PHYSIOLOGICAL ECOLOGY Life Table and Population Parameters of (Homoptera: ) at Different Constant Temperatures

1 BEATRIZ MARIA DIAZ AND ALBERTO FERERES

Departamento de Proteccio´n Vegetal, Centro de Ciencias Medioambientales, C/Serrano 115 Dpdo., Madrid 28006, Spain

Environ. Entomol. 34(3): 527Ð534 (2005) ABSTRACT Age-speciÞc life tables of the lettuce aphid, Nasonovia ribisnigri (Mosley), feeding on lettuce were determined at different constant temperatures under controlled conditions. Our results showed that the proportion of alates increased with increasing temperatures, remaining below 7% at 16ЊC and increasing to 40Ð57% at a temperature above 20ЊC. The longest developmental time of apterous aphids was obtained at 8ЊC (31.5 d), and the shortest was at 26ЊC (6.2 d), whereas the developmental time of alates was always 0.7Ð1.1 d longer than for apterous. Most aphids needed four instars to reach adult stage, but at 8, 26, and 28ЊC, many individuals passed through Þve or six molts. Age-speciÞc survivorship (lx) was always above 90% at the temperature range of 16Ð24ЊC. Mortality rate (qx) was rather low but constant at 8ЊC. However, mortality was high at 28ЊC and occurred mainly in the last nymphal instars and adult stage. Unexpectedly, no nymphs were produced by the adult morphs at 28ЊC, but effective fecundity was high at 8ЊC. Fecundity for alates was always lower than

for the apterous aphids at the same temperature. The largest intrinsic rate of natural increase (rm), and the mean relative growth rate (R៮ GR) occurred at 24ЊC, for both apterous and alate morphs, and the lowest at 8ЊC. Our results show that lettuce aphid is better adapted to survive and reproduce at low (8ЊC) than at high (28ЊC) temperatures, and its best performance occurred at 20Ð24ЊC.

KEY WORDS Nasonovia ribisnigri, lettuce aphid, survival, fecundity, population parameters

THE LETTUCE APHID, Nasonovia ribisnigri (Mosley), is a because the presence of living aphids on the leaves major pest of lettuce (Lactuca sativa L.) crops distrib- reduces the market value or makes lettuce totally uted in temperate regions of Europe, where it origi- unmarketable. Physical postharvest treatments (vac- nates (Blackman and Eastop 1984, Reinink and Diele- uum and controlled atmosphere with CO2) could be man 1993, Parker et al. 2002, Nebreda et al. 2004). It a valuable strategy to reduce cosmetic damage (Liu has recently become a major pest of outdoor and 2003). indoor lettuce crops worldwide (Emmett 1992), in- The living and feeding site preference of the lettuce cluding western United States (Palumbo 2000) and aphid reduces the efÞcacy of insecticide treatments, New Zealand (Stufkens and Teulon 2003). Also, the and therefore, an increasing number of applications of aphid invaded Tasmania in 2004 and, therefore, has broad-spectrum pesticides are needed to control the become a serious threat to Australian lettuce produc- pest (Chaney and Wunderlich 2000). This practice has tion (Teulon 2004). resulted in rapid resistance to several insecticides The life cycle of N. ribisnigri is holocyclic hetero- (RuÞngier et al. 1997, Barber et al. 1999) and accu- ecious between its primary Ribes sp. and secondary mulation of unacceptable pesticide residues (Sances hosts such as Asteraceae (Cichorium sp., Crepis sp., et al. 1993). Implementation of integrated pest man- Hieracium sp., Lactuca sp., Lampsana sp.), Scrofulari- agement (IPM) programs are needed to avoid or re- aceae (Euphrasia sp., Veronica sp.), and Solanaceae duce these risks in lettuce crop production (Chaney (Nicotiana sp., Petunia sp.) species (Blackman and and Wunderlich 2000). Eastop 1984). Recent studies have addressed the population de- Nasonovia ribisnigri deposit their young near the velopment, damage, and control of N. ribisnigri on terminal growing young leaves of lettuce (Palumbo head lettuce (Palumbo 2000, Palumbo and Hannan 2000) and colonize the wrapper leaves inside the de- 2002), phenology to forecast infestation (Collier et al. veloping heads (Mackenzie and Vernon 1988), caus- 1994), and distribution within Þelds and plants (Mac- ing leaf distortion and vigor reduction in seedlings. At kenzie and Vernon 1988). In the same way, the biology harvest, they present a signiÞcant cosmetic problem of N. ribisnigri on three different lettuce cultivars was studied under laboratory conditions (La Rossa et al. 1 Corresponding author: CCMA-CSIC, c/Serrano 115 Dpdo., Ma- 2000), and their life table parameters were compared drid 28006, Spain (e-mail: [email protected]). (Vasicek et al. 2002).

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Temperature being the main abiotic factor affecting inside an environmental growth chamber (MLR-350; population growth and life statistics of aphids (Mes- Sanyo, Gallenkamp PCL, UK). Each study was con- senger 1964, Howe 1967, Andrewartha 1973). Several ducted at a Þxed constant temperature (8, 12, 16, 20, works have been published on the relationships be- 24, 26, and 28 Ϯ 0.5ЊC). All experiments were con- tween temperature on population growth and life ta- ducted at a photoperiod of 14:10 h (L:D) and a relative ble statistics of various aphid species (Michels and humidity of 60 Ϯ 5%. The growth chamber was Behle 1988, Michels and Behle 1989, Kieckhefer et al. equipped with 15 daylight ßuorescent (40 W) lamps 1989, Kieckhefer and Elliott 1989, Asin and Pons 2001). that provided 15.3 ␮mol/m2/s of light intensity to the It is also known that population development of N. plants located Ϸ20 cm from the light source. ribisnigri in the Þeld is well correlated with heat unit Each nymph was observed daily to record the tim- accumulation (Palumbo 2000, Liu 2004). However, ing and number of nymphal stadia produced and the little information exists on how speciÞc constant tem- mortality at the same time of the day (1000Ð1200 perature affects N. ribisnigri life table statistics under hours). The presence of exuviae was used to deter- controlled conditions. mine molting. When the aphids reached adult stage, The aim of this work was to study the effects of the morph, number of progeny per adult, and adult different constant temperature on the life table sta- mortality were recorded daily during a time equiva- tistics of N. ribisnigri feeding on lettuce plants. This lent to the time from birth to onset of reproduction, information will be used to develop a degree-day also called prereproductive period (d) (Wyatt and based phenological model for effective forecasting of White 1977). The neonate nymphs were removed the occurrence of N. ribisnigri in the Þeld. daily with a Þne-hair brush. Developmental time for each instar and the total developmental time from birth to adulthood for both alate and apterous aphids Materials and Methods were calculated for each individual at each tempera- Lettuce Plants. Seeds of a romaine type were sown ture. in plastic pots (10 cm diameter) containing a mixture Calculation of Life-Table Statistics. Mortality, ex- of soil and vermiculite (50:50). Each seedling was pressed as a mortality rate (qx) was calculated as transplanted at the cotyledon stage to individual pots follows: qx ϭ dx/nx, where x ϭ age interval (day), (60 replicates). Plants were used to begin the exper- dx ϭ number dying during the age interval x to x ϩ 1, iments when they reached the one-leaf stage. Three and nx ϭ number of survivors at start of age interval times a week the seedlings were irrigated with nutri- x. tive solution 20:20:20 (N:P:K; Nutrichem 60; Miller Age-speciÞc survival (lx) and age-speciÞc fecundity Chemical and Fertilizer, Hanover, PA). The seedlings (mx) (Price 1984) were calculated for each morph were maintained in a growth chamber at a tempera- and temperature. The product of age-speciÞc survival ture of 26:20ЊC (day:night) and a photoperiod of 14:10 and age-speciÞc fecundity called reproductive expec- h (L:D) until the experiments began. tation (lxmx) was calculated during a time equivalent Aphid Colony. Nasonovia ribisnigri adults were ob- to the prereproductive period. The sum of reproduc- ⌺ tained from a laboratory culture initiated from the tive expectation ( lxmx) calculated as described progeny of one virginoparous apterous female col- above was used as a measure of population growth at lected in a lettuce Þeld at Villa del Prado (Madrid, each of the temperatures used in our study. Spain) in 1999 and maintained on lettuce cultivar Other population parameters such us intrinsic rate

“Cazorla” inside -proof cages in a growth cham- of natural increase (rm) and mean generation time ber at a temperature of 23:18ЊC (day:night) and a (Td) were calculated using the Wyatt and White ϭ photoperiod of 16:8 h (L:D). (1977) equation: rm 0.738 (logeMd)/d, where d is Experimental Conditions. Aphids of nearly equal the prereproductive period, Md is the number of age and weight were selected to start the experiments. young produced in an reproductive period equal to d, For this purpose, 10 alate adult aphids from the colony and 0.738 is a correction factor. Generation time (Td) were placed for 24 h in a plastic cage (9 cm diameter was calculated as follows: Td ϭ d/0.738. and 3 cm high) containing two Þlter paper disks and For aphids, the mean relative growth rate (RGR)is one lettuce leaf. The petiole of the leaf was wrapped closely and positively correlated with the intrinsic rate ϭ with absorbent paper and was inserted into an eppen- of natural increase (rm) as follows rm 0.86RGR dorf tube (1.5 ml) containing water, so that the leaf (Dixon 1987). Therefore, RGR can be easily calcu- ϭ could maintained turgor as long as possible. After 24 h, lated as RGR (0.86 logeMd)/d. adults were removed, and newly born nymphs were Statistical Analysis. All the parameters recorded for collected and reared on lettuce leaves in plastic cages nymphal and adult stages as well as for apterous as described above until they reached the adult stage. and alate morphs at each of the temperatures studied Lettuce leaves were replaced every 2Ð3 d during this were subjected to a one-factor analysis of variance period. Aphids were removed just after they reached (ANOVA). Data on the life-table parameters recorded the adult stage and introduced for 12 h in new plastic were previously transformed by ln(x ϩ 1) to reduce cages to collect newborn nymphs. These nymphs of heteroscedasticity. Statistical analysis was performed the same age were used to begin the experiments. using Superanova v. 1.11 (Abacus Concepts 1989) and Cohorts of 60 Þrst-instar nymph were individually Statview 4.01 software (Abacus Concepts 1992) for placed on individual lettuce seedlings and maintained Macintosh. Mean comparisons of each parameter be- June 2005 DIAZ AND FERERES:BIONOMICS OF LETTUCE APHID AT DIFFERENT TEMPERATURES 529

served in the range between 8 and 26ЊC(F ϭ 933.96, df ϭ 6,217; P Ͻ 0.0001; Table 1). Developmental time decreased with increasing temperatures at the range of 8 (31.5 d) to 26ЊC (6.3 d), whereas it started to slightly increase at 28ЊC (7.0 d). Table 1 also shows that the mean developmental time for the Þrst instar nymph was generally longer than for the rest of the nymphal instars. The developmental time of alates was signiÞcantly (F ϭ 53.94; df ϭ 3,85; P Ͻ 0.0001) different among the temperature range of 20Ð26ЊC, but alates always re- quired more time than apterous to complete the im- mature stage (Tables 1 and 2). There were no signif- icant differences in the developmental time of alates between 26 and 28ЊC (Table 2). Data on the devel- opmental time of alates subjected to a temperature Յ16ЊC were not analyzed because very few individ- Fig. 1. Proportion of alatae and apterae of N. ribisnigri uals developed into alates at such low temperatures obtained at different temperatures. (Fig. 1). All of the aphids completed four nymphal instars before reaching the adult stage at temperatures of 12, tween the different temperatures were made using 16, 20, and 24ЊC. However at 8ЊC, 20% of the total aphid least signiÞcant difference (LSD) Fisher test (P ϭ population passed through a Þfth nymphal instar that 0.05) (Fisher 1935). Њ The relationship between the relative growth rate lasted 6.8 d (Table 1), and at 26 and 28 C, the per- centage of individuals that completed Þve nymphal (RGR) with temperature (T) was calculated and Þt- Њ ted to a curvilinear regression line using SPSS v. 12.05 instars was 30 and 32.5%, respectively. At 26 and 28 C, statistical package (SPSS 2003) and plotted using Sig- some aphids even went into a sixth nymphal instar, but Њ maPlot v. 7 for Windows (SPSS 2001). all died before reaching the adult stage. At 8 C Þfth- instar nymphs had no mortality, but 50% of them died after reaching the adult stage. Results Survival. Age-speciÞc survivorship curves of N. Proportion of Alate Morphs. Temperature had a ribisnigri among all the temperatures used in our study strong effect on the proportion of alate and apterous are shown in Fig. 2. Survival rates (lx) of the total individuals in the population of N. ribisnigri. The per- number of aphids was very high at temperatures be- centage of alates remained rather constant (40Ð57%) tween 16 and 24ЊC, reaching a maximum value at 20ЊC, at the range of 20Ð28ЊC (Fig. 1). However, at a tem- at which no mortality was recorded. High tempera- perature of Յ16ЊC, most of the adult morphs were tures (26Ð28ЊC) affected the survivorship of N. ribisni- apterous (93%). Therefore, the data obtained at tem- gri more than low temperatures (8Ð12ЊC). peratures of 20Ð28ЊC were analyzed separately for High temperatures (26Ð28ЊC) had a higher impact apterous and alate morphs. We also observed that the on the mortality rate (qx) of adults and late nymphal aphids remained pale orange in color at a temperature instars than on early nymphal instars (Fig. 3). Con- equal to or above 16ЊC, but at temperatures below sequently. the cohorts reared at 26 and 28ЊC showed 16ЊC, aphid color changed to dark brown. an evident type I curve (Slobodkin 1962). However, Developmental Time. For apterous aphids, signif- low temperatures (8ЊC) induced a rather low but icant differences in developmental time were ob- constant mortality to all nymphal instars and adults,

Table 1. Developmental time of nymphal instars of apterous N. ribisnigri at different constant temperatures

Days in stadiab Temperature (ЊC) na Totalc First Second Third Fourth Fifth 8 45 8.8 Ϯ 0.34a 8.4 Ϯ 0.56a 7.0 Ϯ 0.37a 5.7 Ϯ 0.2a 6.8 Ϯ 0.70 31.5 Ϯ 0.42a 12 56 5.2 Ϯ 0.10b 3.2 Ϯ 0.10b 3.9 Ϯ 0.14b 3.4 Ϯ 0.19b Ñ 15.8 Ϯ 0.27b 16 54 4.2 Ϯ 0.07c 3.1 Ϯ 0.07b 2.2 Ϯ 0.09c 1.9 Ϯ 0.08c Ñ 11.5 Ϯ 0.20c 20 24 2.6 Ϯ 0.10d 1.4 Ϯ 0.10c 2.0 Ϯ 0.10c 1.9 Ϯ 0.07c Ñ 8.0 Ϯ 0.14d 24 24 2.0 Ϯ 0.00d 1.0 Ϯ 0.00c 1.8 Ϯ 0.08c 1.7 Ϯ 0.09c Ñ 6.5 Ϯ 0.13e 26 17 1.9 Ϯ 0.06d 1.2 Ϯ 0.11c 1.9 Ϯ 0.11c 1.1 Ϯ 0.09d Ñ 6.3 Ϯ 0.11e 28 4 2.0 Ϯ 0.40d 1.2 Ϯ 0.25c 1.5 Ϯ 0.29c 2.2 Ϯ 0.48e Ñ 7.0 Ϯ 0.41de

Means Ϯ SE within a column followed by the same letter are not signiÞcantly different (P Ͻ 0.05; LSD Fisher). a No. individuals reaching the adult stage. b Between 12 and 24ЊC, all individuals passed through four instars before reaching the adult stage. At 8ЊC, 12 individuals passed through a Þfth instar. c Developmental time (days) for the whole nymphal period (from birth of nymphs until adult stage). 530 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3

Table 2. Developmental time in days of nymphal instars of alate N. ribisnigri at different constant temperatures

Days in stadia Temperature (ЊC) na Totalb First Second Third Fourth 20 36 2.7 Ϯ 0.07a 1.6 Ϯ 0.10a 2.6 Ϯ 0.08a 2.2 Ϯ 0.07a 9.2 Ϯ 0.10a 24 35 2.0 Ϯ 0.03b 1.4 Ϯ 0.08ab 1.9 Ϯ 0.05b 1.8 Ϯ 0.05b 7.3 Ϯ 0.08b 26 13 2.0 Ϯ 0.00b 1.5 Ϯ 0.14b 1.7 Ϯ 0.13b 2.4 Ϯ 0.38b 7.9 Ϯ 0.31c 28 5 2.0 Ϯ 0.14b 1.6 Ϯ 0.40ab 2.2 Ϯ 0.50b 2.4 Ϯ 0.51b 8.2 Ϯ 0.20c

Means Ϯ SE within a column followed by the same letter are not signiÞcantly different (P Ͻ 0.05; LSD Fisher). a No. individuals reaching the adult stage. b Developmental time (days) for the whole nymphal period (from birth of nymphs until adult stage).

Fig. 2. Age-speciÞc survivorship (lx) and age-speciÞc fecundity (mx) of N. ribisnigri at different constant temperatures. At 28ЊC, no nymphs were obtained. June 2005 DIAZ AND FERERES:BIONOMICS OF LETTUCE APHID AT DIFFERENT TEMPERATURES 531 SE 0.7c 0.1b 0.15a Ϯ Ϯ Ϯ Ϯ SE Td 0.01c 14.4 0.08b 9.9 0.06a 12.5 Ϯ Ϯ Ϯ Ϯ RGR , intrinsic rate of natural increase; m SE 0.01c 0.140 0.06b 0.354 0.06a 0.297 Alates Ϯ Ϯ Ϯ Ϯ m lxmx r

Fig. 3. Mortality rate (qx) of N. ribisnigri at different age ͚ classes and temperatures. SE 0.4c 3.3 0.120 1.1b 22.7 0.302 1.2a 27.4 0.255 Ϯ Ϯ Ϯ closely resembling a type II survivorship curve. At a Ϯ temperature of 12ЊC, the mortality always remained below 20% (Fig. 2). Fecundity. All adult aphids were able to reproduce a at all temperatures except at 28ЊC, where no nymphs n at all were produced. Reproduction began immedi- ately (Ͻ24 h) after the last molt for temperatures in SE Md 0.5b 5 2.2 0.2a 36 19.7 0.2b 34 23.6 0.2c Ñ Ñ Ñ Ñ Ñ Ñ 0.4d Ñ Ñ Ñ Ñ Ñ Ñ the range of 16Ð24ЊC, and therefore, aphid develop- 0.6e Ñ Ñ Ñ Ñ Ñ Ñ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ mental time was similar to the prereproductive period. Ϯ Њ

However, aphids developing at 8, 12, and 26 C had a 0.05; LSD Fisher).

delay of 2, 2.4, and 3 d, respectively, between their last Ͻ molt and onset of reproduction. P

Figure 2 shows that age-speciÞc fecundity (mx) SE Td at different constant temperatures 0.011c 11.6 0.013f 8.9 0.007e 11.0 0.005d 15.5 0.002b 24.2 0.002a 47.3 curves varied substantially among temperatures. At Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ 8ЊC, the mean number of nymphs/female per day was low (Ϸ1 nymph), but remained rather constant during RGR a period of time equivalent to the prereproductive phase (Ϸ40 d). The mean daily fecundity (number of N. ribisnigri nymphs/female) increased with temperature in the SE 0.09c 0.206 0.11f 0.433 0.06e 0.386 0.04c 0.261 0.02b 0.148 0.02a 0.087

Њ Apterous Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ range of 12Ð24 C, but a reduction in fecundity was Ϯ observed at a temperature of 26ЊC. m Age-speciÞc fecundity (mx) and fecundity in a pe- riod equivalent to the prereproductive time (Md), on average, was higher for apterous than for alate aphids

at all of the three temperatures where pair-wise com- lxmx r parisons were possible (Fig. 2; Table 3). Fecundity of ⌺ apterous aphids was signiÞcantly higher at 16 and 20ЊC compared with the rest (F ϭ 96.34; df ϭ 5,176; P Ͻ SE 0.5d 4.2 0.173 1.0a 27.2 0.372 1.4c 46.9 0.332 0.8c 33.4 0.224 0.8b 23.0 0.127 0.0001; Table 3). The lowest fecundity was observed at 2.2a 19.8 0.074 Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ 26ЊC (3.3 nymphs/female). Fecundity of alates also Ϯ Md lxmx, sum of the product of age-speciÞc survivorship (lx) and age-speciÞc fecundity (mx) during a time equal to a prereproductive period; r showed the same general trend: highest fecundity at ͚ 20ЊC and lowest at 26ЊC (23.6 Ϯ 1.2 and 2.2 Ϯ 0.4, respectively; F ϭ 14.53; df ϭ 2,72; P Ͻ 0.0001). a n Population Growth Parameters. The sum of the reproductive expectation of apterous aphids for a time ͚ SE within a column followed by the same letter are not signiÞcantly different (

equivalent to the prereproductive period ( lxmx) Ϯ Њ reached its highest value at 20 C (46.9) and the lowest 8 22 22.5 C) 26 12 3.4 24 23 22.1 20 24 29.5 16 53 31.9 12 48 17.5 Њ , mean relative growth rate; Td, generation time. (

Њ No. individuals reaching adult stage. at 26 C (4.2). The reproductive expectation of alate Table 3. Population parameters of apterae and alatae morphs of Means Md, effective fecundity; a Temperature aphids followed a similar trend (Table 3). RGR 532 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3

temperature has been used in the past to develop degree-day based models to forecast aphid outbreaks (Collier et al. 1994, Ro et al. 1998). Dixon (1987) showed that the length of time required for an aphid from birth to adult is variable and dependent on two intrinsic factors, birth weight and whether the morph is winged or unwinged, and two extrinsic factors, food quality and temperature. In our study, food quality was probably affected when aphids developed at a con- stant temperature of Ն26ЊC, because these tempera- tures are well above the range for optimum develop- ment of lettuce (15Ð20ЊC) (Flint 1987). Lettuce plants that developed at a constant temperature of Ն26ЊC were unable to form a rosette of leaves, which is the preferred feeding site of N. ribisnigri. Our results reported here show that N. ribisnigri was sensitive to changes in temperature, affecting the pro- portion of alates being produced as well as their de- velopmental time, survival, and fecundity. Low tem- peratures dramatically reduced the proportion of Fig. 4. Relationship between relative growth rate (RGR; dots) and temperature for apterous N. ribisnigri. Fitted re- alates in the population of N. ribisnigri. Apterous gression line equation: y ϭ 0.968 Ϫ 0.220T ϩ 0.017T2 aphids were the predominant morph at a temperature Ð0.0004T3 (R2 ϭ 0.85). of Յ16ЊC, and the proportion of alates increased to almost 60% at a temperature of 20ЊC and remained rather constant in the range of 20Ð28ЊC. Dixon (1998)

The intrinsic rate of natural increase (rm) showed found that cereal aphids reared in isolation never give signiÞcant differences at the different range of tem- rise to alate forms even if they are reared on plants of peratures used in our study both for apterous (F ϭ poor quality; in consequence, our results suggest that 475.64; df ϭ 5,175; P Ͻ 0.0001) and alates (F ϭ 69.40; the occurrence of N. ribisnigri alates is probably re- ϭ Ͻ df 2,72; P 0.0001). The lowest rm value was ob- lated to an increase of rearing temperature more than served at 8ЊC for apterous aphids (0.074) and at 26ЊC with any other factor. Liu (2004) observed that the for alate aphids (0.120). The highest rm value was proportion of N. ribisnigri alates under Þeld conditions obtained at 24ЊC for both apterous and alate aphids did not vary signiÞcantly with increases in population (0.372 and 0.302, respectively; Table 3). density. Therefore, an increase in temperature (T Ն Mean relative growth rate (RGR) of apterous 20ЊC) will have a signiÞcant increase in the proportion aphids increased with increasing temperatures from 8 of N. ribisnigri alates being produced in the Þeld, and to 24ЊC (0.087 Ϯ 0.002 and 0.433 Ϯ 0.013, respectively; this will increase seasonal movement and dispersal of F ϭ 481.43; df ϭ 5,176; P Ͻ 0.0001). The highest value the population. for RGR of alates was recorded also at 24ЊC (0.354 Ϯ We observed that the developmental time of both 0.08; F ϭ 69.40; df ϭ 2,72; P Ͻ 0.0001). The relationship alate and apterous morphs of N. ribisnigri decreased between the RGR values of apterous aphids and tem- with increasing temperatures in the range of 8Ð26ЊC. perature was curvilinear (y ϭ 0.968 Ϫ 0.220T ϩ The shortest developmental period of N. ribisnigri was 0.017T2 Ð0.0004T3; R2 ϭ 0.85), with maximum RGR obtained at 24Ð26ЊC(Ϸ6 d), a similar period as the one occurring at 24ЊC (Fig. 4). reported for aphids that colonize winter cereals (Dean There were signiÞcant differences in the mean gen- 1974). Alates of N. ribisnigri had a longer develop- eration time (Td) among temperatures for both apter- mental time than the apterous morph (0.7Ð1.1 d ous (F ϭ 820.09; df ϭ 5,176; P Ͻ 0.0001) and alate (F ϭ longer), which has been observed in other aphid spe- 124.193; df ϭ 2,75; P Ͻ 0.0001) morphs. As opposed to cies as well (Liu and Hughes 1987, Kieckhefer et al. rm and RGR, the mean generation time decreased with 1989, Liu and Yue 2001). increasing temperatures, reaching the lowest value at For apterous aphids, low temperatures had a much 24ЊC for both apterous (8.9 d) and alate aphids (9.9 d; stronger effect on the duration of the nymphal period Table 3). than high temperatures. This nonlinear response of N. ribisnigri to temperature is clearly observed from 8 to 12ЊC, because a 4Њ increase produced a 50% reduction Discussion in its developmental time (from 31.5 to 15.8 d), Temperature determines the physiological state of whereas the same 4Њ increase from 12 to 16ЊC reduced poikilothermic organisms, and as a consequence, is the its developmental time in only 9% (from 15.8 to key variable regulating their survival, fecundity, and 11.5 d). Increases in temperature Ͼ24ЊC had a very population growth. Information on how temperature small inßuence on developmental time of both apter- can inßuence the life cycle of a given insect pest is ous and alate morphs of N. ribisnigri. essential to develop effective integrated pest manage- Generally, an aphid passes through four nymphal ment (IPM) strategies. The response of aphids to instars in developing from birth to adult (Dixon 1987). June 2005 DIAZ AND FERERES:BIONOMICS OF LETTUCE APHID AT DIFFERENT TEMPERATURES 533

In our study, the number of nymphal instars of N. adapted to develop and reproduce under low temper- ribisnigri changed with temperature, and a variable ature conditions, although the optimum temperature number of N. ribisnigri individuals developed into a for population increase was in the range of 20Ð24ЊC. Þfth-instar (at 8, 26, and 28ЊC) or even into a sixth- Our results agree with observations in Arizona on instar nymph (at 26 and 28ЊC), in agreement with the head lettuce crops where N. ribisnigri population results reported by La Rossa et al. (2000). They found seemed to increase in early March when the average that N. ribisnigri reared at constant 10ЊC on three daily temperature was Ϸ18Ð20ЊC (60Ð65ЊF) and had different lettuce cultivars went through Þve instar a sharp decline in population abundance in April nymphs before reaching the adult stage. Similarly, where daytime highs exceeded 32ЊC (90ЊF), conclud- Diuraphis noxia (Mordvilko) exhibited a variable ing that temperature and planting date had a strong number of instars (four to six) during the course of its inßuence on the seasonal abundance of the lettuce development at different temperatures (Michels and aphid (Palumbo 2000, Palumbo and Hannan 2002). Behle 1988, Nowierski et al. 1995). Survival of N. Because this aphid species is one of the most important ribisnigri was more affected by high (26Ð28ЊC) than pests of lettuce worldwide, and control is always dif- by low temperatures (8ЊC). The highest survivorship Þcult, it is very important to forecast the early occur- obtained in our study was at 20ЊC, the same as for rence of lettuce aphid in the Þeld. The information Rhopalosiphum padi L. and Macrosiphum avenae (F.) reported in our work is essential to develop or improve developing on winter wheat (Dean 1974). existing mathematical models as well as to optimize High temperatures were very detrimental to the the environmental conditions needed for mass rearing reproduction of N. ribisnigri because no nymphs were of this aphid as a host for natural enemy production. produced at 28ЊC, a result similar to Sitobion avenae Њ reared on wheat at a temperature of 30 C (Acreman Acknowledgments and Dixon 1989, Asin and Pons 2001). Age-speciÞc fecundity shape curves varied widely with tempera- We thank E. Garzo for technical advise. This work was ture. From 8 to 12ЊC daily, fecundity was low but supported by the Comisio´n Interministerial de Ciencia y remained rather stable during most of the repro- Tecnologõ´a (AGL-2003-0753-C03-01). ductive period, whereas at higher temperatures (16Ð 24ЊC), fecundity was more concentrated in the Þrst References Cited days (2Ð8 d) of reproduction. Similar reproduction strategies have been observed for Schyzaphis grami- Abacus Concepts. 1989. SuperANOVA. Abacus Concept, Berkeley, CA. num (Rondani), R. padi, and D. noxia, reared on wheat Abacus Concepts. 1992. Statview. Abacus Concept, Berke- at constant and ßuctuating temperatures (Michels and ley, CA. Behle 1989). The temperature associated to the short- Acreman, S. J., and A.F.G. Dixon. 1989. The effects of tem- est generation time (Td) and highest potential for perature and host quality on the rate of increase of the population increase (highest rm value) of N. ribisnigri grain aphid (Sitobion avenae) on wheat. Ann. Appl. Biol. was 24ЊC for both apterous and alate morphs. How- 115: 3Ð9. ever, reproductive expectation was highest at 20ЊC Andrewartha, H. G. 1973. Introduction to the study of an- because no mortality was observed at that given tem- imal populations, 2nd ed. Chapman & Hall, London, UK. perature. In a similar way, A. gossypii showed the Asin, L., and X. Pons. 2001. Effect of high temperature on Њ the growth and reproduction of corn aphids (Homoptera: highest rm value at 25 C on different hosts and rearing Aphididae) and implications for their population dynam- conditions (Van Steenis and El-Khawass 1995, Xia et ics on the Northeastern Iberian Peninsula. Environ. En- al. 1999), as well as Myzus persicae (Sulzer) feeding on tomol. 30: 1127Ð1134. Brussels sprouts (Brassica oleracea variety Ôgemmif- Barber, M. D., G. D. Moores, G. M. Tatchell, W. E. Vice, and eraÕ) (El Din 1976). I. Denholm. 1999. 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University of California Cooperative increase more rapidly in case that an apterous colo- Extension, Salinas CA. Website: http://www.cdpr.ca. nizes a given plant. This reduction in the fecundity of gov/docs/empm/grants/98-99/Þnlrpts/applÞnl.htm. alates has been explained by the fact that winged Collier, R. H., J. Davies, M. Roberts, M. Leatherland, S. aphids have smaller gonads (20% reduction in size) Runham, and J. Blood Smyth. 1994. Monitoring and forecasting the times of attack of the lettuce root aphid, than apterous aphids, which seems to be a trade-off Pemphigus bursarius L. Bull. IOBC/WPRS. 17: 31Ð40. between the investment in gonads and lipoidal re- Dean, G. J. 1974. Effect of temperature on the cereal aphids serves needed for ßight (Dixon et al. 1993). Metopolophium dirhodum (Wlk.), Rhopalosiphum padi This study has shown that N. ribisnigri is very sen- (L.) and Macrosiphum avenae (F.) (Hem., Aphididae). sitive to changes in temperature and that it is very well Bull. Entomol. 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