On Diaphorina Citri (Hemiptera: Psyllidae) at Different Temperatures

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Life Table of Tamarixia radiata (Hymenoptera: Eulophidae) on Diaphorina citri (Hemiptera: Psyllidae) at Different Temperatures Author(s): Mariuxi Lorena Gómez-Torres, Dori Edson Nava, and José Roberto Postali Parra Source: Journal of Economic Entomology, 105(2):338-343. 2012. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/EC11280 URL: http://www.bioone.org/doi/full/10.1603/EC11280

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. BIOLOGICAL AND MICROBIAL CONTROL Life Table of Tamarixia radiata (Hymenoptera: Eulophidae) on Diaphorina citri (Hemiptera: Psyllidae) at Different Temperatures

MARIUXI LORENA GO´ MEZ-TORRES,1 DORI EDSON NAVA,2 1 AND JOSE´ ROBERTO POSTALI PARRA

J. Econ. Entomol. 105(2): 338Ð343 (2012); DOI: http://dx.doi.org/10.1603/EC11280 ABSTRACT Tamarixia radiata (Waterston, 1922) is the main parasitoid of Diaphorina citri (Ku- wayama, 1907), and has been used in classical biological control programs in several countries. The current study investigated the biology and determined the fertility life table of T. radiata in different temperatures, to obtain information to support the establishment of a biological control program for D. citri in Brazil. Fifth-instar nymphs of D. citri were offered to females of T. radiata for parasitism, for 24 h. Then, the parasitoid was removed and the nymphs were placed in incubators at 15, 20, 25, 30, or 35 Ϯ 1ЊC, 70 Ϯ 10% RH, and a 14-h photophase. The percentages of parasitism and emergence, the sex ratio, and the preimaginal period of T. radiata were determined. The fertility life table was developed from the biological data. The highest parasitism rate (77.24%) was obtained at a temperature of 26.3ЊC, and the lowest parasitism rates occurred at 15 and 35ЊC (23.1 and 40.2%, respectively). The highest percentages of emergence of the parasitoid occurred at 25, 30, and 35ЊC (86.7, 88.3, and 78.8%, respectively), with the calculated peak at 30.8ЊC (89.90%). The duration of the preimaginal developmental period for both females and males of T. radiata was inversely proportional to temperature in the thermal range of 15Ð35ЊC. The development of T. radiata occurred at all temperatures studied, and the highest viability of the preimaginal period occurred at 25ЊC. The highest values of net reproductive rate and Þnite growth ratio (␭) were observed at 25ЊC, so that in each generation the population of T. radiata increased 126.79 times, higher than the values obtained at the other temperatures.

KEY WORDS citrus, parasitism, life cycle, net reproductive rate

Diaphorina citri (Kuwayama, 1907) (Hemiptera: Psyl- which had been kept below the economic threshold lidae) has been associated with citrus in Brazil since level through biological control, in accordance with the 1940s (Costa Lima 1942) and now occurs in most the principles of integrated pest management (IPM) of the country. In Brazil until 2004, insecticide control (Yamamoto and Parra 2005). The wide geographical of D. citri was carried out sporadically, that is, only distribution of D. citrus in Brazil and its potential as a when population outbreaks occurred. The only inju- vector of HLB may negatively affect citrus crops, as ries caused by the pest had been leaf curling and shoot has been reported in other countries (Fundecitrus deformation, which prevented normal growth. These 2004, Parra et al. 2010). injuries were caused by a toxin released by D. citri as Alternatives for management of D. citri are cur- it feeds on sap (Fundecitrus 2004). In 2004, Huang- rently being studied, and include biological control longbing (HLB), also known as citrus greening patho- with Tamarixia radiata (Waterston, 1922) (Hymenop- gen, was Þrst detected in Brazil, speciÞcally in citrus tera: Eulophidae). T. radiata is an idiobiont ectopara- groves in the state of Saõ Paulo, and D. citri was sitoid that has been used in classical biological control identiÞed as the vector of the disease (Teixeira et al. programs, signiÞcantly reducing D. citri populations in 2005). several parts of the world (Aubert and Quilici 1984, Insecticide control of D. citri became the principal Chien and Chu 1996, E´ tienne et al. 2001, Hoy and strategy for HLB management in orchards in Brazil. Nguyen 2000, Skelley and Hoy 2004). The consequent frequent use of insecticides has In Brazil, T. radiata was Þrst identiÞed in 2006 in the caused a series of problems, including the destruction state of Saõ Paulo (Go´mez Torres et al. 2006). How- of the natural enemies of other major citrus pests, ever, T. radiata is not found in all regions of Brazil, and the parasitism rate is highly variable. 1 Departamento de Entomologia e Acarologia, Escola Superior de The success of a biological control program depends Agricultura “Luiz de Queiroz”, Universidade de Saõ Paulo, 13418-900, on factors that affect the Þeld efÞciency of organisms Piracicaba, Saõ Paulo, Brazil. raised under laboratory conditions (Bigler 1986). Cli- 2 Corresponding author: Laborato´rio de Entomologia, Embrapa Clima Temperado, 96001-970, Pelotas, Rio Grande do Sul, Brazil mate is probably the most important of these factors, (e-mail: [email protected]). given that a complex set of meteorological variables

0022-0493/12/0338Ð0343$04.00/0 ᭧ 2012 Entomological Society of America April 2012 GO´ MEZ-TORRES ET AL.: LIFE TABLE OF T. radiata 339 affects the development, emergence, survival, activity, Development of T. radiata on D. citri at Different and fecundity of the parasitoids released; temperature Temperatures. Recently emerged females and males and relative humidity are the most inßuential factors of T. radiata were left for 24 h in cages measuring 60 ϫ (King et al. 1985, Fauvergue and Quilici 1991). A life 50 ϫ 50 ϫ 52 cm, to mate. During this period the table is extremely useful for understanding the pop- insects were fed with a mixture of pure honey and ulation dynamics of the target species, because it pollen (Chien et al. 1994), provided on small plates in provides an integrated view of the biological charac- the upper part of the cage, which was made of glass. teristics of a given population under deÞned environ- Afterwards, the females were placed in individual mental conditions, as well as showing the develop- cages consisting of plastic cylinders (15.5 ϫ 5.5 cm), ment rate, longevity, and fecundity, all of which are with their openings covered with voile for ventilation. expressed in terms of population means (Coppel and Each female T. radiata was offered a myrtle plant with Mertins 1977, Silveira Neto et al. 1976). 30 Þfth-instar nymphs of D. citri, according to Chu and The objective of the current study was to investigate Chien (1991) (Gomez-Torres, 2009). Parasitism was the biology of T. radiata and to construct life tables at allowed for 24 h, in incubators at temperatures of 15, Ϯ Њ Ϯ different temperatures, to determine the possible im- 20, 25, 30, and 35 1 C, RH 70 10%, and a 14-h pacts of this factor on parasitism, emergence, devel- photophase. After, the female was removed from the ϫ opment, and the growth potential of the population of cage with the use of a glass tube (12 75 mm), and this parasitoid, envisaging its mass production. This the parasitized nymphs of D. citri were maintained in study will contribute to the establishment of a biolog- the same temperatures until the adults emerged. ical control program for D. citri, as a component of For each of the temperatures (treatment), four rep- IPM in different citrus-growing regions of Brazil. licates were used, each consisting of Þve myrtle plants with 30 nymphs, totaling 150 nymphs/replicate and 600 nymphs/treatment. The following biological parameters were evaluated: percentage of parasitism, Materials and Methods duration of the preimaginal (egg-adult) period, per- We collected adults of D. citri and T. radiata from centage of emergence, and sex ratio. The percentage of parasitism was determined on the Þfth day after the citrus groves in the state of Sa˜o Paulo. The insect populations were maintained at the Insect Biology nymphs were offered to the parasitoids, evaluating the formation of mummies. The sex ratio was deÞned as Laboratory of the Department of Entomology and the number of females divided by the total number of Acarology of the Luiz de Queiroz School of Agricul- individuals. ture, University of Sa˜o Paulo, Piracicaba. Life Table of T. radiata at Different Temperatures. Rearing D. citri. D. citri was reared by a technique Ten pairs of 24-h-old individuals, fed with pure honey adapted from those proposed by Skelley and Hoy and pollen (Chien et al. 1994), were placed in indi- (2004) and Nava et al. (2007). We used seedlings of vidual cylindrical plastic cages (15.5 ϫ 5.5 cm) with the orange jasmine Murraya paniculata (L.) Jack, the openings covered with voile (for ventilation). To 25Ð30 cm in height. The plants were grown in a sub- each female parasitoid, 30 Þfth-instar nymphs of D. strate of vermiculite and compost (1:1), and main- Ϯ Њ Ϯ citri reared on myrtle plants were offered daily. After tained in a incubators (30 1 C, 60 10% RH, and a 24 h, the plants containing the parasitized nymphs 14-h photophase), until new shoots emerged. No pes- were placed in climate-controlled chambers main- ticides were used. The plants were then transferred to Ϯ ϫ ϫ tained at the temperatures of 15, 20, 25, 30, and 35 acrylic cages (34 34 40 cm) containing adult D. 1ЊC, 70 Ϯ 10% RH, and 14-h photophase. Longevity citri females, from which eggs were collected for up to and fecundity were evaluated daily; fecundity was 5 d. After the eggs were laid, the nymphs were trans- determined on the Þfth day after parasitism, based on ϫ ϫ ferred to rearing cages (70 50 50 cm) and main- the number of mummiÞed nymphs. Ϯ Њ Ϯ tained in a incubators (25 1 C, 70 10% RH, and a Each treatment (temperature) consisted of ten rep- 14-h photophase). licates (pairs), and the adults were observed daily Rearing T. radiata. To rear T. radiata, we used until they died. Subsequently, we calculated the mean fourth- and Þfth-instar D. citri (Chu and Chien 1991, number of parasitized nymphs per female (mx) on Skelley and Hoy 2004). T. radiata populations were each date of parasitism (x), based on the total number maintained in rearing cages measuring 60 ϫ 50 ϫ 52 of females, the cumulative survival rate of females (lx) cm, in a incubators (25 Ϯ 1ЊC, 70 Ϯ 10% RH, and a 14-h during the oviposition period, and the number of de- photophase). Fourth- and Þfth-instar D. citri nymphs, scendants that survived to age x. The survival- and which remained attached to the plants, were parasit- fecundity-related data were summarized in a life table, ized by T. radiata for a period of 24 h in cages mea- in accordance with the model proposed by Maia et al. suring 45 ϫ 35 ϫ 37 cm. The nymphs were then (2000). We calculated the net reproductive rate, the transferred, together with the plants, to rearing units, estimated intrinsic rate of increase, the (observed) where they remained for the duration of the preima- intrinsic rate of increase, the interval between gener- ginal period. After the adults emerged, we collected ations, and the Þnite rate of increase using the equa- 80% of them for use in the experiments, leaving the tions from Southwood (1978). remaining adults in the rearing units for use in rearing Statistical Analysis. To determine the relationship and maintaining additional T. radiata populations. between temperature and the percentages of parasit- 340 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 2

Fig. 2. Preimaginal female (A) and male (B) development time for T. radiata on D. citri at temperatures of 15, 20, 25, 30, and 35 Ϯ 1ЊC, 70 Ϯ 10% RH, and 14 h photophase.

Fig. 1. Rate of parasitism (A) and emergence (B) of T. radiata on D. citri at temperatures of 15, 20, 25, 30, and 35 Ϯ was inversely proportional to temperature for both 1ЊC, 70 Ϯ 10% RH, and a 14 h photophase. females (F ϭ 191.21; P Ͻ 0.01) and males (F ϭ 82.02; P Ͻ 0.01) (Fig. 2A, B). For females of T. radiata, the ism, emergence, and the duration of the preimaginal duration varied from 489.60 h at 15ЊC to 247.20 h at period, the data were analyzed by the nonlinear poly- 35ЊC; for males, the duration varied from 343.20 h at nomial Þt model. For the sex ratio, the data were 15ЊC to 146.40 h at 35ЊC. This demonstrated that the submitted to analysis of variance (ANOVA), and the preimaginal development period of the males is more means were compared by Tukey test (P Յ 0.05). The rapid than the females. That is, within the tempera- life table parameters and their respective standard ture range studied (15Ð35ЊC), for each degree-centi- errors were estimated according to the method pro- grade increase in temperature, there was a reduction posed by Meyer et al. (1986). The means were com- in the development period of Ϸ10 h for males and 13 h pared by the two-tailed StudentÕs t-test (P Յ 0.06) with for females (Fig. 2A, B). the lifetable.sas Þles (Maia et al. 2000). The analyses Fertility Life Table. The mean duration of one gen- were carried out with the use of the program SAS eration (T) varied with the temperatures in which the (Statistical Analysis System), version 9.2, 2002Ð2008 parasitoid developed. The variation was from 10.43 d (SAS Institute, Inc., Cary, NC). at 35ЊC to 20.32 d at 15ЊC (Table 1). The net reproduction rate (Ro) differed signiÞcantly as a function of temperature, with the highest fecundity at 25ЊC, Results 12.83 times higher than the lowest Ro, obtained at 15ЊC Biology. Temperature inßuenced the rates of both (Table 1). ϭ Ͻ ϭ parasitism and emergence (F 92.20, P 0.01; and F All the values of the intrinsic rate of increase (rm) 25.29, P Ͻ 0.01, respectively) (Fig. 1A, B). The para- were positive, indicating an increase in population sitism rate was highest at the temperatures of 25 and at the temperatures evaluated; this parameter varied 30ЊC, corresponding to 85.50 and 72.80%, respectively. from 0.1828 to 0.3742, and was highest at 25ЊC. For At 15 and 35ЊC the parasitism rates were 23.1 and the Þnite rate of increase (␭), the values obtained 40.2%, respectively. The optimum temperature at at 25ЊC was the biggest and differ from the other which the highest parasitism occurred was 26.3ЊC, values (Table 1). The maximum rate of increase which corresponded to the predicted value of 77.26% varied in concordance with the previous results, parasitism. For emergence, the highest percentages according to temperature, with the Þrst peaks at the occurred at the temperatures of 25, 30, and 35ЊC, temperatures of 25, 30, and 35ЊC, and was more varying from 88.30 to 78.80%, with the estimated max- delayed at 15 and 20ЊC (Fig. 3). These values are imum at 30.8ЊC with an emergence of 84.91%. The directly correlated with the duration of the insectÕs lowest emergence rates were recorded at 15 and 20ЊC cycle, because the cycle was shortest at 35ЊC and (Fig. 1). Temperature had no signiÞcant effect on prolonged at 15ЊC (Table 1). temperature, with P values below 0.5 (F ϭ 1.731; df ϭ The net reproduction rate (Ro) was highest at 25ЊC, 4; P ϭ 0.196). because in each generation the population of T. radi- The mean duration of the preimaginal developmen- ata will increase 126.79 times, more than the rates tal period of T. radiata on Þfth-instar nymphs of D. citri obtained at the other temperatures (Table 1). April 2012 GO´ MEZ-TORRES ET AL.: LIFE TABLE OF T. radiata 341

Table 1. Characteristics of T. adiata reared at various temperatures, under controlled conditions (relative humidity 70 ؎ 10% and a 14 h photophase)

Њ ␭ Temp ( C) T (days) Ro rm 15 20.32 Ϯ 0.24a 9.88 Ϯ 1.05d 0.1826 Ϯ 0.008d 1.2003 Ϯ 0.010d 20 18.84 Ϯ 0.12ab 23.62 Ϯ 2.48c 0.2531 Ϯ 0.013c 1.288 Ϯ 0.016c 25 15.53 Ϯ 0.21bc 126.79 Ϯ 6.25a 0.3742 Ϯ 0.002a 1.4538 Ϯ 0.004a 30 11.78 Ϯ 0.13c 58.63 Ϯ 3.23b 0.3378 Ϯ 0.002b 1.4019 Ϯ 0.012b 35 10.43 Ϯ 0.35c 21.27 Ϯ 2.01c 0.2528 Ϯ 0.009c 1.2889 Ϯ 0.014c

␭ T, mean generation time; Ro, net reproductive rate; rm, intrinsic rate of increase; , Þnite rate of increase. Values followed by the same lower-case letter are not signiÞcantly different, as assessed by two-tailed StudentÕs t-test (P Յ 0.06).

Discussion radiata in laboratory conditions at 25ЊC, 100% RH, and a 14-h photophase. In this context and taking as a The results obtained in this study demonstrate that reference that the mean annual temperature in the the development of T. radiata is inßuenced by tem- Њ perature, showing that 25ЊC is the optimum temper- state of Sa˜o Paulo oscillates between 20 and 25 C, it is ature for growth of this parasitoid, and is where the important to note that the results obtained in the highest reproduction rate occurs, although the point current study, at the temperatures of 15, 20, 25, 30, and of maximum emergence is close to 30ЊC. 35ЊC, provide basic information for better understand- The values of parasitism, emergence, and sex ratio ing of the dynamics and performance of T. radiata in observed in this study are similar to those obtained by citrus-growing regions of Sa˜o Paulo. Similar results Chu and Chien (1991), who studied the biology of T. have been obtained for other species of the family

Fig. 3. Age-speciÞc survival rate (lx) and age-speciÞc fecundity (mx) for T. radiata on D. citri at temperatures of 15, 20, 25, 30, and 35 Ϯ 1ЊC, 70 Ϯ 10% RH, and 14 h photophase. 342 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 2

Eulophidae. According to Wang et al. (1999), tem- A complex set of meteorological variables can affect peratures ranging from 20 to 30ЊC favor the develop- the development, emergence, survival, activity, and ment, survival, and reproduction of members of Eu- fecundity of T. radiata. Among these variables, tem- lophidae. Although parasitism occurs at high perature occupies a prominent position, because it has temperatures, the emergence rate decreases drasti- a direct inßuence on these parasitoids. cally at temperatures above 32.5ЊC. In contrast, the The information obtained in the current study fa- parasitoids do not emerge at 15ЊC. Those authors cilitates the understanding of the inßuence of tem- found that the number of hosts parasitized by eu- perature on the physiological and ethological param- lophid females, and the eulophid fertility rates were eters studied. These data will allow laboratory rearing higher at 25ЊC than at other temperatures studied, a of T. radiata as well as its release in the Þeld, thus similar Þnding to our observations for T. radiata. making it possible to deploy an additional strategy to Hondo et al. (2006) evaluated, on the basis of ther- manage D. citri at the different times of year, as well mal tolerance, the development, efÞciency, and re- as its eventual establishment as another tactic among production of seven species of the family Eulophidae the measures to be applied in the different climate and concluded that all the species were adapted to regions of Brazil for the control of HLB in citrus- high temperatures, their reproductive capacity de- growing areas. creasing in the 15Ð20ЊC range. Our Þndings regarding T. radiata show that it is important to evaluate thermal Acknowledgments tolerance, particularly in relation to the effects on development and reproduction, before choosing a bi- We are grateful to FAPESP for granting a doctoral fel- ological control agent for a given pest. lowship to the Þrst author (Process: 05/59769-5), to Marineía Minkenberg (1989), Bazzocchi et al. (2003), and L. Haddad (ESALQÐUSP), and to Antonio Gidoni and Ri- cardo Valgas (EMBRAPA) for their help with the statistical Duale (2005) also reported that temperature inßu- analyses and the INCTÐSemioquõ´micos na Agricultura. This ences the rate at which Eulophidae develop. How- work was funded by the Fundaçaõ de Amparo a` Pesquisa do ever, the Þndings of the current study have more in Estado de Saõ Paulo (FAPESP) and the Conselho Nacional common with those obtained by Chu and Chien de Desenvolvimento Cientõ´Þco e Tecnolo´gico (CNPq), and (1991), who studied T. radiata under similar condi- to Janet Reid (JWR ASSOCIATES) for the English revisions. tions. Chu and Chien reported an interval between generations of 17.8 d, a net reproductive rate of 285 References Cited female offspring/female, an intrinsic rate of increase of 0.31, and a Þnite rate of increase of 1.37. Acosta, N. M., and R. J. O’Neil. 1999. Life history charac- Other studies involving Eulophidae have under- teristics of three populations of Edovum puttleri Grissell scored the importance of temperature for develop- (Hymenoptera: Eulophidae) at three temperatures. Biol. ment and reproduction (Acosta and OÕNeil 1999, Cas- Control 16: 81Ð87. Aubert, B., and S. Quilici. 1984. 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