Interaction between life stages in a phytoseiid predator: western flower thrips prey killed by adults as food for protonymphs of Amblyseius cucumeris.
Experimental & Applied Acalvlogy, 17 (1993) 441-449
44 1
Interaction between life stages in a phytoseiid predator: western flower thrips prey killed by adults as food for protonymphs of Amblyseius
cucumeris Conrad Cloutier* and Susan G. Johnson Centre de Recherche en Horticulture, D~partement de biologie, Universitd Laval , Qudbec, P. Q. Canada G I K 71}4 (Accepted 17 February 1993) Abstract Conrad Cloutier and Susan G. Johnson. 1993. Interaction between life stages in a phytoseiid predator: western flower thrips prey killed by adults as food for protonymphs ofAmbly.wius cucumeris. Exp. Appl. Acarol., 17: 441-449. Alternative feeding strategies are important in determining the lifestyle of polyphagous spider mite predators, and could play a key role in their use for biocontrol of prey such as thrips. The small size of Amblyseius cucumeris relative to western flower thrips, Franktiniella occidentalis, limits its survival and development when this prey is the only food available. We show that when A. cucumeris nymphs were reared either alone or with a gravid female on live larvae ofF. occidentalis as the only source of food, survival was increased and development was accelerated by the presence of the adult. Similar pertbrmance by predator nymphs reared alone on freshly killed thrips larvae indicated that those nymphs reared on live prey with an adult were benefiting from feeding on prey killed by the adult. Variation of the period when an adult female was present with the nymph showed that food provided as a result of the adult's preying activities was beneficial until approximately one third through nymphal development, afler which protonymphsbecame independent predators, with good survival and rapid development when provided only with live F. occidentalis larvae. The results are discussed in relation to adult dispersal in specialist as opposed to generalist phytoseiids, and its potential manipulation in using A. cucumeris for thrips biocontrol. INTRODUCTION
Flexibility in feeding strategy expressed in behaviors such as feeding on alternativc prey (polyphagy, but also including cannibalism) or feeding on non-prey tbod (e.g. pollen) have commonly been obscr~'ed in phytoseiid spider mite predators (see Overmeel, 1985 for a review). In addition to functioning as adaptations to survive at low prey density, alternative feeding strategies are also generally desirable in phytoseiids that are candidates for biocontrol. To understand the ecological factors *To wlwm correspondence should be addressed.
©Sciencc and Technology Letters. AIr rights reserved.
442
C. CLOUTIER AND S. G. JOHNSON
selecting for such adaptations, and to manipulate them successfully, it is important to identify the traits involved and to determine how they are expressed in predator behavior. Amblyseius cucurneris Oudemans is a generalist phytoseiid that is commercially available and widely used for thrips biocontrol in greenhouses (De Klerk and Ramakers, 1986; Gillespie 1989; Gilkeson et al. 1990; Steiner and Tellier, 1990). The western flower thrips, Frankliniella occidentalis (Pergande), infests greenhouse vegetable and ornamental crops worldwide (Allen and Broadbent, 1986; Mantel, 1989; van der Hoeven and van Rijn, 1990; Steiner and Tellier, 1990). A major advantage ofA. cucumeris is that it can easily be mass cultured (Ramakers and van Lieburg, 1982), but a disadvantage is its small size relative to the western flower thrips. Previous studies have shown that the success rate ofA. cucumeris at capturing thrips is high only for the smallest thrips larvae, which suggests that this predator is not well adapted to thrips. As a practical consequence for biocontrol, a large proportion of the prey's life cycle escapes predation, which could limit this predator's ability to control thrips populations. Gillespie and Ramey (1989) noted that F. occidentalis larvae are "expensive" prey for A. cucumeris. Bakker and Sabelis (1989) found that predation success of adult A. cucumeris was strongly reduced on second compared to first stage Thrips tabaci Lindeman, and was strongly dependent on starvation. Sengonca and Bendiek (1988) found only 5% survival of A. cucumeris protonymphs on a diet of 1st and 2nd instar E occidentalis. In controlled experiments with predators isolated on leaf disks, Johnson (1990) found a drop in A. cucumeris survival from 100% on spider mites, to only 30% on western flower thrips, and a corresponding increase in developmental time from 6 to 8 days. Because it appears that A. cucumeris young nymphs have difficulty capturing even the smallest F. occidentalis larvae, alternative food might be essential for completion of the life cycle and population growth of the phytoseiid with thrips prey. On greenhouse crops, generally available alternative sources of food for the early feeding stages ofA. cucumeris include pollen (van Rijn and Sabelis, 1990; van Rijn and van Houten, 1990), and e g g s a n d small active stages of commonly present tetranychid pests such as the two-spotted spider mite, Tetranychus urticae Koch (Johnson, 1990). More consistent control of western flower thrips on sweet pepper than on cucumbers (Gillespie, 1989; Ramakers et al., 1989; Bennison et al., 1990; van Rijn and Sabelis, 1990) is circumstancial evidence suggesting feeding on pollen by A. cucumeris. Pollen suitability as food for A. cucumeris was also confirmed experimentally (Ramakers, 1990; van Rijn and van Houten, 1990). However, parthenocarpic greenhouse cucumber plants produce virtually no pollen, and spider mites cannot be relied upon as alternative prey because these pests must be controlled when present. Therefore, on cucumber infested by F. occidentalis, thrips larvae may normally be the only possible som'ce of food forA. cucumeris establishment (except for small numbers of acarid mites used as prey for mass rearing and released with the predator at the time of introduction).
INTERACTION BETWEEN LIFE STAGES IN A PHYTOSEIID PREDATOR
443
The objective of this study was to examine the role that prey killed by mature stages of A. cucumeris could play, when only E occidemalis prey is available, in allowing survival and development of the immature feeding stages of the phytoseiid (proto- and deutonymph). We tested the hypothesis that adult females of A. cucumeris may provide food to nymphs through left overs from dead prey abandoned alter being partly sucked, or tx~ssibly also as casual shares of recent Nlls on which they are still feeding. The hypothesis would be valid if, in the presence of adults, survival of nymphs would increase, and/or developmental time would decrease, compared to nymphs reared without adults being present. MATERIALS AND METHODS Prey and predators A western flower thrips colony was maintained on Phaseolus vulgaris (cv. Contender) in an experimental greenhouse. Cohorts of thrips larvae obtained from adult females were allowed to lay eggs on English cucumber leaf disks supported on fertilized agar (Brodeur and Cloutier, 1992). Amblyseius cucumeris was purchased from Applied Bionomics, Sidney, B.C. Canada. Gravid females extracted from the supplier's mass rearing medium were left to oviposit on cucumber leaf disks for 2-3 hours. Freshly laid eggs were transferred individually to 1 cm diam leaf disks in experimental arenas (Brodeur and Cloutier, 1992) and held at 25°C, 40-50% R.H., and 16:8 L:D throughout the experiment. Experimental design and observations To determine if preying activities of adult A. cucumeris affect survival and development of immature stages, the predators were reared from egg to adult under d i f ferent treatments involving the presence or absence of a gravid female. To determine when an immature A. cucumeris becomes able to develop successfully by predation on F. occidentalis larvae, the presence of the adult was manipulated to obtain three different treatments, i.e, the adult was removed 1,2, or 3 days after the larval-protonymphal molt. Under experimental conditions, adult removal times corresponded to midway through the protonymphal stage, end of protonymphal stage, and end of deutonymphal stages, respectively, tbr predators developing at a normal rate (Arodokoun et at., unpublished data). Two diffcrent "adult absent" controis were (l) immaturcs provided with live E occidentalis larvae (live prey treatment), and (2) immatures with thrips larvae freshly killed by crushing the head with a pin (dead prey treatment). The effect of treatment was tested for by estimating development time and percent survival to adult stage. The development considered was from the protonymphal molt to the adult molt. Starting on the 3rd day after eggs had been laid, arenas were checked every 4 h and the time of the protonymphal molt was recorded (+ 2 h). Newly molted larvae were then isolated and randomly assigncd to each of the five treatments. Gravid female A. cucumeris were then transferred to
444
C. CLOUTIER AND S. G, JOHNSON
arenas assigned to "adult present" treatments. Ten newly hatched thrips larvae (whitish colored larvae with no evidence of food in digestive tract) were transferred to each experimental arena, except to those assigned to the "dead prey" treatment which each received ten newly hatched and freshly killed thrips larvae. Observations and replacement of all live and dead prey were made every 24 h during the experiment which lasted until all immatures had completed the deutonymph stage or died. As the adult molt approached, arenas were checked every 8 h for determination of molting time (+ 4 h). Survival and number of live thrips killed were recorded, and any eggs laid by the adult were removed, at each observation. Mites found trapped in agar or in water were counted as escaped, and mites reaching the adult stage were sexed.
Data analysis Categorical data (predator present or escaped; dead or alive) were submitted to contingency table analyses. Differences between treatments were tested for significance using chi-square statistics (Sokal an Rohlf, 1981). Continuous variables and counts (developmental time, number of prey consumed) were submitted to 1-way or 2-way analyses of variance, followed by mean comparisons using least significant difference tests (Sokal and Rohlt, 1981 ). RESULTS
The survival to adulthood was significantly affected by treatment (Table 1). Survival was high (>95%), except in the treatment where nymphs only had access to live prey as food, which resulted in 15% mortality (three of 20 predators, Table 1). The other treatment where mortality was recorded was the "prey + adult 1 d" treatment (ca. 5 % mortality). Similarly, mite escape was observed in the "prey alive" and "prey + adult 1 d" treatments.
TABLE 1 Data classified by treatment ! and mite fate for Ambtyseius cucumeris reared during nymphal devclopment at 25°C with FranklinieUa occMentalis as prey (N is number of individuals rcared; "'dead" were mites found on leaf disk; "'escaped" were missing mites or those found trapped in agar or water). Treatment
N
Alive
(females)
Dead
Escaped
Live prey Prey + adult 1 day Prey + adult 2 days Prey + adult 3 days Dead prey
27 24 21 24 22
17 20 21 24 22
(6) (12) (t4) ( I 1) (15)
3 1 0 0 0
7 3 0 0 0
IChi-square= 26.0, P~---O.001 for the effect of treatment on survival (P value approximate because .some observed frequencies are equal to zero).
INTERACTION BE'I'WEENLIFE STAGES IN A PHYTOSEIIDPREDATOR
445
Nymphal development time of predators that did survive did not vary significantly between the sexes but was strongly affected by treatment (Table 2). Treatments were thus compared using pooled data for both sexes, to reveal that nymphal development was significantly longer for predators reared alone on live prey than those with an adult for 1-3 days, or those supplied with dead prey. Development was also significantly longer for predators reared for just 1 day with an adult, compared to those with an adult for a longer period. Prey mortality varied significantly with treatment (Table 3). Nymphs surviving to adulthood alone with live prey killed a total of 5-6 prey during their average 6 day development, compared to a combined kill of 13 prey when an adult was prcsent for just one day during early protonymph',d development, and 24 prey when the adult was present for 3 days.
TABLE2 Nymphal development times (days) of Amblyseius cucumeris at 25cC under various rearing treatments with Frankliniella occidentalis larvae as prey (N is number of mites reared to adult stage; SE is standard error of mean). Sexes combined Treatment
:V
Mean
SE
Live prey Prey + adult 1 day Prey + adult 2 days Prey + adult 3 days Dead prey
17 20 21 24 22
6.34 4.27 3.05 2.81 2.82
0.60 1.82 0.49 0.37 0.45
a b c c c
Male
Female
6.15 4.96 2.81 2.65 2.80
6.75 3.80 3.18 2.99 2.83
1two-way ANOVA results for the effects of sex and treatment are F 1,94=0.02, P--0.88 I scx) and [;4,94=23.9, P~_0.0001 (treatment); pooled means with same letter are not significantly different at 5% level, as compared using the least significant difference test.
TABLE 3 Prey consumption by AnUSlvseius cucumeris at 25°C under various rearing treatments I with Frankliniella occidentalis larvae as prey (N is number of immatures reared; SE is standard error of mean). Treatment
N
Mean
SE
Prey Prey Prey Prey
21 25 20 24
5.5 13.2 19.4 24.5
0.81 0.89 0.61 0.98
alive ÷ adult 1 day + adult 2 days + adult 3 days
lOne-way ANOVA results for the effect of treatment are F3,89=89.8, P~_0.0001 ; means are all significantly different from each other at 5% level, as compared using the least significant difference test.
446
t?. CLOUTIER AND S. G. JOHNSON
DISCUSSION
The above results confirm previous observations made by Gillespie and Ramey (1989), Sengonca and Bendiek (1988) and Johnson (1990) about the relative inefficiency of A. cucumeris as a predator of F. occidentalis. Nymphal survival was reduced significantly when immatures only had access to live prey, whereas no mortality was observed with dead prey. Escape incidence followed a similar pattern (Table 1), suggesting that mites confined with live thrips dispersed in search of food. Nymphs clearly have difficulty capturing and/or killing live larvae of E occidentalis. This is also supported by development time data. For both male and female predators, those that survived by preying as young nymphs on live thrips took significantly longer to develop than those with an adult for 1, 2 or 3 days. We extend the previous observations by establishing that A. cucumeris nymphs become independent predators of small E occidentalis larvae about midway through the protonymphal stage.Variation in development time with respect to the fraction of development during which an adult was present indicates that it is early protonymphs that have great difficulty in capturing their own prey (Table 2). Young predators were clearly inefficient during the early protonymphal stage, because adult removal "after only ! d in the arena resulted in significantly longer development than later adult removal. Adult removal alter 2-3 days no longer had an effect on development time, indicating self-sufficiency roughly one-third through nymphal development. The main significance of our results is to illustrate how adult-nymph interactions in a phytoseiid predator could play a role in survival and development of the small stages on unusual prey, through the preying activities of the larger and more efficient adult predator. Considering that A. cucumeris survival was reduced and development was longer with live prey, and that these negative effects were absent with dead prey, it is evident that it is through the supplying of food as captured and killed prey, that the adult was beneficial. Predation data indicate that nymphs surviving alone on live prey could complete development by killing 5-6 prey, while taking 6 days on average to develop, i.e. twice as long as predators given freshly killed thrips. With a combined predation rate for the adult plus immature of around 8 kills/day, and a maximum rate for the immature alone of about 2 kills/day (Fig. 1), the young nymph in fact had many opportunities to feed on prey captured by the adult. This is supported by casual observations of adults and nymphs feeding concurrently on dead thrips. Phytoseiids are thought to be under strong selection for traits that favor rapid population increase to achieve maximal production of dispersers, an evolutionary consequence of their dependence on ephemeral spider mite patches (Sabelis, 1985a). Notwithstanding the high costs of dispersion, this pattern should be selected for if the habitat is normally destroyed alter a spider mite infestation. However, if phytoseiids control their spider mite prey under the host plant's carrying capacity,
INTERACTION
BE'I'WEEN
I.I|;E
STAGES
IN A PHYTOSEIID
PRI'~DAI'OR
447
--El--
NO A D U L T
- - -L~-- -
ADULT 2 d
---O---
ADULTld
~
ADULT3d
10
A
PREY KILLED
== z 0
2
4
I Z
6
""
8
........
b. . . . . . . . .
B
_o
10 J
r--
F--
l-n" O 0.5
• -:
,--i
.
12
. . . . .
ADULTS
-j-~
el
O Ptel
0
i
0
2
4
6
8
i
10
t
i
l
;
12
DAYS
Fig. 1. Amblyseius cucumeris : changes with time in number of thrips prey killed (A). and proportion of nymphs becoming adults (B), for immature predators developing on cucumber leaf disks under various treatments involving the presence or absence of an adult female. Error bars represent standard error of means; final b,r s for proportions (B) vat5' between 17 and 24 individuals.
selection might be equally strong for alternative t~eeding strategies and/or other adaptations potentially allowing survival at low prey density. Our observations on A. cucumeris reveal an alternative feeding strategy that has previously attracted little or no attention. As discussed by Sabelis (!985b and references therein), cannibalism as an alternative feeding strategy is likely to appear in nymphs of specialists such as Phytoseiulus persirnilis Athias-Henriot, because of the nymphs' reduced ability to disperse successfully compared to adults. We did not specifically look for cannibalism in A. cucumeris, but adults killed few or no nymphs in our experiment, even though all available thrips prey were often found dead in arenas at the time of observation. This polyphagous predator (Burrell and McCormick, 1964) is possibly less dependent on adult dispersal as a strategy to survive at low prey dcnsity than the spccialist P persimilis. Under conditions of reduced dispersal, prey killed by adults would be more consistently available to nymphs, and this in turn should favor a lesser tendency for cannibalism to appear in A. cucumeris. Pollen feeding, an already known alternative mode of feeding for A. cucumeris, should act similarly to reduce pressure for resorting to cannibalism, although in this case without the necessity for immatures and adults to remain aggregated and interact. The relation between dispersal and adult-nymph interactions in polyphagous phytoseiids should be better "known. Factors involved could possibly be manipulated to ensure their more predictable use, particularly against alternative prey that
448
C. CI.OUTIER AND S. G. JOHNSON
probably were not involved in the evolution of the predator's lifestyle through natural selection. In releasing A. cucumeris for thrips control, factors encouraging adult foraging in the vicinity of eggs and larvac, should contribute to local population buildup. As shown by van Rijn and Sabelis (1990) pollen reduced A. cucumeris adult female emigration on cucumber plants. Providing pollen supplements could thus have an indirect (as a dispersal inhibitor for adults) as well as a direct (food) effects on nymphal survival. It would "also be important to know if characteristics of the initial age structure in micro-populations released on foliage could play a role in explaining variable establishment and impact of A. cucumeris releases against western flower thrips (e.g. Ramakcrs et aL, 1989; Bennison et al., 1990). ACKNOWLEDGEMENTS
Special thanks are due to Jacques Brodeur for useful comments and reviewing the manuscript, and to France Bauduin, Josre Charbonneau, and Louis Gdlinas for technical help, all from Laval University. This work was supported by the Canada-Quebec Agreement on Food and Agriculture Development, and the Natural Sciences and Engineering Research Council of Canada. REFERENCES Allen, W.R. and Broadbent, A.B. 1986. Transmission of tomato spotted wilt virus in Ontario greenhouses by Frankliniella occidentalis. Can. J. Plant Pathol. 8: 33-38. Bakker, F.M. and Sabelis, M.W. 1989. How lalwae ofThrips tabaci reduce the attack success of phytoseiid predators. Entomol. Exper. Appl. 50:47-5 I. Bennison, J.A., Hockland, S. and Jacobson, R. 1990. Recent developments with integrated control of thrips on cucumber in the United Kingdom. O.I.L.B. Bull. S.RO.P./W.P.R.S. 13: 19-26. Brodeur, J. and Cloutier, C. 1992. A modified leaf disk method for rearing predaceous mites (Acarina: Phytoseiidae). Phytoprotection 73: 69-72. Bmxell, R.W. and McCormick, W.J. 1964. Typhlodromus and And~lyseius (Acarina: Phytoseiidae) as predators on orchard mites. Ann. Entomol. Soc.Amer.57: 483-487. l)e Klerk, M.-L. and Ramakers, P.M.J. 1986. Monitoring population densities of the phytoseiid predator Amblyseius cucumeris and its prey after large scale introductions to control Thrips tabaci on sweet peppers, Med. Fac. Landtx)uww, Rijksuniv_ Gent. 51: 1045-1048. Gilkeson, L.A., Morewood, W.D. and Elliott, D.E. 1990. Current status of biological control of thrips in Canadian greenhouses with Amblyseius cucumeris and Orius tristicolor. O.I.L.B. Bull. S.R.OP./W.P.R.S. 13: 71--75. Gillespie, D.R. 1989. Biological control of thrips (Thysanoptera: Thripidae) on grennhouse cucumber by Amblyseius cucumeris.. Entomophaga 34: 185-192. Gillespie, D.R. and Ramey, C.A. 1989. Life history and cold storage ofAmhlyseius cucumeris. (Acarina: Phytoseiidae). J. entomol. Soc. Brit. Columbia 85:71-76. Johnson, S.G. 1990. Biology and predacious ability ofAmblyseius barkeri (Hughes) and A. cucumeris (Oudemans)(Acari: Phytoseiidae), predators of the western flower thrips, Franktiniellu occidentalis (Pergande)(Thysanoptcra: Thripidae). M.Sc. Thesis. McGill University. Mantel, W.P. 1989. Bibliography of the western ltower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). O.I.L.B. Bull. SR.O.P./W.PR.S. 13: 29-~6. Ovennecr, W.P.J. 1985. Alternative prey and other food resources. In: W. Helle and Sabelis, M.W. (Editors), Spider mites, their biology, natural enemies and control. Vol. lB. Elsevier, Amsterdam, pp. 131-139.
INTI'2RACTION BE'I'WEEN LIFE STAGES IN A PHYTOSEIID PREDATOR
449
Ramakers, P.M.J. and van Lieburg, M.J. 1982. Start of commercial production and introduction of Amblyseius mckenziei Sch. & Pr. (Acarina: Phytoseiidae) for the control of Thrips tabaci Lind. (Thysanoptera: Thfipidae) in glasshouses. Med. Fac. Landbouww. Rijksuniv. Gent. 47: 541-545. Sabelis, M.W. 1985a. Life history. Capacity for population increase. In: W. Helle and Sabelis, M.W. (Editors), Spider mites, their biology, natural enemies and control. Vol. 1B. Elsevier, Amsterdam. pp. 35-41 Sabelis, M.W. 1985b. Life history. Development. In: W. Helle and Sabelis, M.W. (Editors), Spider mites, their biology, natural enemies and control. Vol. 1B. Elsevier. Amsterdam, pp. 43-53. Sengonca, C. and Bendiek, J. 1988. Die eignung zweier raubmilbena~'ten zur biologischen bekampfung von Frankiniella occidentafis (Pergande) (Thysanoptera: Thripidae) (in German, with English abstract). Nachrichtenbl. Deut. Pflanzenschutzd. 40:171-175. Sokal, R.R.and Rohlf, F.J.. 1981. Biometry: the principles and practice of statistics in biological research. 2rid edition. Freeman. New York, 859 pp. Steiner, M.Y. and Tellier, A.J. 1990. Western Flower thrips. Franklmiella occidemalis (Pergande), in greenhouse cucumbers in Alberta, Canada. O.I.L.B. Bull. S.R.O.P./W.P.R.S. 13: 202-205. van der Hoeven, W.A.D. and van Rijn, P.C.J.. 1990. Factors affecting the attack success of predatory mites on thrips larvae. Proc. exper. & appl. Entomol. N E. V. Amsterdam. 1: 25-30. van Rijn, P.C.J. and Sabelis, M.W. 1990. Pollen availability and its effect on the maintenance of populations ofAmblyseius cucumeris, a predator of thrips. Med. Fac. Landbouww. Rijksuniv. Gent. 55: 335-341. van Rijn, P.C.J. and van Houten, Y.M. 1990. Life history ofAmblyseius cucumeris and A. barkeri (Acarina: Phytoseiidae) on a diet of pollen. In: Proc. 8th Int. Congr. Acarol. (in press).
