Evaluating Prey Preference by Several Phytoseiid Predators forMononychellus tanajoa (Bondar) and M. caribbeanae

McGregor (Acari: Tetranychidae) in Cassava

LINCOLN SMITH, MARIA ELENA CUELLAR, AND ELSA LILIANA MELO

Cassava Program, International Center of Tropical Agriculture, Apartado aereo 6713, Cali, Colombia

Received December 21, 1995; accepted March 22, 1996

Five phytoseiid predators from the dry regions ofColombia and Ecuador, which are candidate classicalbiological control agents of the cassava green mite,were evaluated for preference of the predominantindigenous prey, Mononychellus caribbeanae McGre-gor, and the target prey, Mononychellus tanajoa (Bon-dar). Preference by adult female phytoseiids was mea-sured in two-choice, split-leaf-disk experiments usingfour parameters: consumption of prey eggs, consump-tion of prey immatures, location of phytoseiid eggs,and periodic observations of the location of the forag-ing adult female phytoseiid. None of the phytoseiidspecies showed any preference with respect to theconsumption of prey tetranychid eggs. Galendromushelveolus Denmark, Neoseiulus californicus (McGre-gor), and Neoseiulus idaeus Denmark and Mumashowed substantial preference for M. tanajoa. Typhlo-dromalus tenuiscutus McMurtry & Moraes was theonly species that failed to show a preference for eithertetranychid for any of the parameters. Typhlodroma-lus manihoti (Moraes) showed a preference only forM.tanajoa immatures. None of the phytoseiids exhibiteda preference forM. caribbeanae in any of the assays, sothey can all be considered suitable biological controlcandidates with respect to preference for these twoprey species. The results are compared with resultsfrom previously published olfactometer studies. r 1996

Academic Press, Inc.

KEY WORDS: prey preference; selection of naturalenemies; biological control; predatory mites.

INTRODUCTION

The cassava greenmite,Mononychellus tanajoa (Bon-dar) (Acari: Tetranychidae) occurs on cassava Manihotesculenta Crantz (Euphorbiaceae) throughout most ofSouth America and is an important pest in dry regions,such as northeast Brazil (Farias et al., 1982; Byrne etal., 1983; Veiga, 1985). This mite was accidentallyintroduced into East Africa around 1971 and subse-

quently spread throughout the sub-Saharan cassava-growing region (Markham et al., 1987; Yaninek andHerren, 1988), where it can cause severe losses (Yanineket al., 1990; Skovgard et al., 1993; Bonato et al., 1994).Classical biological control efforts to control the pest inAfrican have continued since the 1970s (Girling et al.,1979; Yaninek and Herren, 1988) and began in 1993 innortheast Brazil.The International Center for Tropical Agriculture

(CIAT), in Colombia, has been collaborating with theInternational Institute for Tropical Agriculture (IITA),inBenin, andEmpresaBrasileira de PesquisaAgropecu-aria (EMBRAPA), in Brazil, to find and evaluate natu-ral enemies, particularly phytoseiids, to import intoAfrica. The strategy has been to identify regions inLatin America that match the climate of the targetregions, survey the arthropod fauna on cassava andnearby plants, and evaluate candidate natural enemiesin the laboratory (Yaninek and Bellotti, 1987; Yanineket al., 1993; and references therein). Northeast Brazilwas also targeted for classical biological control of thecassava green mite. This region has less than 1200 mmrain per year and more than four ‘‘dry’’ months (lessthan 60 mm rain per month). This climate correspondsto that of the northern coasts of Colombia (Guajira) andVenezuela (Lara and Zulia) and the coast of Ecuador(Guayas and Manabı). However, there are few M.tanajoa in these dry regions, and there is none inEcuador. Instead, Mononychellus caribbeanae McGre-gor, which appears to be better adapted to hot dryclimates, predominates. Because we would like to usenatural enemies from these regions in northwesternSouth America againstM. tanajoa in Brazil andAfrica,it is important to evaluate the suitability and prefer-ence for these two prey species.Determining the specificity of predators in relation to

the suitability and preference of different prey speciesis an important part of the evaluation of candidates forclassical biological control (see van Lenteren, 1980;Grant and Shepard, 1985; Rosen and Huffaker, 1983;and references therein). Such an evaluation is useful

BIOLOGICAL CONTROL 7, 179–184 (1996)ARTICLE NO. 0082

179 1049-9644/96 $18.00Copyright r 1996 by Academic Press, Inc.

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for selecting biological control agents to minimize non-target effects and maximize control of the target pest.Generally we expect suitability of prey and innatepreference to be correlated because of natural selectionto optimize fitness (Dicke et al., 1990a). However,because predator foraging behavior is complex andmaybe influenced by many different factors (e.g., Stephensand Krebs, 1986; Bell, 1990), it is worthwhile to evalu-ate more than one behavioral parameter. For example,olfactometers and wind tunnels can be used to studylong-range attraction, arena choice experiments forshort-range preference, and life history studies for preysuitability. Concordance among the different param-eters measured should improve our confidence in thedecision to include or exclude a candidate from aclassical biological control program.The purpose of this paper is to compare the acceptabil-

ity ofM. tanajoa andM. caribbeanae as prey for severalcandidate phytoseiid predators.

MATERIALS AND METHODS

Five species of phytoseiids were collected from cas-sava in dry regions of Ecuador and Colombia,Galendro-mus helveolus Denmark, Neoseiulus idaeus DenmarkandMuma,Neoseiulus californicus (McGregor),Typhlo-dromalus manihoti (Moraes) (5T. limonicus (Garmanand McGregor) sensu lato (de Moraes et al., 1994)), andTyphlodromalus tenuiscutus McMurtry and Moraes(Table 1). Phytoseiid cultures were maintained in thelaboratory on cassava leaves infested by tetranychidmites (25°C, 70 6 5% relative humidity, 12:12 h L:Dphotoperiod; Mesa and Bellotti, 1986). Tetranychusurticae Koch was used for the first three phytoseiidspecies and M. caribbeanae for the remaining species.Females 0–24 h old were held with males and M.caribbeanae for 2 days to copulate and mature.

M. tanajoa and M. caribbeanae were reared on2-month-old cassava plants (six fully expanded leaves,variety ‘CMC-40’) in screen houses. One week afterinfestation (by 200 females per plant), leaves contain-ing eggs and immature stages were collected from eachmite colony to use in experiments.The experimental arena was a cylinder 25 mm in

diameter, 15 mm in height. Two matching semicircles(25 mm diameter), one each from a leaf from each mitecolony, were placed in the bottom of the cylinder to forma tightly fitting leaf disk (Hoy and Smilanick, 1981).The main vein of the leaves ran perpendicular to theflat cut edge. The interface between the two leafsemidisks was sufficient to limit the movement ofimmature tetranychid mites, but did not restrict themovement of adult phytoseiids. Moist filter paper wasplaced under the leaf disk to prevent wilting. Leaf diskswere cut from leaf lobes having a visually similardensity of mites to try to provide an equal number ofprey on both sides of a leaf disk (see Sabelis, 1990). Thenumber of prey present on each side of the leaf disk wascounted in 35% of the replicates for each phytoseiidspecies tested. These aliquots were used to verifywhether equal numbers of the two prey species werepresented. One female phytoseiid was placed in eachcylinder at 15:00, the top of which was closed withtransparent plastic film. On the following day, fiveobservations were made of the location of the phyto-seiid (at 08:00, 11:30, 13:00, 14:00, and 15:00). After 24h, the number of eggs and immatures of each preyspecies that were consumed was recorded. The occur-rence of predation was detected by the collapsed shapeof the prey. The number of phytoseiid eggs placed oneach side of a leaf disk also was observed. The numberof replicates ranged between 21 and 35 for each phyto-seiid species.Paired t tests were used to analyze the differences

TABLE 1

Origin of Phytoseiids Used in the Experiments

Species Country Dateb Locationc

Climate Native preya

PPTd DMe MT f MC g MOh

Galendromus helveolus Ecuador 11/94 Portoviejo 523 8 0 100 0Neoseiulus californicus Ecuador 2/94 Chone 1291 7 0 80 20Neoseiulus idaeus Colombia 6/94 Aremasain 361 11 10 90 0Typhlodromalus manihoti Colombia 1/94 Monterıa 1175 4 66 28 6Typhlodromalus tenuiscutus Ecuador 2/94 Guayaquil 778 8 0 100 0

a Estimate of proportion of eachMononychellus species encountered at the collection site.b Date of collection.c Location of collection.d Average annual precipitation (mm).e Average number of dry months (,60 mm per month) per year.f Proportion ofMononychellus tanajoa.g Proportion ofMononychellus caribbeanae.h Proportion of otherMononychellus species (primarilyM. mcgregori Flechtmann & Baker).

180 SMITH, CUELLAR, AND MELO

between the two prey species in the number of preyeggs and immatures offered and the numbers con-sumed, and the location of phytoseiid oviposition. Datafor each phytoseiid species were analyzed separately.Location of the female phytoseiid was analyzed by a x2

test with all five temporal observations combined(df 5 1).

RESULTS

The average number of eggs and immatures (larvae,protonymphs, and deutonymphs) of the two prey spe-cies offered generally did not differ for any of thephytoseiid species (a 5 0.05). However, G. helveolusreceived an average of 86.1 6 11.9 (SD; n 5 7) M.caribbeanae eggs and 49.1 6 21.3M. tanajoa eggs, andT. tenuiscutus received 71.3 6 19.2 (n 5 6) M. tanajoaeggs and 42.0 6 15.4 M. caribbeanae eggs. The overallaverage numbers of prey presented were 78.3 6 25.0(SD; n 5 45) M. tanajoa and 86.2 6 47.1 M. car-ibbeanae eggs and 27.6 6 18.1 M. tanajoa and 30.1 6

12.2 M. caribbeanae immatures. Neither the averagenumber of eggs nor the average number of immaturesdiffered significantly for the two prey species.Results of the four measurements of preference for

the two prey species are presented in Figs. 1 to 5, andthe results are summarized in Table 2. The numbers onthe horizontal axis in the figures refer to the proportionof observations on female location, the number ofphytoseiid eggs laid, or the number of prey consumedon each of the two halves of a leaf disk. None of thephytoseiids showed any preference between the preyspecies in consumption of eggs. T. tenuiscutus was theonly species that showed no preference for eithertetranychid in any of the assays.N. idaeus preferredM.tanajoa with respect to consumption of immatures andsite of oviposition. T. californicus and G. helveolus

females also were observed more often on the M.tanajoa side of a leaf disk. T. manihoti preferred M.tanajoa only with respect to consumption of imma-tures. None of the phytoseiids exhibited preference forM. caribbeanae in any of the assays.

DISCUSSION

Only 5 to 10 eggs and immatures were consumed ineach experiment while about 80 eggs and 30 immatureswere available. Thus, the number of prey offered wasmuch greater than the number consumed. This shouldminimize the effect of any differences in the number ofthe two prey species offered in each trial and helpjustify the use of aliquots to estimate the number ofeach prey species offered.BecauseM. tanajoawas always at least as acceptable

FIG. 1. Preference of Neoseiulus idaeus for M. tanajoa and M.caribbeanae (mean 6 95% CI; n 5 31; *P , 0.05; **P , 0.01;***P , 0.001; x2 for location, paired t test for others).

FIG. 2. Preference of Neoseiulus californicus for M. tanajoa andM. caribbeanae (mean 6 95% CI; n 5 35; *P , 0.05; **P , 0.01;***P , 0.001; x2 for location, paired t test for others).

FIG. 3. Preference of Galendromus helveolus for M. tanajoa andM. caribbeanae (mean 6 95% CI; n 5 21; *P , 0.05; **P , 0.01;***P , 0.001; x2 for location, paired t test for others).

181PREY PREFERENCE OF PHYTOSEIID PREDATORS IN CASSAVA

as M. caribbeanae, all these phytoseiid species qualifyas suitable candidates, with respect to prey preference,for biological control of M. tanajoa. These resultsencourage us to continue evaluating phytoseiids col-lected from the dry cassava-growing regions in north-ern South America, where M. caribbeanae predomi-nates, to send to northeast Brazil and Africa, whereM.tanajoa is the onlyMononychellus species on cassava.The lack of preference for M. caribbeanae in any of

the assays is surprising given that four of the phyto-seiid species were collected from locations where M.caribbeanae predominates. It is not clear why thisspecies is less preferred than M. tanajoa. However, wefind it to be an aggressive species, capable of displacingM. tanajoa in our screen house cultures. It also appearsto be more abundant in dry regions. Because thisspecies appears to be a more harmful pest of cassava

thanM. tanajoa, it is fortunate that it has not expandedbeyond its present geographic range of the Caribbeanregion and Ecuador.T. tenuiscutus and T. manihoti show the least prefer-

ence for either of the two prey species. This lack ofpreference for M. tanajoa over M. caribbeanae is notnecessarily a disadvantage with regard to efficacyagainst M. tanajoa in locations where M. caribbeanaedoes not occur. Oviposition and prey consumption bythese two phytoseiids were similar to what has beenreported for other species. T. manihoti has alreadybecome established inWestAfrica where it is spreadingand appears to be reducing cassava mite populations(J. S. Yaninek, personal communication). This speciesalso is present in humid regions of northeast andsoutheast Brazil (de Moraes and McMurtry, 1983;Bellotti et al., 1987; G. J. de Moraes personal communi-cation).Of the four types of preference assays that we made,

consumption of immatures appears to be the mostsensitive (i.e., most capable of detecting a difference),because the largest number of species showed a prefer-ence. Larvae and protonymphs of M. tanajoa wereconsumed in much higher numbers than the otherdevelopmental stages in no-choice tests with N. idaeusand T. tenuiscutus (unpublished data). These resultssupport the intuitive idea that the preferred preystages are the best ones to use in preference studies.Although eggs were also consumed in large numbers,there is evidently little difference in acceptance be-tween these two prey species. Preference for ovipositionsite appears to be a more discriminatory test, which‘‘excluded’’ the two Typhlodromalus species. Location ofthe foraging female appears to be the most selective ofour assays, with only N. californicus and G. helveolusshowing a preference. Based on these results the fivespecies can be ranked with respect to strength ofpreference forM. tanajoa overM. caribbeanae, with G.

FIG. 4. Preference of Typhlodromalus tenuiscutus forM. tanajoaandM. caribbeanae (mean 6 95% CI; n 5 29; *P , 0.05; **P , 0.01;***P , 0.001; x2 for location, paired t test for others).

FIG. 5. Preference of Typhlodromalus manihoti for M. tanajoaandM. caribbeanae (mean 6 95% CI; n 5 27; *P , 0.05; **P , 0.01;***P , 0.001; x2 for location, paired t test for others).

TABLE 2

Summary of Prey Preference of Five Phytoseiids forM.tanajoa andM. caribbeanae

Predator

Consumption ofSite of

ovipositionLocationof female

Olfactom-eteraEggs Immatures

N. idaeus 5b Mtb Mt 5 5

N. californicus 5 Mt Mt Mt 1

G. helveolus 5 Mt Mt MtT. tenuiscutus 5 5 5 5 5

T. manihoti 5 Mt 5 5 1

a Data from Janssen et al. (1990); 1 preference for M. tanajoa-infested leaves over clean leaves; 5, no preference.

b Mt, preference for M. tanajoa; 5, no preference. There were nocases of preference forM. caribbeanae.

182 SMITH, CUELLAR, AND MELO

helveolus and N. californicus having the strongestpreference and T. tenuiscutus having the least.It is interesting to compare our results, which pertain

to behavior when in immediate contact with prey, tothose of olfactometer studies, which involve orientationwhen not in direct contact with prey. Janssen et al.(1990) compared the preference of phytoseiids for odorof cassava leaves infested with M. tanajoa to that forodor of uninfested leaves or clean air using a Y-tubeolfactometer. They found that N. californicus and T.manihoti were attracted to M. tanajoa, but that N.idaeus and T. tenuiscutus were not. Our observationson preferences of N. californicus and T. tenuiscutuswere consistent with these olfactometer responses;however, our observations for T. manihoti differ fromthe positive olfactometer response. Agreement betweenthe two studies is somewhat equivocal for N. idaeus,and G. helveolus was not tested in the olfactometerstudy. Thus, while there is some concordance betweenthe olfactometer results and our results on preferencefor location, oviposition, and prey consumption, it ap-pears that there is sufficient variation in the responsesto these assays to warrant the use of more than oneassay to evaluate prey preference. This is particularlyimportant if we consider that ‘‘preference’’ represents asuite of foraging behaviors (Bell, 1990), and thus is agraduated rather than an all-or-none phenomenon.Dicke et al. (1990a) similarly found that there was

some concordance between preference detected by Y-tube olfactometer and prey suitability (fecundity, devel-opment time, survivorship) experiments for Ambly-seius finlandicus (Oudemans), but not for A. potentillae(Garman) nor Typhlodromus pyri Scheuten, for thetetranychid Panonychus ulmi (Koch) and the eriophyidAculus schlechtendali (Nalepa). However, the differ-ences in suitability of the two prey for the latter twopredators was very small, so that a strong innatepreference for one prey over the other would notnecessarily be expected. This suggests that the olfactom-eter results may be overly sensitive (i.e., may tend togive false positives or negatives) in relation to prefer-ence based on direct predation and oviposition site.This technique also may be very sensitive to thephysiological state of a predator, its previous condition-ing, and its handling during an experiment (Dicke etal., 1990b; Lewis et al., 1990).It is important to realize that prey preference may be

affected by the relative abundance of different prey(e.g., Sabelis, 1990) and competition among predators(Janssen et al., 1991). Foraging behavior also can beinfluenced by learning and thus may be very plastic innature (e.g., Dicke et al., 1990b). Therefore, in appliedstudies such as this, preference studies can help usevaluate the ‘‘safety’’ of a candidate biological controlagent by determining the range of prey that couldpossibly be attacked in the field. However, it is much

more difficult to predict the precise balance of re-sponses a candidate species will make among severalpossible prey species in a given environmental situa-tion, which is important in evaluating its potentialeffectiveness as a biological control agent.

ACKNOWLEDGMENTS

We thank Rodrigo Zuniga for technical assistance. This work wassupported by the United Nations Development Programme GrantGLO/91/013/A/01/31, ‘‘Ecologically Sustainable Cassava Plant Protec-tion in South America and Africa: An Environmentally Sound Ap-proach.’’

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184 SMITH, CUELLAR, AND MELO