Bulletin of Entomological Research (2001) 91, 477–487 DOI: 10.1079/BER2001120 Development, survival and reproduction of black citrus aphid, Toxoptera aurantii (Hemiptera: Aphididae), as a function of temperature J.J. Wang1,2 and J.H. Tsai1* 1Fort Lauderdale Research and Education Center, IFAS, University of Florida, 3205 College Avenue, Fort Lauderdale, FL 33314, USA: 2Department of Plant Protection, Southwest Agricultural University, Chongqing, 400716, People’s Republic of China Abstract The development, survival, and reproduction of the black citrus aphid Toxoptera aurantii (Boyer de Fonscolombe) were evaluated at ten constant temperatures (4, 7, 10, 15, 20, 25, 28, 30, 32 and 35°C). Development was limited at 4 and 35°C. Between 7 and 32°C, developmental periods of immature stages varied from 44.2 days at 7°C to 5.3 days at 28°C. Overall immature development required 129.9 degree-days above 3.8°C. The upper temperature thresholds of 32.3, 28.6, 29.3, 27.2, and 28.6°C were determined from a non-linear biophysical model for the development of instars 1–4 and overall immature stages, respectively. Immature survivorship varied from 82.1 to 97.7% within the temperature range of 10–30°C. However, immature survivorship was reduced to 26.3% at 7°C and 33.1% at 32°C. Mean adult longevity was the longest (44.2 days) at 15°C and the shortest (6.2 days) at 32°C. The predicted upper temperature limit for adult survivorship was at 32.3°C. Total nymph production increased from 16.3 nymphs per female at 10°C to 58.7 nymphs per female at 20°C, declining to 6.1 nymphs per female at 32°C. The estimation of lower and upper temperature limits for reproduction was at 8.2 and 32.5°C, respectively. The population reared at 28°C had the highest intrinsic rate of increase (0.394), the shortest population doubling time (1.8 days), and shortest mean generation time (9.5 days) compared with the populations reared at six other temperatures. The population reared at 20°C had the highest net reproductive rate (54.6). The theoretical lower and upper temperature limits for population development, survival and reproduction were estimated at 9.4 and 30.4°C, respectively. The biology of T. aurantii was also compared with three other citrus aphid species. Introduction citrus encompasses 347,101 planted ha with a total of 107 million trees in the 33 citrus producing counties. The annual Citrus is one of the most important economic crops in the earning on citrus is estimated at $1.1 billion (Tsai & Wang, USA with about 500,000 ha in citrus groves mostly in 1999). The economic importance of aphids in commercial California, Florida, Texas and Arizona. In Florida alone, citrus groves is seasonal and concomitant with new shoot growth on trees in cooler temperatures of spring and autumn. The major damage associated with the citrus *Author for correspondence aphids, including brown citrus aphid, Toxoptera citricida Fax: (+1) 954 475 4125 Kirkaldy, the black citrus aphid, T. aurantii (Boyer de E-mail: jhtsai@ufl.edu Fonscolombe), the melon aphid, Aphis gossypii Glover and 478 J.J. Wang and J.H. Tsai the spirea aphid, Aphis spiraecola Patch (all Hemiptera: three days throughout the study. The plants were fertilized Aphididae), however, is the transmission of citrus tristeza with a controlled release fertilizer (Osmocote, 14:14:14 virus (CTV). Citrus tristeza virus is found in most citrus- [N:P:K], Scotts, Marysville, Ohio) and watered as required. producing areas of the world and is the most economically Five apterous adult T. aurantii were transferred from stock important viral disease of citrus (Rocha-Pena et al., 1995). colonies to one seedling and were allow to reproduce for 4 h. Citrus tristeza virus is known to cause decline and death The adults and all but one new-born nymph were then primarily of citrus trees grafted on sour orange Citrus removed. The seedlings were caged with a plastic cage (7 ϫ aurantium L. (Rutaceae) rootstock, but some CTV isolates can 4.5 cm diameter with a nylon cloth top), and placed in cause stem pitting regardless of rootstock (Bar-Joseph et al., growth chambers (Percival, Boone, Iowa) at 4, 7, 10, 15, 20, 1989), and can result in long-term debilitation that reduces 25, 28, 30, 32 and 35°C, 70–90% r.h., and a photoperiod of yields of sweet orange and grapefruit from 5 to 45%. 14:10 h (L:D). Individual insects were checked twice daily Toxoptera aurantii is a polyphagous species with a for ecdysis (i.e. for life stage and developmental times) and worldwide distribution (Carver, 1978) and is reported to be a survivorship. The presence of exuviae was used to major pest of citrus in Tunisia, Italy and Peru (Talhouk, determine moulting. 1975). It is more widely distributed than T. citricida, and being more or less common with T. citricida in South Experimental procedures for adult longevity and reproduction America, Africa, India, eastern Asia and Australia but also widespread in the Mediterranean region, central America After the immatures reached adulthood and initiated and southern USA (Carver, 1978). Based on our nymphal reproduction, adult mortality and fecundity were observations, this aphid is abundant on orange jessamine recorded daily and offspring were removed from each Murraya paniculata (L.) Jack (Rutaceae) and occasionally seedling until the death of the adult. appears in citrus groves in South Florida (J.J.Wang & J.H.Tsai, unpublished data). In the past ten years, the biology Data analysis and model development and ecology of T. citricida, A. spiraecola and A. gossypii have been well documented (Komazaki, 1982, 1988; Kocourek et Developmental times, survivorship, longevity, and al., 1994; van Steenis & El-Khawass, 1995; Tsai, 1998; Tang et fecundity were subjected to analysis of variance (ANOVA) al., 1999; Tsai & Wang, 1999; Wang & Tsai, 2000; Tsai & Wang, for the effects of temperatures. General linear model 2001). However, little is known of the biology of T. aurantii, procedure (PROC GLM, SAS Institute, 1988) was used and especially about its developmental rate, temperature means were separated by Duncan‘s multiple range test thresholds, age-specific fecundity and survivorship. when significant F-values were obtained (P < 0.05). A linear Therefore, an experiment was initiated to quantify T. aurantii regression analysis (PROC REG, SAS Institute, 1988) was development, reproduction and longevity in relation to used for computing the lower developmental threshold of temperature and to provide an experimental basis for different nymphal stages (Campbell et al., 1974). developing an overall aphid population model. Development > 30 °C was outside the linear segment of the growth curve and therefore not included in the linear regression. Materials and methods Temperature-dependent developmental rates were described using the non-linear, biophysical model of Sharp Aphid source & DeMichele (1977), modified by Schoolfield et al. (1981). Laboratory colonies of T. aurantii were established with THA 1 1 RHO25 exp − field-collected aphids from orange jessamine M. paniculata 298. 15 RT 298. 15 groves on the campus of Fort Lauderdale Research and r(T) = (1) HL 11 HH 1 1 Education Center, University of Florida, Broward County, 1+−exp +− exp RTLT RTHT Florida, USA, in October 1998. Stock colonies were maintained on potted seedlings (20–40 cm tall) of orange jessamine, a preferred host for this aphid (J.J.Wang & where r(T) is developmental rate at temperature T (°K); R is J.H.Tsai, unpublished data) in an insect-rearing room at 25 ± the universal gas constant (1.987 cal degreeϪ1 mole–1); 1°C, 80 ± 5% r.h., and a photoperiod of 14:10 h (L:D). After a RHO25 is the developmental rate at 25°C (298.15°K) 4-month rearing period, the ensuing colonies were used for assuming no enzyme activation; HA is the enthalpy of the tests. The identity of T. aurantii was confirmed by S.E. activation of a developmental reaction that is assumed to be Halbert at the Division of Plant Industry, Florida catalysed by a rate-controlling enzyme; TL (or TH) is the Department of Agriculture and Consumer Services, Kelvin temperature at which the rate-controlling enzyme is Gainesville, Florida, USA. Voucher specimens were half active and half low- (or high-) temperature inactive; HL deposited at the collection of the Division of Plant Industry, (or HH) is the change in enthalpy associated with low- (or Florida Department of Agriculture and Consumer Services, high-) temperature inactivation of the enzyme. An SAS Gainesville, Florida, USA. program developed by Wagner et al. (1984a) using Marquardt‘s techniques was employed to fit the model to developmental data sets of different immature stages. Experimental procedures for development Cumulative frequency distributions of developmental Orange jessamine seedlings grown to 4–5 cm tall in a times for each nymphal stage were normalized using potting soil mix (50% pine bark, 40% Florida sedge peat, and median development time as the normalizing constant. A 10% sand) in pots (7.5 by 4.5 cm diameter) were used for single, temperature-independent, cumulative distribution aphid rearing, and test plants were replaced every two or was calculated as a weighted mean of the normalized Biology of Toxoptera aurantii 479 ␣ cumulative distributions, to which the cumulative Weibull where equals the number of rm to be tested, the sample size 2 distribution was fitted. of ith rm is ni. Si is the jackknife estimate of the variance for ␤ the ith r . F(x) = 1 – exp(–[(x – ␥)/␩] ) (2) m The Gompertz function (Strehler, 1977) was used to where F(x) is the probability of a cohort that has completed describe the age-specific survival of female adults (lx): ␤ development at a normalized developmental time x, and , = becx ␥, and ␩ are empirical constants.