ECOLOGY AND POPULATION BIOLOGY Host Plant and Temperature Effects on Lysiphlebus testaceipes (: Aphidiidae), a Native Parasitoid of the Exotic Brown Citrus (Homoptera: Aphididae)

1 2, 3 A. A. WEATHERSBEE III, C. L. MCKENZIE, AND Y. Q. TANG

USDAÐARS, U.S. Horticultural Research Laboratory, 2001 South Rock Rd., Fort Pierce, FL 34945

Ann. Entomol. Soc. Am. 97(3): 476Ð480 (2004) ABSTRACT The brown citrus aphid, Toxoptera citricida (Kirkaldy), is an exotic pest of citrus in the United States that was introduced into Florida in 1995. The native parasitoid Lysiphlebus testaceipes (Cresson) has demonstrated acceptance of the brown citrus aphid as a host. This experiment evaluated the effect of citrus host plants on brown citrus aphid parasitism by L. testaceipes, and the effect of temperature on development of the parasitoid. The levels of parasitism achieved by L. testaceipes were similar among brown citrus aphid populations on Þve citrus cultivars used as host plants for the (range 34Ð36%). The percentage of adult parasitoid emergence was highest on ÔDuncan grapefruitÕ (82%) and signiÞcantly lower on ÔMexican limeÕ (63%) than on any of the other citrus cultivars. The proportion of adults that were female was signiÞcantly higher on ÔDuncan grapefruitÕ (81%) than on any of the other cultivars. The results demonstrate that the effects of multiple trophic levels can inßuence parasitoid performance in a cascading manner. The developmental periods for both male and female L. testaceipes on the brown citrus aphid declined from 21 to 9 d with ascending temper- atures in the range 18Ð27ЊC. The developmental threshold was 10.4ЊC and the degree-day (DD) requirement for development was 158.7 DD, indicating that the temperature conditions experienced in Florida are conducive to rapid development of L. testaceipes on the brown citrus aphid.

KEY WORDS Toxoptera citricida, biological control, citrus, multitrophic

THE BROWN CITRUS APHID, Toxoptera citricida ducing high rates of parasitism and adult emergence (Kirkaldy), is an exotic pest of citrus in the United on this host (Tang et al. 2002, Weathersbee et al. 2004). States that was Þrst detected in Florida in 1995 (Hal- Although the brown citrus aphid was once considered bert and Brown 1996). This exotic aphid species is the a poor host for this parasitoid (Yokomi and Tang predominant vector of citrus tristeza virus, a devas- 1996), currently L. testaceipes is the most common tating disease agent of citrus causing great concern in primary parasitoid collected from Þeld populations of the industry (Yokomi et al. 1994). Biological control this aphid in Florida (Weathersbee et al. 2004). The efforts directed against the brown citrus aphid have generalist behavior of L. testaceipes with regard to host included releases of parasitoids imported from regions selection (Stary 1993, Gonzales et al. 2002) may have where the aphid has been long-established (Denmark facilitated exploitation of this new aphid species. The and Porter 1973, Evans and Stange 1997, Hoy and apparent adaptation of brown citrus aphid as a host by Nguyen 2000, Hill and Hoy 2002, Liu and Tsai 2002). L. testaceipes may also have been accelerated due to Indigenous natural enemies also have been evaluated the extensive citrus monoculture present in the re- and exploited for potential biological control activity gion. against this exotic pest (Michaud 1999, 2000, 2001; Several factors may inßuence the rate of parasitism Belliure and Michaud 2001). The native parasitoid and subsequent development of L. testaceipes on Lysiphlebus testaceipes (Cresson) has demonstrated brown citrus aphid. Both citrus host plant and tem- acceptance of brown citrus aphid as a host and has perature can affect the rate of development and lon- been selectively adapted in the laboratory, thus pro- gevity of the brown citrus aphid (Tsai 1998, Tang et al. 1999). Such environmental effects on the host aphid Mention of a trademark or proprietary product does not constitute also would be expected to impact the Þtness of the a guarantee or warranty of the product by the U.S. Department of parasitoid in a cascading manner (Price et al. 1980). In Agriculture and does not imply its approval to the exclusion of other particular, the levels of nutrients and secondary com- products that may also be suitable. pounds present in plants can inßuence the quality of 1 E-mail: [email protected]. 2 Biological Control Research Institute, Fujian Agricultural Uni- herbivorous (second trophic level) as hosts for versity, Fuzhou, China. parasitoids (third trophic level) (Turlings and Benrey 3 Current address: 3717 Pickwick Dr., Orlando, FL 32817. 1998). For example, parasitism of the mealybug May 2004 WEATHERSBEE ET AL.: ENVIRONMENTAL EFFECTS ON DEVELOPMENT OF L. testaceipes 477

Phenacoccus manihoti Matile-Ferrero by the parasitoid Five citrus cultivars were used in the experiments, Apoanagyrus lospzi De Santis was inßuenced by host including seedlings of ÔSour orangeÕ; ÔCarrizo citrangeÕ; plant type, and parasitoid emergence was lowest from ÔDuncan grapefruitÕ, Citrus paradisi Macf.; ÔPineapple mealybugs reared on the most resistant cassava culti- sweet orangeÕ, Citrus sinensis (L.); and ÔMexican limeÕ, var (Souissi and Le Ru 1998). Additionally, Teder and Citrus aurantifolia (Christm.). The seedlings (12Ð15 Tammaru (2002) reported positive correlations be- cm in height and Ͻ1 yr old) of each citrus cultivar tween vigor of the host plant (cattail, Typha latifolia were grown in 140-cm3 containers with potting soil L.) and the pupal weights of the two noctuid herbi- (Metromix 500, Scotts, Marysville, OH). vores Nonagria typhae Thunberg and Archanara spar- Effect of Host Plant on Parasitoid Success. Brown ganii Esper. They further indicated that the adult citrus aphids were reared on the Þve citrus cultivars weights of three ichneumonid parasitoids, Exephanes described above and exposed to L. testaceipes to de- occupator Gravenhorst, Spilichneumon limnophilis termine whether host plant affected the degree of Thomson, and Chasmias paludator Desvignes, func- parasitism, survival of parasitoids to the adult stage, tioning at the third trophic level, were dependent on and female parasitoid emergence. Single plants of the vigor of the plants and herbivores repre- each citrus cultivar containing young foliage were senting the lower trophic levels. infested initially with 20Ð30 brown citrus aphid adults. Before the anticipated arrival of the brown citrus Aphid populations were allowed to increase to 300Ð aphid in Florida, Tang and Yokomi (1995) used a 500 of the second and third instars per plant. The aerial related indigenous species, the black citrus aphid, Tox- portions of each plant were caged in 1-liter clear optera aurantii (Boyer de Fonscolombe), as a host to plastic containers with screened lids afÞxed by elastic study the temperature-dependent development of L. bands. A 1-cm-diameter opening was cut in the side of testaceipes and other potential brown citrus aphid each container to provide access for parasitoid intro- parasitoids. They determined that L. testaceipes had a ductions. Parasitoids were used in the experiment Յ12 shorter developmental period, albeit a lower thermal h after emergence, without regard for prior mating or tolerance, than either of two aphelinid species, Aph- oviposition experience. Ten pairs of adult parasitoids elinus gossypii Timberlake and Aphelinus spiraecolae were added to each caged plant containing aphids for Evans & Schauff, on the black citrus aphid. The cur- a period of 24 h and then removed. All treatments were rent research evaluates the effect of citrus host plant replicated four times and maintained in a growth on the parasitism rate and adult emergence of L. testa- chamber at 25 Ϯ 0.1ЊC and a photoperiod of 14:10 ceipes on brown citrus aphid and the effect of tem- (L:D) h. Aphid mummies that formed on each caged perature on development of this parasitoid within the plant were collected, returned to the growth chamber, host. Differences in observed developmental periods and monitored daily for adult parasitoid emergence. for L. testaceipes have been attributed to genetic vari- Adult parasitoids that emerged were sexed using a ability among distinct populations and differences in stereomicroscope. The numbers of aphids, aphid the host aphid species (Stary et al. 1988, Tang and mummies, and emerged male and female adult para- Yokomi 1995). Identifying the factors that regulate sitoids were counted for each treatment. interactions between L. testaceipes and the brown cit- Effect of Temperature on Parasitoid Development. rus aphid will improve conservation and augmentation Brown citrus aphids were reared on seedlings of ÔCar- efforts for this indigenous biological control agent. rizo citrangeÕ and exposed to parasitism by L. testa- Enhancing control strategies for brown citrus aphid ceipes at four constant temperatures (18, 21, 24, and through the use of natural enemies will assist in re- 27 Ϯ 0.1ЊC) to determine the effects of temperature on ducing the spread of citrus tristeza virus. the developmental rate of the parasitoid. Tang and Yokomi (1995) reported the rate of development for L. testaceipes on a related host species, the black citrus Materials and Methods aphid, was linear within this temperature range. The Insect and Plant Sources. Laboratory colonies of aerial portion of each plant, with 100Ð150 second and brown citrus aphid were maintained on young citrus third instars of brown citrus aphid, was caged as de- foliage of ÔSour orangeÕ, Citrus aurantium L., or ÔCar- scribed previously, and Þve pairs of adult parasitoids rizo citrangeÕ, Citrus sinensis (L.) Osbeck ϫ Poncirus (Յ12 h after emergence) were introduced for a period trifoliata (L.) Raf., in an air-conditioned greenhouse of 8 h and then removed. All treatments were repli- as described previously (Tang et al. 1999). The L. cated Þve times and maintained in growth chambers testaceipes colony was originally established from at the appropriate constant temperature and a pho- specimens reared from parasitized brown citrus toperiod of 14:10 (L:D) h. MummiÞed aphids were aphids collected in Orlando, FL, in 1999 (Tang et al. collected, returned to the growth chamber at the ap- 2002). Progeny from this original collection have been propriate temperature, and monitored daily for adult propagated on brown citrus aphid since then at the parasitoid emergence. Adult parasitoids were sexed U.S. Horticultural Research Laboratory (USHRL), and the developmental time (days) from oviposition Fort Pierce, FL. The numbers of L. testaceipes gener- to adult emergence was determined for males, fe- ations were recorded during the Þrst 16 mo of colony males, and pooled males plus females. maintenance between November 1999 and March Data Analysis. Percentage data for parasitism, adult 2001. Adult parasitoid emergence and sex ratios were parasitoid emergence, and female parasitoid emer- measured approximately monthly during this period. gence on Þve citrus cultivars; and data for develop- 478 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 3 mental time of the parasitoid at four constant tem- Table 1. Effect of citrus host plant on parasitism, adult emer- peratures were analyzed by the General Linear gence, and female emergence of L. testaceipes on brown citrus aphid Models procedure (SAS Institute 1999). Percentage data were transformed (arcsine) before the analyses, Mean % Ϯ SE and the untransformed means were reported in the Female Host plant Parasitized Adult data table. Differences among treatment means were emergence aphids emergence determined by StudentÐNewmanÐKeuls multiple (&/(( ϩ &)) Յ comparison at a probability level of 5% (P 0.05). ÔDuncan grapefruitÕ 35.5 Ϯ 1.0a 82.0 Ϯ 1.5a 81.0 Ϯ 1.1a The rate of parasitoid development at each constant ÔMexican limeÕ 35.0 Ϯ 0.7a 62.8 Ϯ 1.5b66.0 Ϯ 1.8b temperature was calculated as the reciprocal of de- ÔPineapple sweet orangeÕ 34.5 Ϯ 0.6a 79.3 Ϯ 3.2a 68.5 Ϯ 2.2b Ϯ Ϯ Ϯ velopmental time (1/d) from oviposition to adult ÔSour orangeÕ 35.8 1.0a 77.8 1.5a 72.5 1.7b ÔCarrizo citrangeÕ 34.0 Ϯ 0.7a 76.3 Ϯ 0.9a 71.3 Ϯ 1.9b emergence. The developmental rate was modeled for pooled adults. Linear regression was used to describe Means within a column followed by the same letter are not signif- the relationship between the rate of parasitoid devel- icantly different (P Ͼ 0.05, StudentÐNewmanÐKeuls multiple com- opment (y) and temperature (x), where y ϭ a ϩ bx parison). (SAS Institute 1999). The thermal threshold (t) for development was estimated from the x intercept, niÞcantly (P Յ 0.05) higher on ÔDuncan grapefruitÕ where t ϭϪa/b. The thermal constant (K), expressed (81%) than on any of the other cultivars (Table 1). as the developmental time in degree-days (DD), was Among the same citrus cultivars used in this exper- estimated as the reciprocal of the regression coefÞ- iment, Tang et al. (1999) found that the net repro- cient, where K ϭ 1/b (Campbell et al. 1974). ductive rate and the intrinsic rate of increase were lowest for the brown citrus aphid on ÔMexican limeÕ. Tsai (1998) reported that brown citrus aphid exhibited Results and Discussion a higher intrinsic rate of increase when reared on Parasitoid Colony Statistics. Between November grapefruit than on three other citrus and four non- 1999 and March 2001, the L. testaceipes colony was citrus host plants. Undoubtedly, the compositions and reared through 47 generations at the USHRL. Adult concentrations of nutrients and secondary substances parasitoid emergence during this period ranged from vary greatly among citrus cultivars, sometimes increas- 72.1 to 90.0%, with a mean Ϯ SE of 83.5 Ϯ 1.2% (n ϭ ing their suitability as host plants, whereas at other 18). Female emergence ranged from 52.6 to 69.6%, times conferring resistance to insect herbivores. Al- with a mean of 61.3 Ϯ 1.2%. The average generation though the compounds causing these differences have time was estimated to be Ϸ10.2 d based on the 480 d not been identiÞed speciÞcally in citrus, it is reason- required to complete 47 generations. able to assume that factors present in the plant that This estimate is similar to the developmental time of affect vigor of the host aphid also would inßuence 10.5 d reported for L. testaceipes on the black citrus Þtness of the parasitoid. In this experiment, L. testa- aphid at approximately the same temperature (Tang ceipes performed best on the citrus cultivar previously and Yokomi 1995). It is important to consider that the identiÞed most suitable for the brown citrus aphid, estimate for generation time for the USHRL colony and worst on the cultivar least suitable for the aphid may also include a short interval after adult eclosion (Tsai 1998, Tang et al. 1999). Souissi and Le Ru (1998) before oviposition is initiated. The actual develop- reported similar performance for a parasitoid of P. mental time for individuals in the USHRL colony may manihoti reared on cassava cultivars differing in levels have been shorter than the estimate for generation of insect resistance. Mounting evidence indicates that time. Additionally, temperatures in the air-condi- host plant suitability inßuences herbivore quality, tioned greenhouse, where the USHRL colony was which in turn affects parasitoid Þtness (Price et al. maintained, may not have been as consistent as those 1980; Bhatt and Singh 1989, 1991; Teder and Tammaru of the growth chamber used by Tang and Yokomi 2002). The host plant effects on L. testaceipes perfor- (1995). mance observed during this experiment indicate that Host Plant Effects. During a 24-h period, L. testa- the multitrophic interactions among commercial cit- ceipes parasitized a similar proportion of the aphid rus cultivars, the brown citrus aphid, and this native populations on each of Þve citrus cultivars used as host parasitoid should be further investigated. Whether plants (F ϭ 0.7; df ϭ 4, 12; P ϭ 0.6063) (Table 1). The differences in parasitoid emergence rates observed in proportions parasitized ranged from 33 to 38%, with an this experiment were due to plant nutritional effects overall mean Ϯ SE of 35.0 Ϯ 0.4% (n ϭ 20). Despite on the Þtness of the host aphid or to the presence of that, citrus cultivar affected the percentage of emer- plant allelochemicals ingested by the host aphid would gence of adult parasitoids (F ϭ 15.2; df ϭ 4, 12; P ϭ be an interesting aspect for further study. Although 0.0001) as well as the percentage of adults that were others have not been able to exclude the possibility female (F ϭ 10.5; df ϭ 4, 12; P ϭ 0.0007). Adult that plant nutritional effects are involved in tritrophic parasitoid emergence ranged from 82% on ÔDuncan responses, it seems more likely that the observed ef- grapefruitÕ to 63% on ÔMexican limeÕ. Emergence was fects on insect predators and parasitoids are mediated signiÞcantly (P Յ 0.05) lower on ÔMexican limeÕ than by secondary plant metabolites present in the diet of on any of the other citrus cultivars tested. The per- insect herbivores (Stamp 2001, Singer and Stireman centage of adult parasitoids that were female was sig- 2003). May 2004 WEATHERSBEE ET AL.: ENVIRONMENTAL EFFECTS ON DEVELOPMENT OF L. testaceipes 479

Table 2. Average developmental time (days) from oviposition to adult emergence of the parasitoid L. testaceipes on brown citrus aphid at four constant temperatures

(( && Pooled Temperature (( ϩ &) (ЊC) n d n d n d 18 131 20.4 Ϯ 0.2a 163 20.7 Ϯ 0.2a 294 20.6 Ϯ 0.1a 21 95 15.8 Ϯ 0.2b112 15.8 Ϯ 0.2b207 15.8 Ϯ 0.2b 24 90 12.6 Ϯ 0.2c 109 12.7 Ϯ 0.1c 199 12.6 Ϯ 0.1c 27 71 9.3 Ϯ 0.1d 120 9.3 Ϯ 0.1d 191 9.3 Ϯ 0.0d

Means within a column followed by the same letter are not signif- icantly different (P Ͼ 0.05, StudentÐNewmanÐKeuls multiple com- parison).

Temperature Effects. The developmental periods were similar for male and female L. testaceipes on brown citrus aphid over the range of temperatures tested (F ϭ 0.5; df ϭ 1, 882; P ϭ 0.4624); therefore, the data for both sexes were pooled (Table 2). The de- velopmental period for the parasitoid was inversely correlated with temperature and signiÞcantly de- Fig. 1. Relationship between temperature and develop- clined from 21 to 9 d within the temperature range mental rate of L. testaceipes on the brown citrus aphid. The Њ 18Ð27ЊC(F ϭ 1493.3; df ϭ 3, 882; P ϭ 0.0001). The thermal threshold and degree-day requirement were 10.4 C numbers of days required for the parasitoid to com- and 159.7 DD, respectively. Vertical lines denote standard Յ errors of the means and dashed lines denote 95% CL for the plete development were signiÞcantly (P 0.05) dif- equation. ferent from one another among all of the temperatures tested, indicating that variability among response data within a temperature regime was low. The data also (K), expressed as the developmental time in degree- indicate that L. testaceipes performance as a biological days, was 158.7 DD. control agent of brown citrus aphid may vary with In comparison, the thermal threshold and degree- day requirement previously reported for L. testaceipes differences in seasonal temperatures. Њ The developmental period for L. testaceipes isolates on the black citrus aphid was 7.5 C and 212.8 DD, from Nebraska, Oklahoma, and Texas on greenbug, respectively (Tang and Yokomi 1995). The combined (Rondani), was Ϸ2 d shorter thermal thresholds and degree-day requirements for Њ the Nebraska, Oklahoma, and Texas isolates of L. testa- within the temperature range 18Ð27 C (Royer et al. Њ 2001). These western populations of L. testaceipes are ceipes on greenbug were 6.2 C and 192.3 DD, respec- geographically and reproductively isolated from Flor- tively (Royer et al. 2001). The higher thermal thresh- ida populations, and differences in developmental old and lower degree-day requirement for times would be expected. The differences could be development of the current Florida population indi- caused by genetic variability among populations of the cates that this parasitoid is well adapted to regional temperature conditions and the brown citrus aphid as parasitoid (Stary et al. 1988) due to selective adapta- a host. L. testaceipes should be conserved and aug- tion to local climates, or differences in suitability of the mented as a natural enemy of brown citrus aphid. It is host aphid (Tang and Yokomi 1995). The upper range currently established in Florida and its emergence rate of temperatures in this experiment (24Ð27ЊC) is more on brown citrus aphid is comparable to that of im- representative of conditions encountered by the ported parasitoids whose establishment has not been brown citrus aphid and L. testaceipes in Florida. Within conÞrmed (Deng and Tsai 1998, Hill and Hoy 2002, Liu this upper temperature range, L. testaceipes completed and Tsai 2002). Michaud (2002) points out that fund- development on the brown citrus aphid 1 d sooner ing, scientiÞc resources, and ample time for establish- than Tang and Yokomi (1995) observed on the black ment are given to imported natural enemies, whereas citrus aphid. The brown citrus aphid may be a more the same opportunities are not afforded to potentially suitable host than the black citrus aphid for Florida adaptive native species. Perhaps expenditures for con- populations of L. testaceipes. servation and augmentation of native L. testaceipes are The relationship between temperature and devel- long overdue. opmental rate of L. testaceipes on the brown citrus aphid was described by the linear regression equation y ϭ Ð0.0654 ϩ 0.0063x (r2 ϭ 0.875, P ϭ 0.0001) (Fig. References Cited 1). The developmental rate of the parasitoid was linear Belliure, B., and J. P. Michaud. 2001. Biology and behavior within the range of temperatures used in the experi- of Pseudodorus clavatus (F.) (Diptera: Syrphidae), an ment. The thermal threshold (t) for development of important predator of citrus aphids. Ann. Entomol. Soc. the parasitoid was 10.4ЊC and the thermal constant Am. 94: 91Ð96. 480 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 3

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