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Combatting whiteflies: predatory mites as a novel weapon

Nomikou, M.

Publication date2003

Link to publication

Citation for published version (APA):Nomikou, M. (2003). Combatting whiteflies: predatory mites as a novel weapon. IBED,Universiteit van Amsterdam.

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Download date:23 Jul 2021

M.. Nomikou [2003] Combatingwhite!'lies: Predatorymitesas a novel'weapon

Phytoseii dd predator s of whiteflie s feed and reproduc ee on non-pre y foo d source s

Mariaa Nomikou, Arne Janssen A Maurice W. Sabelis

IBED,IBED, Population Biology, University of Amsterdam, P.O. Box 94084, 1090 GB Amsterdam,Amsterdam, The Netherlands

Pollenn and insect-produced honeydew are among the food sources that aree likely to be available in crops where phytoseiid predators are releasedd in biological control programmes. The two species Euseius scutalisscutalis (Athias-Henriot) and Typhlodromips swirskii (Athias-Henriot) aree able to suppress whitefly populations on isolated plants and are candidatee biological control agents for the whitefly Bemisia tabaci (Gennadius).. Utilization of non-prey food sources by phytoseiids is significantt for biological control, if these diets allow reproduction or prolongg survival of predators because populations of predators will persistt in the crop in periods that whitefly prey is scarce or absent. We studiedd the impact of pollen and whitefly-produced honeydew on two phytoseiidd predators of whiteflies E. scutalis and T. swirskii. Cattail pollenn enhanced survival, development and reproduction of both predatorss studied here. Whitefly-produced honeydew increased survival off E. scutalis, and allowed low oviposition and development. TyphlodromipsTyphlodromips swirskii showed similar adult survival on leaf tissue in thee presence and absence of honeydew and pollen for a week period thatt the experiment lasted. On a diet of whitefly-produced honeydew, T.T. swirskii showed high juvenile mortality but it oviposited at a very loww rate. Both pollen and honeydew may play an important role in the biologicall control of whiteflies because these non-prey food sources affectt life history of the two predator species under study.

KeyKey words: Bemisia tabaci, biological control, Euseius scutalis, TyphlodromipsTyphlodromips swirskii, cucumber, alternative food, pollen, whitefly-producedd honeydew

Plant-inhabitingg predatory arthropods can uti l ize a variety of food sources fromm their habitat, such as plant-produced pollen, nectar, frui ts, leaf tissue, honeydeww produced by homopteran insects and phylloplane microorganisms (Hagenn 1986; Alomar and Wiedenmann 1996; Zemek and Prenerova 1997;

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Colll 1998; van Rijn and Tanigoshi 1999a, 1999b). Non-prey food sources can servee as a supply of water and nutrients complementary to a prey diet (Stonerr 1970; Salas-Aguilar and Ehler 1977; Limburg and Rosenheim 2001; Colll and Guershon 2002), but sometimes also allow for reproduction of the predatorss (McMurtry and Rodriguez 1987; McMurtry and Croft 1997).

Phytoseiidd predators are no exception to this; many predatory mites aree generalist predators that attack various prey such as spider mites, thrips andd whiteflies and use non-prey food sources such as pollen, nectar and honeydeww (McMurtry and Croft 1997). The two species Euseius scutatis (Athias-Henriot)) and Typhtodromips swirskii (Athias-Henriot) are able to suppresss whitefly populations on isolated plants (Nomikou et al. 2002) and aree candidates for biological control of the whitefly Bemisia tabaci (Gennadius).. When predation and oviposition of the two phytoseiids was measuredd on a diet of whitefly pupae, female predators were found to ovipositt without killing prey. For E. scutalis, we attributed this to feeding on whitefly-producedd honeydew, whereas for 7. swirskii we found that it retainedd eggs produced from food previously ingested (Nomikou et at. in prep).. Other studies with E. scutalis and 7". swirskii showed that coccid-producedd honeydew did not promote development and oviposition (Swirski etet al. 1967). Hence, honeydew from whiteflies may be of higher quality than coccid-producedd honeydew, at least for E. scutalis.

Utilisationn of non-prey food sources by phytoseiids is significant for biologicall control since it allows populations of predators to persist in the cropp in periods that prey is scarce or absent (Bakker 1993; van Rijn et al. 2002a).. In this article, we study the impact of pollen and whitefly-produced honeydeww on E. scutalis and T. swirskii. These two alternative food sources weree chosen because they are likely to be found in crops where the two phytoseiidss are released for biological control of whitefly. We tested the survival,, development and oviposition of the two phytoseiids when supplied withh each of the two non-prey food sources.

MATERIALSS AND METHODS

Cultures Cultures

Cucumberr plants (var. Ventura RZ®, RijkZwaan, De Lier, The Netherlands) andd lima bean plants {Phaseolus lunatus L., var. Arena) were grown from seedss in pots (2 I) in a greenhouse compartment ; l:d = 16:8) for 2.5-3 weeks. .

BemisiaBemisia tabaci strain B (= B. argentifolii) were obtained from poinsettiaa from the Research Station for Floriculture in Aalsmeer in March 1995,, and were reared on cucumber plants in climate boxes ; l:dd = 16:8).

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PhyfoseiidpredatorsPhyfoseiidpredators of'white f Hes f eed and reproduce on non-prey food sources

EuseiusEuseius scutatis was collected in Jordan in 1998 on Ricinus communis L.. infested with whiteflies (Nomikou et al. 2001). It was reared on lima bean (Phaseolus(Phaseolus lunatus L.) leaves, placed upside-down on wet cotton wool in a plasticc tray. Glue barriers were applied along the inner side of the tray and onn the wet cotton wool around the leaf to prevent escapes and contaminationn with other mite species. A piece of transparent plastic sheet (1-22 cm2), folded in the shape of a tent was placed on each arena and functionedd as a shelter for the mites (Overmeer 1985a). A few cotton threadss were put underneath the shelter to serve as an oviposition substrate (Overmeerr 1985a). Broad bean pollen (Viciafaba L.) was supplied as food by dustingg it on the arenas twice per week.

TyphlodromipsTyphlodromips swirskii was collected in Israel in 1997 on cotton infestedd with B. tabaci (Nomikou et al. 2001). It was cultured on plastic arenass (8x15 cm), placed on a wet sponge in a plastic tray containing water (seee Overmeer 1985a). Strips of wet tissue were placed on the plastic arena alongg its periphery so that the predators had access to water. Glue barriers weree applied on this tissue to prevent escape and contamination with other mitee species. Shelters and pollen were supplied as above. The predatory mitee cultures were maintained in a climate room , 60% RH).

Broadd bean pollen was collected from potted plants cultivated in a greenhousee compartment at the University of Amsterdam and cattail pollen, TyphaTypha latifolia L , was collected at the campus the University of Amsterdam andd it was used for the experiments. Both types of pollen were kept in the refrigerator. .

ExperimentalExperimental set-up

EuseiusEuseius scutalis and T. swirskii were tested individually on leaf disc arenas (244 mm diameter),, floating upside down on water-soaked cotton wool in a smalll plastic vial (60 mm diameter and 65 mm high). Leaf discs were replacedd with fresh ones every other day and, if necessary, water was added too the vial. In this way, the leaf arena remained fresh, predators had access too water, and the water served as barrier to prevent escapes of predators. Thee vial was closed with a piece of fine-mesh gauze (80 fim), kept in place byy a lid with a round hole (diameter ca. 35 mm) to allow air exchange.

Too obtain leaf arenas covered with whitefly honeydew and associated microorganisms,, 10-20 whitefly crawlers were transferred to a clean cucumberr leaf disc placed upside down on wet cotton wool in a tray placed inn a climate room , 60% RH). All prey were removed at the pupal stage, leavingg their excretions and exuviae behind and leaf discs were placed in the experimentall set up. To obtain cucumber leaf arenas with pollen, cattail pollenn (ca. 900 \ig per leaf disc) was dusted on a clean leaf disc. Clean cucumberr leaf discs without pollen were used as control.

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AdultAdult survival and oviposition

Too test the adult survival and oviposition of predators, we transferred one femalee predator (8-10 days old) of either species to arenas with honeydew, pollenn or clean leaf discs, and survival and oviposition was scored daily. This experimentss lasted for 6 days except for one replicate of E scutalis, which wass continued for 2 more weeks.

JuvenileJuvenile survival and development

Too test survival and development of juvenile predators, we placed one egg off T. swirskii or E. scutalis, less than 24 h old, to a clean leaf disc or an arenaa with honeydew or pollen, and we recorded the survival and the stage off the predator daily. The experiment lasted until the mites reached adulthood,, whereupon a female and a male were transferred to a leaf disc withh either honeydew or pollen and check for oviposition on the same food sourcee on which they developed. The sex ratio was calculated as the proportionn of females among the offspring.

Inn the statistical analysis, the critical a level for all post-hoc comparisonss (log-rank test for survival, Hosmer and Lemeshow 1999; Mann-Whitneyy (Mest for oviposition and development, Siegel and Castellan 1988) wass adjusted with the Dunn-Sidak correction (Sokal and Rohlf 1995).

RESULTS S

AdultAdult survival and oviposit/on

EuseiusEuseius scutalis showed higher survival in presence on honeydew or pollen, thann in their absence (Figure 1a; log-rank test; honeydew vs. clean leaf disc, testt statistic = 5.94, P < 0.007; pollen vs. clean leaf disc, test statistic = 5.41,, P < 0.006;). Similar survival was observed when this species was tested onn arenas with honeydew and pollen (Figure 1a; log-rank test; honeydew vs. pollen,, test statistic = -0.45, P = 0.67).

TyphlodromipsTyphlodromips swirskii showed similar survival on arenas with honeydew,honeydew, pollen and clean leaf discs (Figure 1b; log-rank test; honeydew vs.vs. clean leaf disc, test statistic = 1.42, P = 0.16; pollen vs. clean leaf disc, testt statistic = 1.08, P = 0.28; honeydew vs. pollen, test statistic = 1.67, P = 0.096).. Compared to E. scutalis, this species had higher survival on leaf tissuee alone than f. scutalis (Figure 1; log-rank test, test statistic = 6.06, PP < 0.008) and similar survival on arenas with honeydew (Figure 1; log-rank test,, test statistic = -1.38, P = 1.678) and with pollen (90-100%; Figure 1).

Ovipositionn data of the first day were excluded because they are affectedd by the previous food source of the adult predatory mites (Sabelis 1990;; van Houten et al. 1995). The total numbers of eggs from the 2nd to the

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Figur ee 1 Kaplan-Meier survival curves of adult females (a) f. scutalis, (b) T. swirskii onn leaf discs with whitefly-produced honeydew (closed circles), with pollen (triangulars)) or no other food (open circles). + shows censored data, i.e. mites that weree found in the glue.

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polle n n E.E. scutalis

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Figuree 2 Oviposition of E. scutalis (circles) and T. swirskii (triangles) on leaf discs withh pollen (solid line with closed symbols), whitefly-produced honeydew (solid line withh gray symbols), or no other food (dotted line with open symbols). Data shown aree means + SE.

6thh day varied with treatment in both predatory mite species (Figure 2, Kruskal-Walliss ANOVA by ranks; H3,45 • 34.28, P < 0.001; Siegel and Castellan 1988).. Both predatory mites showed higher oviposition on pollen than on honeydeww (Figure 2; Mann-Whitney IMests; P < 0.001). Euseius scutalis laid moree eggs on honeydew than T. swirskii (Figure 2; Mann-Whitney U-test; P < 0.001)) and similar numbers on pollen (Mann-Whitney L/-test; P = 0.1). When predatorss were not supplied with pollen or honeydew, both predatory mite speciess ceased ovipositing after the second day of the experiment (Figure 2).

Whenn f . scutalis was tested for 3 weeks on leaf discs with honeydew, itt showed 50% mortality after 15 days and 80% mortality after 21 days whereass on clean leaf discs 50% mortality was observed within 4 days. Its ovipositionn rate was on average 0.62 0.06 eggs / female / day, which correspondss with the rate obtained during the test of one week.

JuvenileJuvenile survival and development

Bothh species showed higher juvenile survival on arenas with pollen than on arenass with honeydew and this difference was significant for J. swirskii (Figuree 3; log-rank test, test statistic = 3.32, P < 0.001), but not for E. scutalisscutalis (Figure 4; log-rank test, test statistic = 1.68, P = 0.09). On clean leaf

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PhytoseiidPhytoseiid predators of whiteflies f eed and reproduce on non-prey food sources

discs,, none of the predatory mite species developed further than the protonymphh stage. On arenas wi th pollen, the two predatory mite species hadd similar juvenile mortal i ty (Figure 3, 4; log-rank test; test statistic = 0.51,, P = 0.6)

Duee to the low number of T. swirskii reaching adulthood, data on developmentt wi th honeydew as food source were not included in the analysis.. Developmental rates among the groups (each predator species sub

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Figuree 3 Juvenile survival and development of T. swirskii on leaf discs with (a) whitefly-producedd honeydew and (b) pollen.

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PartPart 1 - Screening predator traits in the laboratory

jectedd to each treatment) varied (Figure 3, 4; Kruskal-Wallis ANOVA by ranks;; H2> 70 = 44.93, P < 0.001). Euseius scutalis had a shorter development onn pollen than on honeydew (Figure 4; Mann-Whitney U-test; P = 0.02). EuseiusEuseius scutalis also showed higher developmental rate on pollen than T. swirskiiswirskii (Figure 3, 4; Mann-Whitney U-test; P < 0.001).

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Figuree 4 Juvenile survival and development of £. scutalis on leaf discs with (a) whitefly-producedd honeydew and (b) pollen.

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PhyfoseiidPhyfoseiid predators of whiteflies f eed and reproduce on non-prey food sources

Thee sex ratio of the offspring of Euseius scutatis was slightly female-biasedd on pollen (0.60) and slightly male-biased on honeydew (0.43; Figure 3),, and all females reproduced after having developed on each of the two foodd sources. The sex ratio of T. swirskii was 0.70 when it developed on pollen,, and all females reproduced at the end of the experiment. On a diet off honeydew, one individual reached adulthood, but died within two days withoutt reproducing.

DISCUSSION N

Cattaill pollen enhances survival, development and reproduction of both predatorss studied here. Pollen of several plant species is suitable for growth andd reproduction of various predatory insect and mite species (Hagen 1986; vann Rijn and Tanigoshi 1999a) and it is frequently used for mass rearing of predatoryy mites (Overmeer 1985a, 1985b; McMurtry and Croft 1997; van Rijn andd Tanigoshi 1999a). Morphological studies of several phytoseiid species showedd that Euseius scutatis, just as all other Euseius spp. investigated, havee a spoon-like structure on the lobe of the fixed digit and a wider deutosternall groove than other species (Flechtmann and McMurtry 1992a,b); thee authors hypothesized that these are adaptations for pollen feeding. Besidess morphological, physiological adaptations may also be responsible for thee ability of phytoseiids to feed on pollen.

Manyy greenhouse crops produce pollen and, if suitable as a food source,, phytoseiid populations can be established and persist in the absence off prey. Populations of F. scutatis and T. swirskii were found to aggregate on leavess with pollen, also during periods that plants were infested with 8. tabacitabaci (Nomikou et ai. 2002). Euseius scutatis switched to pollen feeding, whenn both whitefly crawlers and pollen were available and this did not changee its oviposition rate (Nomikou et at. in prep). For T. swirskii, the additionn of pollen to a diet of whitefly crawlers did not alter predation on whiteflyy or its oviposition rates (Nomikou et at. in prep.) However, mixed dietss can sometimes affect oviposition rates. On a diet of spider mites and antherss of almond, the oviposition rate of E. scutatis was higher than on eitherr of the two diets alone (Swirski et at. 1967), probably due to a synergisticc effect of the two food sources on its reproduction. On a mixed diett of eriophyoid mites and castor bean pollen, T. swirskii showed higher ovipositionn than on pollen alone and the highest reproduction on a diet of eriophyoidd mites alone (Ragusa and Swirski 1977). Hence, utilizing non-prey foodd in combination with prey can differentially influence the predation and ovipositionn rates of the two phytoseiids, but, as far as the evidence goes, thee numerical response to densities of the target prey remains equal or is evenn improved by the addition of non-prey foods.

Whitefly-producedd honeydew increased survival of E. scutatis, and allowedd low oviposition and development. Similar results were found for EuseiusEuseius stipulatus (Athias-Henriot) (Ferragut et at. 1987). Typhlodromips

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swirskiiswirskii showed similar adult survival on leaf tissue in the presence and absencee of honeydew and pollen. Other studies of T. swirskii, where it was offeredd coccid-produced honeydew or honey for longer periods than here, showedd enhanced adult survival (Ragusa and Swirski 1977; Momen and El-Sawayy 1993). Had continued the experiment for a longer period, we may havee found that T. swirskii has higher survival on a diet of honeydew comparedd to clean leaf. On a diet of whitefly or coccid-produced honeydew, T.T. swirskii showed high juvenile mortality but it oviposited at a very low ratee (Ragusa and Swirski 1977). Other studies have shown that the addition off honeydew to a spider mite or pollen diet increased oviposition of several phytoseiidd species (McMurtry and Scriven 1964; Ragusa and Swirski 1977; Zhimoo and McMurtry 1990). Hence, utilizing honeydew is beneficial for both phytoseiidd species.

Honeydeww is the excretion product of homopteran insects and, therefore,, co-occurs with whiteflies, aphids and coccids. Its quality and quantityy varies depending on the insect species, their developmental stage, thee host plant species on which the honeydew-producing insects feed, as welll as the microorganisms (e.g. black moulds) that live on honeydew (Hagenn 1986; Hendrix et at. 1996; Costa et ai. 1999). Some leaf strata are occupiedd by whiteflies for a longer time and will therefore be covered with higherr amounts of honeydew.

Whetherr honeydew is recognized as a prey product by the predators andd consequently arrests them in a patch has not been studied. However, evenn assuming that phytoseiids search randomly, since they feed on honeydew,, we expect that they will be arrested more on leaves covered withh honeydew than on other leaves. Hence, predators will encounter more whiteflyy prey by foraging on leaves covered with honeydew than on leaves withoutt honeydew.

Nevertheless,, honeydew can also have negative effects on predator behaviour.. We observed that on highly infested leaves with whitefly immatures,, predators - especially the juvenile stages - were hindered by the thickk sticky layer of honeydew (Nomikou, pers.obs.). Hulspas-Jordaan and vann Lenteren (1978) have also found that Encarsia formosa Gahan, a parasitoidd of whiteflies, can be hampered by the presence of honeydew, especiallyy when the parasitic wasps forage on hairy leaves that retain more honeydeww that the smooth ones.

Inn conclusion, phytoseiid species that can utilize these alternative food sourcess and cope well with patches covered with honeydew, will have an advantagee in that their populations show improved persistence when whitefliess are scarce (or even absent), and maintain their effectiveness againstt the whiteflies throughout the crop-growing season.

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PhytoseiidPhytoseiid predators of whiteflies f eed and reproduce on non-prey food sources

ACKNOWLEDGEMENTS S

Wee thank Sam Elliot, Farid Faraji, Erik van Gool, Sara Magalhaes, Marta AAontserrat,, Angelo Pallini, Madelaine Venzon for discussions. RijkZwaan B.V.,, De Lier, provided cucumber seeds. The manuscript was improved by Joopp van Lenteren and Joanne Fransen. The research was funded as project ABLL 4165 by the Technology Foundation STW to MN and AJ.

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PhytoseiidPhytoseiid predators ofwhite f//es f eed and reproduce on non-prey food sources

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