des citrus Dialeurodes citri (HomAleyrodidae) Entomophaga 33 517-519

Muma M H 1956 Life cycles offour species ofladybeetles Fla EntomoI 39 115-118

Russell L 1975 Collection records of Bemisiatabaci (Gennadius) in the United States USDACoop Econ Insect Rep 25 229-230

SAS Institute 1982 SAS users guide statisticsSAS Institute Cary NC

April 1993 HOELMER ET AL FEEDING BEHAVIOR OF Delphastus pusillus 329

Savoiskaya G I 1960 Morphology and taxonomyof coccinellid larvae from southeast KazakhstanEntomol Rev (Eng transl Entomo Obozr) 3980-88

Schuster D J T F Mueller J B Kring amp J F Price1990 Relationship of the sweetpotato whitefly to anew tomato fruit disorder in Florida Hortscience25 1618-1620

Schuster D J J B Kring amp J F Price 1991 As-sociation of the sweetpotato whitefly with a silver-leaf disorder of squash Hortscience 26 155-156

Smith H D H L Maltby amp E J Jimenez 1964Biological control of the citrus blackfly in MexicoUSDA Tech Bull 1311

Stegner B L amp A Bostrom 1984 CRISP interac-

tive statistical package Crunch Software San Fran-cisco

Timofeeva T V amp Hoang Duik Nyaun 1978 Mor-phological and biological characteristics of the In-dian coccinellid Serangium parcesetosum (Sicard)(Coleop Coccinellidae) a predator of the citruswhitefly in Adzharia Entomo Rev (Engl transEntomol Obozr) IS 210-214

Yokomi R K K A Hoelmer amp L S Osborne 1990Relationships between the sweetpotato whiteflyand the squash silverleaf disorder Phytopathology80 895-900

Received for publication 30 December 1991 ac-cepted 22 October 1992