A comparative study of development and demographic parameters ...

Exp Appl Acarol (2011) 54:1–19 DOI 10.1007/s10493-010-9420-6

A comparative study of development and demographic parameters of Tetranychus merganser and Tetranychus kanzawai (Acari: Tetranychidae) at different temperatures M. S. Ullah • D. Moriya • M. H. Badii • G. Nachman • T. Gotoh

Received: 13 June 2010 / Accepted: 29 November 2010 / Published online: 17 December 2010 Ó Springer Science+Business Media B.V. 2010

Abstract We investigated the effect of temperature on development and demographic parameters such as the intrinsic rate of natural increase (rm) of the two spider mite species Tetranychus merganser Boudreaux and T. kanzawai Kishida at eleven constant temperatures ranging from 15 to 40°C at intervals of 2.5°C. Both male and female T. merganser and T. kanzawai completed development from egg to adult at temperatures ranging from 15 to 37.5°C. The longest developmental duration of immature stages was found at 15°C and the shortest developmental duration was found at 35°C for both species. Using linear and non-linear developmental rate models, the lower thermal thresholds for egg-to-adult (female and male) and egg-to-egg development were estimated as 12.2–12.3°C for T. merganser and as 10.8°C for T. kanzawai. The highest developmental rates were observed at around 35°C, whereas the upper developmental thresholds were around 40°C for both species. In fact, at 40°C, a few eggs of either species hatched, but no larvae reached the next stage. The rm-values of T. merganser ranged from 0.072 (15°C) to 0.411 day-1 (35°C), whereas those of T. kanzawai ranged

M. S. Ullah  D. Moriya  T. Gotoh (&) Laboratory of Applied Entomology and Zoology, Faculty of Agriculture, Ibaraki University, Ami, Ibaraki 300-0393, Japan e-mail: [email protected] M. S. Ullah e-mail: [email protected] D. Moriya e-mail: [email protected] M. H. Badii Universidad Autonoma de Nuevo Leon, 66450 San Nicolas de los Garza, NL, Mexico e-mail: [email protected] G. Nachman Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Ø Copenhagen, Denmark e-mail: [email protected]

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from 0.104 (15°C) to 0.399 (30°C). The rm-values were higher for T. kanzawai than for T. merganser at temperatures from 15 to 30°C, but not at 35°C (0.348 day-1). Total fecundity of T. merganser was also higher than that of T. kanzawai at 35°C. These results indicate that higher temperatures favor T. merganser more than T. kanzawai. Keywords T. merganser  T. kanzawai  Demographic parameter  Thermal threshold  Degree-day  Intrinsic rate of natural increase

Introduction The spider mite Tetranychus merganser Boudreaux occurs on solanaceous, rosaceous, oleaceous and caricaceous plants in China, the United States and Mexico (Bolland et al. 1998). This species, which is not known to occur in Japan, has frequently been detected on squash (pumpkin) shipped to Japan from the United States and Mexico during plant quarantine inspections (Masaki 1991; Masaki et al. 1991; Masaki and Kitamura 2004). In those studies, it was described as T. hydrangeae Pritchard and Baker. Tetranychus merganser is closely related to T. kanzawai Kishida, which is a pest of many crops worldwide. Thus, the finding of T. merganser at Japan’s doorstep raises fears that it will invade Japan and cause damage to crops. To prepare for an invasion of T. merganser, it is essential to know how temperature affects its rate of population growth (expressed as the intrinsic rate of natural increase (rm) at a given temperature) as well as its susceptibility to various acaricides. Tetranychus hydrangeae is a junior synonym of T. kanzawai, because there is no reproductive isolation between mites referred to be T. kanzawai collected from tea in Japan and specimens identified as T. hydrangeae from hydrangea in Australia, and because there are no morphological differences between them (Navajas et al. 2001). So we investigated the morphology of mites identified as T. hydrangeae collected in Mexico and determined them as T. merganser. This identification was later confirmed by C. H. W. Flechtmann (University of Sao Paulo, Brazil). Tetranychus merganser and T. kanzawai can be distinguished by the length of the aedeagal knob (5.5 and 4.0 lm, respectively) and by the color of males (pale yellowish green and reddish, respectively). Tetranychus kanzawai is a serious pest of a variety of crops such as solanaceous and rosaceous plants in Japan (Ehara and Gotoh 2009). It is distributed all over Asia, Oceania, North America and Mexico, where it is of considerable economic importance (Bolland et al. 1998). Nevertheless, there is no information on demographic parameters of T. kanzawai exposed to different temperature regimes. Temperature is the main abiotic factor influencing the temporal and spatial distribution of insects and mites in the field (Laing 1969; Tanigoshi et al. 1975; Carey and Bradley 1982; Perring et al. 1984; Bonato et al. 1990). Population growth rates largely determine the pest status of spider mites (Janssen and Sabelis 1992) and temperature strongly affects population growth (Sabelis 1985a; Roy et al. 2003; Mori et al. 2005; Gotoh et al. 2010). Therefore, knowing the temperature requirements of the different stages of mite pests can be used to forecast their potential distribution and abundance. Especially the rm-value is a key parameter to assess the potential severity of a pest species. The aim of the present study was to investigate the effect of temperature on development and reproduction of T. merganser and T. kanzawai collected in Mexico and Japan, respectively, and to use this information to compare the two species with respect to their potential growth rates in various temperature regimes.

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Materials and methods Mites Scores of T. merganser were collected originally from pumpkin on 6 April 2007 at Sonora, Mexico (28°580 N–111°330 W), and several tens of T. kanzawai were collected from tea on 19 May 1993 at Shizuoka, Japan (34°480 N–138°230 E). The T. merganser strain was imported to Japan with the authorization of the Ministry of Agriculture, Forestry and Fisheries of Japan (no. 18-Y-1274). All experiments with T. merganser and T. kanzawai were carried out in a level P2 biohazard room under negative pressure hood and the residual individuals as well as trash were autoclaved before discarding. Laboratory stocks were separately reared on leaf discs (ca. 16 cm2) of common bean, Phaseolus vulgaris L., placed on water-saturated polyurethane mats in plastic dishes (90 mm diameter, 20 mm depth) at 25 ± 1°C and under a 16:8 h light:dark photoperiod with 60–70% relative humidity. Development of immatures To determine the effect of different temperatures on developmental duration of T. merganser and T. kanzawai, inseminated female adults obtained from cultures were transferred individually onto a leaf disc (ca. 4 cm2) of common bean and kept at eleven constant temperatures from 15 to 40°C at a 2.5°C interval, under a long-day photoperiod (16L:8D). Females were allowed to lay eggs for 24 h at 15–25°C, 12 h at 27.5–35°C, and 6 h at 37.5–40°C. Only one egg was left and reared on each leaf disc and the developmental stages were recorded at the same time every day until all individuals reached the adult stage. There were some non-hatched eggs and some drowned immatures. We used these individuals to calculate survival rate, but did not include them in the calculation of the developmental duration. Oviposition and adult longevity When a female deutonymph emerged in the developmental experiments for each temperature, two adult males obtained from a stock culture were introduced onto the leaf disc for mating. The newly emerged females were observed at a 24-h interval to assess the date of first oviposition and determine the preoviposition period from 15 to 40°C at a 2.5°C interval. Oviposition and longevity of female mites were observed at temperatures at 15, 20, 25, 30 and 35°C. The number of eggs laid by a female was recorded daily throughout her life to calculate life-history parameters and after recording, eggs were removed by means of tweezers. During the oviposition period, some adult females drowned, especially just after replacing the leaf discs, or were killed accidentally. These individuals were discarded from the succeeding analysis. To calculate age-specific survival rate (lx) and fecundity rate (mx), it was necessary to assess (1) egg hatchability, (2) the survival rate of immature stages and (3) the proportion of female offspring at 15, 20, 25, 30 and 35°C. To obtain these data, single teleiochrysalis females were placed with two male adults on a leaf disc (ca. 16 cm2) of common bean for copulation. The females were allowed to lay eggs for 5 days after the pre-oviposition period. The eggs obtained from each female were kept to determine the above-mentioned parameters after reaching adulthood.

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Demographic parameters Daily age-specific survival (lx) and fecundity (mx) rates were used to generate life tables for each species and temperature. The intrinsic rate of natural increase (rm) was P estimated from the life-fecundity table according to the equation given by Birch (1948): ½ erm x lx mx ¼ 1; where x is female age in days, lx is the age-specific survival rate [(the fraction of females surviving at age x) 9 (rate of egg hatchability) 9 (survival rate of immature stages)] and mx is the expected number of daughters produced per female alive at age x [(age-specific oviposition) 9 (proportion of females)] (Sabelis 1985b; Gotoh P and Gomi 2003; Gotoh et al. 2010). The net reproductive rate (R0) is given by [R0 = lxmx], the mean generation time (tG) in days is given by [tG = ln R0/rm], the finite rate of increase (k) is given by ½k ¼ erm ; and the doubling time (tD) in days is [tD = ln 2/rm]. After rm was computed from the original data (rall), the standard errors for the life-history parameters at different constant temperatures were estimated using the Jackknife method (Meyer et al. 1986; Maia et al. 2000). Briefly, one of the mites is omitted and rm (ri) is calculated for the remaining mites (n-1). Based on Meyer et al. (1986), the Jackknife pseudo-value (rj) is computed for this subset of the original data according to the equation [rj = n rall-(n-1) ri]. This process was repeated for all possible omissions of one mite from the original data set to produce pseudo-values which allowed for computing confidence limits for the parameter values. Developmental rate model Ikemoto and Takai’s (2000) linear model was used to obtain estimates of the lower temperature threshold and thermal constant. The law of total effective temperature applied to the temperature-dependent development of arthropods was expressed by the equation: 1 t 1 ¼  þ T; D k k where D, T, t, and k represent the duration of development (days), environmental (mean/ isothermal) temperature (8C), lower threshold temperature and thermal constant, respectively. The equation of the non-linear thermodynamic model is applied for a wide range of temperatures and the equation can be expressed as follows (Ikemoto 2005, 2008): h  i 1 1 A q½T½TU exp DH R ½TU   ½T        ; r¼ DHH 1 1 1 1 L þ exp   1 þ exp DH R ½TL  ½T  R ½TH  ½T  where r represents the development rate (the dependent variables) at the absolute temperature (T) (the independent variable). All other parameters are constants: [TL], [TH], and [TU] represent the absolute temperatures, DHA, DHL, and DHH represent enthalpy changes, R is the universal gas constant, and q is the developmental rate at [TU]. [TL] equals t, [TH] is the upper threshold temperature, and [TU] is the intrinsic optimum temperature for development that exhibits the minimum effects on enzyme inactivation related to development at low and high temperatures. Statistical analysis Data were analysed by means of analyses of covariance (ANCOVA), using temperature as the covariate. The purpose was to quantify relationships between the response variables

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(eggs/female, hatch rate, survival rate, sex ratio, oviposition period, adult longevity, developmental time from egg to adult, total oviposition, net reproductive rate, and intrinsic rate of increase) and predictor variables [species (S), gender (G) and temperature (T)] in order to identify which of the predictor variables contribute most to explain the variation in data. Specifically, the analyses aimed at identifying whether species is a significant predictor variable, because this implies that the two species differ with respect to their temperature responses. The full ANCOVA model for analyzing all response variables reads: y ¼ b0 þ b1 S þ b2 G þ b3 T þ b4 T 2 þ b5 SG þ b6 ST þ b7 ST 2 þ b8 GT þ b9 GT 2 þ b10 SGT þ b11 SGT 2 þ e; where y is the response variable, bi is the parameter associated with the i-th term, and e the residual error. All response variables were analyzed by means of Generalized Linear Models (McCullagh and Nelder 1989) using PROC GENMOD (Enterprise Guide 4.1, SAS Institute SAS 2006). The advantage of GENMOD is that it permits data with non-normal distributions. Proportions (sex ratio, hatch rate and survival rate) are likely to be binomially distributed, discrete numbers (eggs/female) to be distributed according to the Poisson or the negative binomial distribution, whereas the continuous variables (developmental duration, oviposition period, adult longevity, Ro and rm) are likely to be normally distributed. When needed, continuous variables were subjected to a logarithmic transformation in order to stabilize the variance and to ensure that the back-transformed values were non-negative. To test for differences between species with respect to temperature responses, we compared the deviance of the full model with the increase in deviance resulting from omitting species from the full model. The difference was tested by means of Manly’s (1990) test: Fm1 ;m2 ¼

ðD1  D2 Þ=ðp2  p1 Þ ; D2 =ðN  p2  1Þ

where D1 and D2 denote the deviance of the reduced and the full model, respectively, p1 and p2 are the number of parameters of the reduced and full model, and N is the total number of observations in the data set. The degrees of freedom were calculated as m1 = p2-p1 and m2 = N - p2 - 1. Likewise, the effects of temperature and gender were assessed by comparing deviances of models with and without temperature and gender, respectively. Polynomial regression models with first, second and, in some cases, third order terms of temperature as predictor variables were fitted to data for each species separately.

Results Reproduction The pre-oviposition period decreased with increasing temperatures from 15 to 25°C for T. merganser and from 15 to 30°C for T. kanzawai (Appendixes 1, 2). The pre-oviposition period, oviposition period, post-oviposition period, adult longevity and daily egg production (eggs/female/day) were strongly affected by temperature, but with significant differences between the two species (Tables 1, 2; Fig. 1). Total fecundity (eggs/female)

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Normale

Neg. binl

Egg-to-adult development

Eggs/female for 5-day oviposition

Normal

Intrinsic rate of increase (rm)

)

) )

0.46 (F5,408 = 978.2

)

***

1.05 (F5,408 = 11140***)

)

***

427.8 (F5,408 = 313364

44.7 (F5,408 = 255.1

)

)

***

***

50.6 (F5,408 = 256.3

296.6 (F5,327 = 20.3

***

541.6 (F5,327 = 21.3***)

440.0 (F5,327 = 34.4

***

572.0 (F5,327 = 18658

***

10.7 (F11,1679 = 8044***)

Full modelb

)

)

438.7 (F4,408 = 2.59 ) 6.03 (F4,408 = 1222.2

)

***

138.6 (F4,408 = 13352***)

)

***

184.2 (F4,408 = 318.2 *

)

)

***

207.2 (F4,408 = 315.6

365.4 (F4,327 = 18.9

***

700.5 (F4,327 = 24.0***)

670.1 (F4,327 = 42.8

***

4107.2 (F4,327 = 505.2

***

566.1 (F8,1679 = 10888***)

Full model excl. Temperaturec

0.55 (F3,408 = 25.6***)

32.0 (F3,408 = 4007***)

433.9 (F3,408 = 1.94)

48.4 (F3,408 = 11.2***)

62.7 (F3,408 = 32.3***)

340.0 (F3,327 = 15.9***)

577.3 (F3,327 = 7.19***)

443.1 (F3,327 = 0.76)

806.2 (F3,327 = 44.6***)

22.9 (F6,1679 = 319.7***)

Full model excl. Speciesd

Full model also includes gender and its interactions with species and temperature

Dependent variable was subjected to a logarithmic transformation prior to analysis

The link function used in PROC GENMOD is the logit function

The link function used in PROC GENMOD is the logarithmic function

The F test measures whether the increase in deviance by omitting species from the full model is significant

The F test measures whether the increase in deviance by omitting temperature from the full model is significant

* P \ 0.05, ** P \ 0.01, *** P \ 0.001

h

g

f

e

d

c

Full model includes species, temperature, temperature2 and their interactions except adult longevity (see below). The F test measures whether the full model is significantly better than the null model (i.e. a model without any predictor variables)

b

6.03

144.5

1643289.6

184.5

209.6

388.9

718.2

671.5

163774.9

574.9

Null model

Deviancea

Deviance is measure of model quality. The lower the deviance relative to the deviance of the null model is, the better the fit

Normalg

a

Neg. bin.

e

Total oviposition/female

Normal

g

Normal

g

Binomial

Net reproduction rate (R0)

Adult longevity

h

Oviposition period

Sex ratio for 5-day oviposition

f

Binomial

Binomialf

Hatch rate for 5-day oviposition

Juv. survival rate for 5-day oviposition

f

e

Distribution

Response variable

Table 1 Results of the statistical analyses based on PROC GENMOD

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b

b

184

184

184

184

184

153

153

153

153

799

n

a

c

b

a

2

y = 0.524(0.099) - 0.086(0.013)T ? 0.0048(0.0005)T - 0.00007(0.000007)T3

2

y = - 0.152(0.043) ? 0.395(0.004)T - 0.0078(0.0001)T

y = 1.130(0.441) ? 0.297(0.037)T - 0.0057(0.0007)T

2 2

2

y = 4.062(0.392) - 0.0188(0.033)T - 0.00010(0.0007)T

y = 3.527(0.422) ? 0.0072(0.036)T - 0.0014(0.0007)T

2

y = - 0.840(0.780) ? 0.224(0.061)T - 0.0048(0.0011)T

2

y = - 2.134(1.806) ? 0.503(0.135)T - 0.0110(0.0024)T

y = 1.056(1.996) ? 0.291(0.144)T - 0.0075(0.0025)T

2

y = -2.908(0.331) ? 0.442(0.026)T - 0.0068(0.0005)T

2

y = 7.293(0.045) - 0.301(0.004)T ? 0.0041(0.00007)T2

Link function

T. merganser

230

230

230

230

230

180

180

180

180

892

n

y = 1.224(0.118) - 0.178(0.015)T ? 0.0088(0.0006)T2 - 0.00013(0.000009)T3

y = - 3.557(0.055) ? 0.722(0.005)T - 0.015(0.001)T2

y = - 1.873(0.410) ? 0.616(0.035)T - 0.0133(0.0007)T2

y = 3.257(0.285) ? 0.066(0.024)T - 0.0031(0.0005)T2

y = 2.008(0.299) ? 0.160(0.025)T - 0.0051(0.0005)T2

y = - 0.678(0.415) ? 0.152(0.033)T - 0.0028(0.0006)T2

y = 3.454(1.354) ? 0.028(0.104)T - 0.0014(0.0019)T2

y = 2.687(1.232) ? 0.141(0.092)T - 0.0044(0.0017)T2

y = -3.153(0.300) ? 0.491(0.024)T - 0.0084(0.0005)T2

y = 5.706(0.042) - 0.196(0.003)T ? 0.0023(0.00006)T2

Link functiona

T. kanzawai

e Link-function is the logit function. Back-transformed values are obtained as y ¼ 1þe y

y

Link-function is the logarithmic function. Back-transformed values are obtained as y ¼ exp ðyÞ

The link function relates y to the expected value of the response variable. Values in parentheses give standard errors of the estimated parameters

All models were highly significant (P \ 0.0001). See Table 1 for more details

Intrinsic rate of increase (rm)

Net reproductive rate (R0)

Total oviposition/female

Adult longevity

b

Oviposition period

b

Sex ratio for 5-day oviposition

c

Juv. survival for 5-day oviposition

Hatch rate for 5-day oviposition

c

c

b

Eggs/female for 5-day oviposition

Egg-to-adult developmentb

Response variable

Table 2 Temperature responses of Tetranychus merganser and T. kanzawai. n is the number of observations

Exp Appl Acarol (2011) 54:1–19 7

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Fig. 1 Effect of temperature on mean durations of oviposition period, adult longevity and total fecundity in Tetranychus merganser and T. kanzawai. See Appendix 3 for further information. Points show the sample averages with 95% confidence limits. The heavy lines show the predictions based on the generalized linear models after eliminating non-significant terms. Thin lines show the 95% confidence limits for the predicted line. The models as well as total sample sizes are given in Table 2

was highest at 30°C for T. merganser and at 25°C for T. kanzawai (Appendix 3). Daily egg production (eggs/female/day) was highest at 30°C for both species. To calculate age-specific survival rate (lx) and fecundity rate (mx), number of eggs laid during the first 5 days of the oviposition period, their hatchability, survival rate of immature stages and the proportion of female offspring were recorded (Appendix 4). The effect of temperature on these variables was highly significant (P \ 0.0001). In most cases, performance increased with temperature to peak around 25–30°C followed by a steep decline at temperatures above 30°C (Fig. 2). The models describing the temperature response of each species separately are given in Table 2. Manly’s test showed that the two species can be considered as similar with respect to hatching rate, whereas they are significantly different with respect to all other response variables (Table 1). Development Development time from egg to adult differed between species but not between males and females within the species (Table 1; Fig. 3; Appendixes 1, 2). Ikemoto and Takai’s linear model, when fitted to values of developmental rates, gave a close fit to the data for the

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Fig. 2 Temperature effects on a number of eggs laid per female during the first 5 days of oviposition; b hatch rate from eggs to larvae; c survival rate from hatching to the adult stage; d sex ratio expressed as proportion of adults that are females. Points show the sample averages with 95% confidence limits. The heavy lines show the predictions based on the generalized linear models after eliminating non-significant terms. Thin lines show the 95% confidence limits for the predicted line. The models as well as total sample sizes are given in the Table 2

15–35°C range of temperatures (0.979 B r2 B 0.990) (Table 3; Fig. 4; Appendixes 1, 2). The estimated lower thresholds (t = TL) for egg-to-adult and for egg-to-egg development were very similar and the values were 12.2–12.3°C for T. merganser and 10.8°C for T. kanzawai (Table 3). The thermal constant (k) for the respective stages was 130.1, 124.4

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Fig. 3 Effect of temperature, sex and/or species on the developmental period from egg to adult in Tetranychus merganser and T. kanzawai at various temperatures. See Appendixes 1 and 2 for further information. Points show the sample averages with 95% confidence limits. The heavy lines show the predictions based on the generalized linear models after eliminating non-significant terms. Thin lines show the 95% confidence limits for the predicted line. The models as well as total sample sizes are given in Table 2

Table 3 Estimated values of constants in linear and non-linear models describing the relationship between temperature (°C) and developmental rates in Tetranychus merganser and T. kanzawai on bean leaf discsa Stage and species Law of total effective temperature linear model t (S. E.)

k (S. E.)

r2

Thermodynamic non-linear model

Linear model equation TU

TH

v2

Egg-to-female adult T. merganser

12.21 ± 0.43 130.12 ± 7.97

0.9901 y = 0.0077x - 0.0938 24.0

37.2

0.0013

T. kanzawai

10.81 ± 0.75 130.97 ± 10.32 0.9797 y = 0.0076x - 0.0826 25.0

38.7

0.0021

T. merganser

12.25 ± 0.39 124.42 ± 7.04

0.9902 y = 0.0080x - 0.0985 24.0

36.7

0.0013

T. kanzawai

10.81 ± 0.70 127.46 ± 9.46

0.9822 y = 0.0079x - 0.0848 25.0

38.8

0.0015

T. merganser

12.15 ± 0.44 144.42 ± 8.90

0.9882 y = 0.0069x - 0.0841 23.5

37.2

0.0010

T. kanzawai

10.78 ± 0.72 146.72 ± 11.16 0.9787 y = 0.0068x - 0.0735 25.0

38.5

0.0017

Egg-to-male adult

Egg-to-egg

a

t lower threshold temperature (°C; = TL), k thermal constant (°C), TH upper threshold temperature (°C), TU intrinsic optimum temperature (°C)

and 144.4 DD for T. merganser, and 131.0, 127.5 and 146.7 DD for T. kanzawai (Table 3). Ikemoto’s non-linear model, when fitted to values of developmental rates, gave a close fit to the data in the temperature range between 15 and 37.5°C (0.0010 B v2 B 0.0021) (Table 3; Fig. 4). The intrinsic optimum temperature (TU) for egg-to-female adult, for eggto-male adult and for egg-to-egg development was 23.5–25.0°C for both species (Table 3). The upper developmental thresholds (TH) for the respective stages were 36.7–38.8°C for

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Fig. 4 Ikemoto and Takai’s (2000) linear and thermodynamic (non-linear) models fitted to the temperaturedependent development of Tetranychus merganser and T. kanzawai. Circles show data points. Open circles indicate data points outside the range of the linear model. Squares show lower (t), middle (TU) and upper (TH) constant values estimated by non-linear model (see also Table 3)

both species. In fact, no eggs (0/120) of T. merganser and a few eggs (4/96) of T. kanzawai hatched at 40°C, and those that did hatch died during the larval stage. Demographic parameters The age-specific survival rate (lx) started to drop at earlier ages as the temperature increased from 15 to 35°C (Fig. 5). The age-specific fecundity rate (mx) peaked at earlier ages and the width of the peak, i.e. the oviposition period, became narrower as the temperature increased. In T. merganser, the first oviposition was observed on days 39, 19, 11, 8 and 7 at 15, 20, 25, 30 and 35°C, respectively. Daily egg production reached a peak of 3.2 eggs on day 55 at 15°C, 6.4 eggs on day 28 at 20°C, 12.5 eggs on day 15 at 25°C, 16.7 eggs on day 12 at 30°C, and 16.5 eggs on day 9 at 35°C. Female adults started to die on days 61, 31, 23, 14, and 11 at the respective temperatures. In T. kanzawai, the age at the first oviposition was on days 26, 16, 11, 7, and 6 at 15, 20, 25, 30, and 35°C, respectively. Daily egg production reached a peak of 4.1 eggs on day 37 at 15°C, 8.2 eggs on day 25 at 20°C, 15.3 eggs on day 18 at 25°C, 15.8 eggs on day 10 at 30°C, and 9.2 eggs on day 8 at 35°C. Female adults started to die on days 47, 32, 24, 13, and 10 at the respective temperatures. The net reproductive rate (R0), the intrinsic rate of natural increase (rm), and the mean generation time (tG) were affected by temperature and there were significant differences between the two species with respect to temperature responses (Tables 1, 2; Fig. 6). The highest R0 value was observed at 25°C in T. merganser (117.3) and T. kanzawai (146.1)

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Exp Appl Acarol (2011) 54:1–19

Fig. 5 Age-specific survival rate (lx upper panel) and age-specific fecundity rate (mx bottom panel) of females of Tetranychus merganser and T. kanzawai at different temperatures

(Appendix 5), whereas the lowest value was found at 35°C (55.6 and 18.6, respectively). The rm and k values increased with increasing temperature from 15 to 35°C in T. merganser, but peaked at 30°C in T. kanzawai. The peak values were 0.411 day-1 for T. merganser and 0.399 day-1 for T. kanzawai. Mean generation time (tG) and doubling time (tD) decreased with increasing temperature: tG ranged from 56.20 days at 15°C to 9.80 days at 35°C for T. merganser, whereas the corresponding values for T. kanzawai were 37.33 and 8.56 days. Likewise, tD declined from 9.69 days at 15°C to 1.69 days at 35°C for T. merganser and from 6.75 days at 15°C to 1.74 at 30°C for T. kanzawai (Appendix 5).

Discussion The present study shows that T. merganser and T. kanzawai developed successfully to adult over a temperature range of 15–35°C with a high pre-imaginal survival rate (C79.2%). At 37.5°C, eggs of the two species could hatch and reach adulthood, but their survival rates were about 50%. No larvae of either species developed to the next stage at 40°C. The results agree with the upper developmental threshold (TH) values (36.7–38.8°C), when extrapolated from data obtained in the present study at a temperature range of 15–37.5°C (Table 3). Development from egg to female adult in T. merganser at 15–30°C closely resembled that in T. okinawanus Ehara (38.5–6.8 days; Takafuji et al. 1996) and T. evansi Baker and Pritchard (45.1–6.9 days; Gotoh et al. 2010), which occur in tropical and sub-tropical zones. The outcome in T. kanzawai was closer to that in T. mcdanieli McGregor (23.0 days at 18°C to 9.3 days; Tanigoshi et al. 1975), T. pacificus McGregor (36.4–6.7 days), T. turkestani (Ugarov and Nilolski) (29.0–6.4 days), T. urticae Koch (green form) (25.8–6.1 days; Carey and Bradley 1982; 25.3–7.4 days; Bounfour and Tanigoshi 2001), and T. pueraricola (28.2–7.0 days; Gotoh et al. 2004), which mainly occur in temperate

123

Exp Appl Acarol (2011) 54:1–19

13

Fig. 6 Effect of temperature and/or species on demographic parameters of Tetranychus merganser and T. kanzawai. See Appendix 5 for further information. R0, net reproductive rate; rm, intrinsic rate of natural increase; tG, mean generation time; k, finite rate of increase. The heavy lines for R0 and rm show the predictions, based on the generalized linear models after eliminating non-significant terms. Thin lines show the 95% confidence limits for the predictions. The models as well as total sample sizes are given in the Table 2

zones. The lower threshold temperature (t) calculated from the results of developmental duration is 12.2–12.3°C for T. merganser and 10.8°C for T. kanzawai (Table 3). The t-value of T. merganser is close to that of seven strains of T. evansi (11.9–12.5°C) (Gotoh et al. 2010), but slightly higher than that of T. urticae red form (9.9°C; Ito 1974), T. urticae green form (10.0°C; Uchida 1982), T. okinawanus (11.6°C; Takafuji et al. 1996) and T. pueraricola (10.8°C; Gotoh et al. 2004).

123

14

Exp Appl Acarol (2011) 54:1–19

Generally, life-history parameters from different studies are difficult to compare, as differences can be due to the organisms as well as the experimental methodology, for instance the type of rearing method, environmental conditions other than temperature like humidity, photoperiod and so on, and inclusion or exclusion in life-history calculations of aspects such as survival of eggs to adult stage and sex ratio (Bonato 1999; Ferrero et al. 2007). Nevertheless, Sabelis (1985a, 1991), in an extensive review of life-history parameters of tetranychid mites, found rm-values for Tetranychus mites to range from 0.200 to 0.336 day-1 at ca. 25°C. The rm-values of T. merganser and T. kanzawai fall within this range. The rm-values of T. merganser increased with increasing temperature from 15°C (rm = 0.072 day-1) to 35°C (0.411 day-1) without any decline as seen in T. mcdanieli (Tanigoshi et al. 1975) and T. evansi (Gotoh et al. 2010). On the other hand, the rm-value of T. kanzawai increased from 15°C (rm = 0.104 day-1) to 30°C (0.399 day-1), but the value declined at 35°C (0.348 day-1) suggesting that T. merganser is better adapted to hot weather than T. kanzawai. The rm-value of T. kanzawai at 25°C ranged from 0.187 to 0.283 day-1 when reared on five different host plants (Gotoh and Gomi 2003). The rm-value (0.282 day-1) obtained in the present study is consistent with the previously reported values, indicating the consistency of our experimental procedures. At around 25°C, the rm-values for Tetranychus species were 0.245 for T. mcdanieli (Tanigoshi et al. 1975), 0.207, 0.204 and 0.219 for T. pacificus, T. turkestani and T. urticae green form, respectively (Carey and Bradley 1982), 0.316 for T. okinawanus (Takafuji et al. 1996), 0.299 for T. pueraricola (Gotoh et al. 2004), and 0.265–0.277 day-1 for T. evansi (Gotoh et al. 2010). Bounfour and Tanigoshi (2001) reported the rm-value for T. urticae green form (0.188 day-1), which was much lower than for other Tetranychus species because of its longer developmental duration (13.9 vs. ca. 10 days). The rm-values of T. merganser and T. kanzawai examined in the present study are slightly lower than those of T. okinawanus and T. pueraricola, but their values are comparable to those of other Tetranychus species, which are serious pests in many crops. Thus, the reproductive traits of T. merganser are similar to those of other pest mite species and since its total fecundity at temperatures above 30°C exceeds that of T. kanzawai, it suggests that T. merganser has the potential to become a serious pest. Tetranychus evansi is an invasive species that has spread rapidly since the mid 1990s throughout the world and has become an important pest species on solanaceous crops in the invaded countries (Gotoh et al. 2009, 2010). Like T. evansi, T. merganser may become a serious hazard if it succeeds to establish in Japan. Therefore, strong quarantine measures should be implemented in order to prevent this potential pest from entering Japan. Acknowledgments The authors are grateful to Dr. C. H. W. Flechtmann, University of Sao Paulo, for helping us to identify T. merganser correctly, Dr. N. Hinomoto, National Institute of Agrobiological Sciences, for his kind help on data analysis, Mr. M. Masaki, Plant Protection Office, for providing information on T. merganser, and Dr. Y. Kitashima, Ibaraki University, for his kind help in this research.

123

b

a

58

17

56

30

33

10

$

#

$

#

$

#

61

32

$

#

56

28

$

#

68

39

30

#

$

52

$

#

52

31

$

2.6 ± 0.04 1.0 ± 0.14 0.5 ± 0.00

2.4 ± 0.03 0.8 ± 0.04 0.4 ± 0.02

2.4 ± 0.05 0.8 ± 0.06 0.4 ± 0.04

2.5 ± 0.02 0.6 ± 0.03 0.5 ± 0.02

2.6 ± 0.14 0.7 ± 0.06 0.5 ± 0.03

2.5 ± 0.02 0.8 ± 0.03 0.5 ± 0.02

3.0 ± 0.03 0.8 ± 0.05 0.6 ± 0.03

2.7 ± 0.03 0.9 ± 0.03 0.6 ± 0.02

3.7 ± 0.05 1.0 ± 0.04 0.7 ± 0.05

3.7 ± 0.03 1.1 ± 0.03 0.7 ± 0.03

4.6 ± 0.09 1.1 ± 0.07 0.8 ± 0.07

4.2 ± 0.05 1.4 ± 0.06 0.9 ± 0.05

5.5 ± 0.09 1.6 ± 0.10 1.1 ± 0.06

5.0 ± 0.02 2.0 ± 0.00 1.1 ± 0.05

8.3 ± 0.09 1.8 ± 0.12 1.6 ± 0.09

8.1 ± 0.08 2.2 ± 0.08 1.4 ± 0.07

21 13.0 ± 0.13 3.4 ± 0.21 2.1 ± 0.10

#

#

26 16.9 ± 0.13 6.1 ± 0.29 2.6 ± 0.17

62 12.1 ± 0.06 4.3 ± 0.09 2.0 ± 0.07

#

$

Number of eggs tested

0.5 ± 0.04

0.5 ± 0.02

0.5 ± 0.03

0.5 ± 0.02

0.5 ± 0.03

0.5 ± 0.02

0.6 ± 0.04

0.7 ± 0.03

0.6 ± 0.04

0.7 ± 0.03

1.0 ± 0.08

0.8 ± 0.05

0.9 ± 0.06

1.0 ± 0.02

1.3 ± 0.08

1.8 ± 0.06

2.1 ± 0.07

2.4 ± 0.07

2.9 ± 0.11

3.2 ± 0.09

0.5 ± 0.00

0.5 ± 0.02

0.4 ± 0.04

0.5 ± 0.02

0.4 ± 0.05

0.5 ± 0.02

0.6 ± 0.04

0.6 ± 0.03

0.7 ± 0.05

0.7 ± 0.03

0.7 ± 0.10

0.7 ± 0.05

1.0 ± 0.03

1.0 ± 0.00

1.4 ± 0.09

1.4 ± 0.07

2.1 ± 0.08

2.2 ± 0.05

2.8 ± 0.12

2.6 ± 0.09

0.7 ± 0.08

0.8 ± 0.03

0.6 ± 0.04

0.5 ± 0.01

0.5 ± 0.03

0.6 ± 0.03

0.6 ± 0.05

0.7 ± 0.03

0.7 ± 0.05

0.9 ± 0.03

0.7 ± 0.07

1.1 ± 0.04

1.0 ± 0.03

1.0 ± 0.05

1.5 ± 0.09

2.1 ± 0.08

2.4 ± 0.11

3.0 ± 0.05

3.2 ± 0.09

3.9 ± 0.11

0.5 ± 0.03

0.6 ± 0.02

0.5 ± 0.00

0.5 ± 0.01

0.6 ± 0.04

0.7 ± 0.03

0.7 ± 0.05

0.6 ± 0.02

0.8 ± 0.04

1.0 ± 0.02

0.8 ± 0.08

1.2 ± 0.05

1.2 ± 0.09

1.5 ± 0.07

1.4 ± 0.09

1.8 ± 0.06

2.5 ± 0.13

2.3 ± 0.08

3.7 ± 0.19

3.7 ± 0.12 38.1 ± 0.55

6.2 ± 0.23

6.0 ± 0.07 0.6 ± 0.03

5.5 ± 0.07

5.5 ± 0.04 0.9 ± 0.03

5.6 ± 0.16

6.1 ± 0.04 0.6 ± 0.03

6.7 ± 0.09

6.7 ± 0.05 0.8 ± 0.04

8.3 ± 0.12

8.8 ± 0.05 0.7 ± 0.03

9.8 ± 0.12

10.4 ± 0.10 0.8 ± 0.05

12.4 ± 0.09

12.8 ± 0.09 1.3 ± 0.07

17.3 ± 0.23

18.8 ± 0.19 2.0 ± 0.09

27.8 ± 0.30

28.2 ± 0.19 2.8 ± 0.12

44.8 [96]

89.6 [96]

87.2 [86]

96.9 [96]

87.5 [96]

89.2 [120]

85.4 [96]

86.5 [96]

86.5 [96]

73.3 [86]b

Preoviposition % Immature period survival

38.7 ± 0.36 3.4 ± 0.11

Protochrysalis Protonymph Deutochrysalis Deutonymph Teleiochrysalis Egg-toadult

37 15.7 ± 0.14 6.8 ± 0.21 2.8 ± 0.08

Larva

$

Na Egg

Number of individuals tested

37.5

35

32.5

30

27.5

25

22.5

20

17.5

15

Temperature (°C)

Table 4 Developmental duration (days ± S. E.) from egg to adult, preoviposition period (days ± S. E.) and percentage (%) of immature survival (egg to adult) of Tetranychus merganser on bean leaf discs at various temperatures under a 16L:8D photoperiod

Appendix 1

Exp Appl Acarol (2011) 54:1–19 15

123

123

b

a

57

40

61

40

39

19

$

#

$

#

$

#

61

34

$

#

61

40

$

#

55

37

36

#

$

61

$

#

53

39

$

#

2.5 ± 0.03 0.5 ± 0.03 0.5 ± 0.02

2.5 ± 0.02 0.5 ± 0.03 0.5 ± 0.02

2.5 ± 0.02 0.4 ± 0.03 0.5 ± 0.02

2.4 ± 0.03 0.5 ± 0.02 0.5 ± 0.01

2.5 ± 0.03 0.5 ± 0.02 0.5 ± 0.04

2.5 ± 0.02 0.6 ± 0.24 0.5 ± 0.03

2.8 ± 0.04 0.7 ± 0.05 0.6 ± 0.03

2.7 ± 0.03 0.6 ± 0.03 0.6 ± 0.02

3.8 ± 0.04 0.8 ± 0.04 0.7 ± 0.04

3.6 ± 0.03 0.9 ± 0.03 0.7 ± 0.03

4.7 ± 0.08 1.0 ± 0.03 0.7 ± 0.08

4.4 ± 0.07 1.0 ± 0.04 0.9 ± 0.06

5.8 ± 0.07 1.1 ± 0.08 1.1 ± 0.05

5.5 ± 0.07 1.1 ± 0.06 1.2 ± 0.05

7.5 ± 0.09 1.7 ± 0.08 1.0 ± 0.06

7.0 ± 0.05 2.0 ± 0.07 0.9 ± 0.06

39 10.2 ± 0.10 2.2 ± 0.09 2.0 ± 0.05

40 10.6 ± 0.12 1.7 ± 0.10 1.9 ± 0.06

$

37 11.6 ± 0.14 2.7 ± 0.15 2.1 ± 0.09

#

43 11.3 ± 0.10 2.6 ± 0.10 2.1 ± 0.06

Number of eggs tested

0.4 ± 0.03

0.4 ± 0.02

0.3 ± 0.04

0.5 ± 0.01

0.4 ± 0.03

0.4 ± 0.03

0.5 ± 0.03

0.5 ± 0.02

0.6 ± 0.03

0.6 ± 0.03

0.8 ± 0.09

0.8 ± 0.06

0.9 ± 0.06

1.0 ± 0.03

1.1 ± 0.06

1.2 ± 0.05

1.2 ± 0.08

1.4 ± 0.10

1.5 ± 0.12

1.8 ± 0.09

0.5 ± 0.02

0.5 ± 0.01

0.5 ± 0.02

0.5 ± 0.01

0.4 ± 0.03

0.5 ± 0.02

0.5 ± 0.03

0.5 ± 0.02

0.7 ± 0.04

0.7 ± 0.03

1.0 ± 0.10

0.8 ± 0.06

1.1 ± 0.05

1.0 ± 0.04

1.4 ± 0.09

1.4 ± 0.07

1.9 ± 0.05

2.0 ± 0.05

2.2 ± 0.08

2.1 ± 0.05

0.5 ± 0.03

0.5 ± 0.02

0.4 ± 0.04

0.5 ± 0.02

0.5 ± 0.02

0.5 ± 0.02

0.6 ± 0.03

0.7 ± 0.03

0.6 ± 0.03

0.8 ± 0.03

0.9 ± 0.10

1.1 ± 0.06

0.9 ± 0.05

1.2 ± 0.05

1.2 ± 0.08

1.3 ± 0.07

1.3 ± 0.08

1.7 ± 0.08

1.8 ± 0.09

2.0 ± 0.06

0.5 ± 0.04

0.6 ± 0.02

0.5 ± 0.02

0.6 ± 0.02

0.6 ± 0.02

0.6 ± 0.03

0.5 ± 0.03

0.7 ± 0.03

0.8 ± 0.04

0.9 ± 0.03

0.5 ± 0.08

0.9 ± 0.06

1.2 ± 0.08

1.2 ± 0.05

1.3 ± 0.10

1.7 ± 0.06

2.3 ± 0.08

2.3 ± 0.08

2.6 ± 0.09

2.8 ± 0.07

5.4 ± 0.08

5.6 ± 0.06 0.7 ± 0.03

5.1 ± 0.04

5.3 ± 0.04 0.7 ± 0.03

5.4 ± 0.04

5.6 ± 0.04 0.7 ± 0.03

6.2 ± 0.09

6.3 ± 0.05 0.7 ± 0.03

7.8 ± 0.08

8.2 ± 0.06 0.9 ± 0.04

9.5 ± 0.09

9.8 ± 0.10 1.1 ± 0.05

12.0 ± 0.11

12.1 ± 0.07 1.5 ± 0.07

15.1 ± 0.10

15.6 ± 0.09 1.6 ± 0.07

20.9 ± 0.20

21.7 ± 0.22 2.5 ± 0.11

24.4 ± 0.40

48.3 [120]

84.2 [120]

80.8 [120]

79.2 [120]

84.2 [120]

95.8 [96]

80.8 [120]

95.8 [96]

82.3 [96]

83.3 [96]b

Preoviposition % Immature period survival

24.5 ± 0.21 3.1 ± 0.14

Protochrysalis Protonymph Deutochrysalis Deutonymph Teleiochrysalis Egg-toadult

#

Larva

$

Na Egg

Number of individuals tested

37.5

35

32.5

30

27.5

25

22.5

20

17.5

15

Temperature (°C)

Table 5 Developmental duration (days ± S. E.) from egg to adult, preoviposition period (days ± S. E.) and percentage (%) of immature survival (egg to adult) of Tetranychus kanzawai on bean leaf discs at various temperatures under a 16L:8D photoperiod

Appendix 2

16 Exp Appl Acarol (2011) 54:1–19

Exp Appl Acarol (2011) 54:1–19

17

Appendix 3

Table 6 Mean duration (days ± S. E.) of adult phases and longevity, and oviposition rates (mean ± S. E.) in Tetranychus merganser and T. kanzawai on bean leaf discs at five temperatures under a 16L:8D photoperiod Temperature Species

15°C 20°C 25°C 30°C 35°C a

Na Oviposition

PostLongevity oviposition

Total eggs/ female

Egg/$/day

T. merganser 37 29.0 ± 1.52 4.1 ± 0.52

36.3 ± 1.47

76.1 ± 4.90

2.6 ± 0.08

T. kanzawai

35.7 ± 1.34

86.7 ± 5.44

3.1 ± 0.12

43 27.4 ± 1.25 5.2 ± 0.59

T. merganser 36 26.1 ± 3.07 2.1 ± 0.46

30.1 ± 3.20 115.3 ± 10.35

5.2 ± 0.30

T. kanzawai

28.3 ± 1.34 149.3 ± 7.00

6.5 ± 0.12

52 23.1 ± 1.11 3.6 ± 0.51

T. merganser 28 19.8 ± 1.74 1.1 ± 0.47

22.0 ± 1.80 143.9 ± 10.49

8.1 ± 0.65

T. kanzawai

47 19.3 ± 0.83 2.7 ± 0.39

23.2 ± 0.91 198.5 ± 7.96

10.4 ± 0.20

T. merganser 44 11.5 ± 0.58 1.7 ± 0.37

13.7 ± 0.74 146.2 ± 6.35

13.0 ± 0.35

T. kanzawai

44

8.4 ± 0.35 1.0 ± 0.21

10.2 ± 0.42

93.3 ± 4.39

11.2 ± 0.28

T. merganser 39

8.0 ± 0.29 0.0 ± 0.03

9.0 ± 0.40

94.4 ± 4.64

11.8 ± 0.32

T. kanzawai

4.0 ± 0.23 1.6 ± 0.22

6.4 ± 0.29

27.6 ± 2.74

6.7 ± 0.31

44

Number of females tested

Appendix 4

Table 7 Number of eggs laid during the first 5 days of the oviposition period, hatchability of eggs, survival rate of immature stages and the proportion of females reaching adulthood (mean ± S. E.) of Tetranychus merganser and T. kanzawai on bean leaf discs at five temperatures under a 16L:8D photoperiod Temperature 15°C 20°C 25°C 30°C 35°C a

Species

Na

No. of eggs laid

% Hatch

% Survival

% Female

T. merganser

24

10.17 ± 0.39

94.14 ± 1.42

93.82 ± 1.38

82.92 ± 1.34

T. kanzawai

33

13.00 ± 0.50

97.60 ± 0.80

97.30 ± 0.90

72.00 ± 1.20

T. merganser

31

23.42 ± 0.91

98.98 ± 0.37

97.98 ± 0.62

83.82 ± 0.74

T. kanzawai

44

21.40 ± 0.50

97.80 ± 0.40

97.50 ± 0.40

78.40 ± 1.10

T. merganser

38

44.66 ± 1.59

99.37 ± 0.20

97.38 ± 0.63

84.23 ± 0.87

T. kanzawai

37

49.30 ± 0.90

96.70 ± 0.50

96.10 ± 0.70

79.20 ± 1.30

T. merganser

34

75.91 ± 1.24

93.73 ± 0.64

95.02 ± 0.63

83.37 ± 0.96

T. kanzawai

34

61.40 ± 1.60

95.40 ± 0.30

96.00 ± 0.30

79.00 ± 0.40

T. merganser

26

62.62 ± 2.49

90.18 ± 1.06

87.48 ± 1.76

74.69 ± 2.30

T. kanzawai

32

37.30 ± 1.70

90.30 ± 0.40

93.90 ± 0.60

76.80 ± 0.50

Number of females tested

123

18

Exp Appl Acarol (2011) 54:1–19

Appendix 5 Table 8 Demographic parameters (mean ± S. E.) of Tetranychus merganser and T. kanzawai on bean leaf discs at five temperatures under a 16L:8D photoperiod: net reproductive rate (R0), intrinsic rate of natural increase (rm, day-1), mean generation time (tG, day), finite rate of increase (k), doubling time (tD, day) Temper- Species ature 15°C 20°C

a

k

tD

55.71 ± 0.10 0.072 ± 0.002 56.20 ± 0.81 1.075 ± 0.001 9.69 ± 0.14

43

46.08 ± 0.05 0.104 ± 0.003 37.33 ± 0.60 1.109 ± 0.002 6.75 ± 0.11

T. merganser 36

97.12 ± 0.24 0.158 ± 0.005 29.26 ± 0.51 1.172 ± 0.004 4.43 ± 0.08

52 109.36 ± 0.09 0.181 ± 0.002 26.03 ± 0.15 1.198 ± 0.001 3.84 ± 0.02

T. merganser 28 117.25 ± 0.32 0.279 ± 0.009 17.31 ± 0.37 1.322 ± 0.009 2.52 ± 0.05 47 146.11 ± 0.13 0.282 ± 0.003 17.70 ± 0.13 1.326 ± 0.003 2.46 ± 0.02

T. merganser 44 108.09 ± 0.10 0.379 ± 0.005 12.38 ± 0.09 1.462 ± 0.004 1.83 ± 0.01 T. kanzawai

35°C

tG

T. merganser 37

T. kanzawai 30°C

rm

T. kanzawai T. kanzawai 25°C

Na R0

44

67.35 ± 0.07 0.399 ± 0.006 10.57 ± 0.09 1.491 ± 0.005 1.74 ± 0.02

T. merganser 39

55.62 ± 0.07 0.411 ± 0.006

9.80 ± 0.09 1.509 ± 0.005 1.69 ± 0.02

T. kanzawai

18.55 ± 0.04 0.348 ± 0.013

8.56 ± 0.18 1.418 ± 0.011 2.03 ± 0.04

44

Number of females tested

References Birch LC (1948) The intrinsic rate of natural increase of an insect population. J Anim Ecol 17:15–26 Bolland HR, Gutierrez J, Flechtman CHW (1998) World catalogue of the spider mite family (Acari: Tetranychidae). Brill Academic Publisher, Leiden, p 392 Bonato O (1999) The effect of temperature on life history parameters of Tetranychus evansi (Acari: Tetranychidae). Exp Appl Acarol 23:11–19 Bonato O, Cotton D, Kreiter S, Gutierrez J (1990) Influence of temperature on the life-history parameters of the yellow grape-vine mite Eotetranychus carpini (Oudemans) (Acari: Tetranychidae). Int J Acarol 16:241–245 Bounfour M, Tanigoshi LK (2001) Effect of temperature on development and demographic parameters of Tetranychus urticae and Eotetranychus carpini borealis (Acari: Tetranychidae). Ann Entomol Soc Am 94:400–404 Carey JR, Bradley JW (1982) Developmental rates, vital schedules, sex-ratios and life tables for Tetranychus urticae, T. turkestani and T. pacificus (Acarina: Tetranychidae) on cotton. Acarologia 23:333–345 Ehara S, Gotoh T (eds) (2009) Colored guide to the plant mites of Japan. Zenkoku-Noson-Kyoiku-Kyokai, Tokyo, p 349 Ferrero M, de Moraes GJ, Kreiter S, Tixier MS, Knapp M (2007) Life tables of the predatory mite Phytoseiulus longipes feeding on Tetranychus evansi at four temperatures (Acari: Phytoseiidae, Tetranychidae). Exp Appl Acarol 41:45–53 Gotoh T, Gomi K (2003) Life-history traits of the Kanzawa spider mite Tetranychus kanzawai (Acari: Tetranychidae). Appl Entomol Zool 38:7–14 Gotoh T, Suwa A, Kitashima Y, Rezk HA (2004) Developmental and reproductive performance of Tetranychus pueraricola Ehara and Gotoh (Acari: Tetranychidae) at four constant temperatures. Appl Entomol Zool 39:675–682 Gotoh T, Araki R, Boubou A, Migeon A, Ferragut F, Navajas M (2009) Evidence of co-specificity between Tetranychus evansi and T. takafujii (Acari: Prostigmata, Tetranychidae): comments on taxonomical and agricultural aspects. Int J Acarol 35:485–501 Gotoh T, Sugimoto N, Pallini A, Knapp M, Hernandez-Suarez E, Ferragut F, Ho CC, Migeon A, Navajas M, Nachman G (2010) Reproductive performance of seven strains of the tomato red spider mite Tetranychus evansi (Acari: Tetranychidae) at five temperatures. Exp App Acarol 52:239–259

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Ikemoto T (2005) Intrinsic optimum temperature for development of insects and mites. Environ Entomol 34:1377–1387 Ikemoto T (2008) Tropical malaria does not mean hot environments. J Med Entomol 45:963–969 Ikemoto T, Takai K (2000) A new linearized formula for the law of total effective temperature and the evaluation of line-fitting methods with both variables subject to error. Environ Entomol 29:671–682 Ito H (1974) Influence of temperature upon the incubation period and the time required for development from hatching to adult carmine mite, Tetranychus cinnabarinus (Boisduval) (Acarina: Tetranychidae). Bull Kanagawa Hort Exp Stn 22:120–123 (in Japanese) Janssen A, Sabelis MW (1992) Phytoseiid life-histories, local predator-prey dynamics, and strategies for control of tetranychid mites. Exp Appl Acarol 14:233–250 Laing JE (1969) Life history and life table of Tetranychus urticae Koch. Acarologia 11:33–42 Maia AHN, Luiz AJB, Campanhola C (2000) Statistical inference on associated fertility life table parameters using jackknife technique: computational aspects. J Econ Entomol 93:511–518 Manly BFJ (1990) Stage-structured populations: sampling analysis and simulation. Chapman & Hall, London, p 187 Masaki M (1991) A list of Acarina intercepted in plant quarantine. Res Bull Pl Prot Japan 27:87–92 (in Japanese with an English summary) Masaki M, Kitamura H (2004) A list of intercepted tetranychoid mites (Acari: Tetranychoidae) on imported plants at the plant quarantine of Narita Airport. Res Bull Pl Prot Japan 40:119–125 (in Japanese with an English summary) Masaki M, Hayase T, Miyajima S (1991) Notes on eight species of spider mites and predacious thrips intercepted on squash imported from USA, Mexico, Colombia and New Zealand. Res Bull Pl Prot Japan 27:107–114 (in Japanese with an English summary) McCullagh P, Nelder JA (1989) Generalized linear models. Monographs on statistics and applied probability 37, 2nd edn. Chapman & Hall, Boca Raton, p 511 Meyer JS, Ingersoll CC, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs bootstrap techniques. Ecology 67:1156–1166 Mori K, Nozawa M, Arai K, Gotoh T (2005) Life-history traits of the acarophagous lady beetle, Stethorus japonicus at three temperatures. BioControl 50:35–51 Navajas M, Gutierrez J, Williams M, Gotoh T (2001) Synonymy between two spider mite species, Tetranychus kanzawai and T. hydrangeae (Acari: Tetranychidae), shown by ribosomal ITS2 sequences and cross-breeding experiments. Bull Entomol Res 91:117–123 Perring TM, Holtzer TO, Kalisch JA, Norman JM (1984) Temperature and humidity effects on ovipositional rates, fecundity, and longevity of adult female Banks grass mites (Acari: Tetranychidae). Ann Entomol Soc Am 77:581–586 Roy M, Brodeur J, Cloutier C (2003) Temperature and sex allocation in a spider mite. Oecologia 135:322–326 Sabelis MW (1985a) Capacity for population increase. In: Helle W, Sabelis MW (eds) Spider mites: their biology natural enemies and control. Elsevier, Amsterdam, pp 35–41 Sabelis MW (1985b) Reproductive strategies. In: Helle W, Sabelis MW (eds) Spider mites: their biology natural enemies and control. Elsevier, Amsterdam, pp 265–278 Sabelis MW (1991) Life-history evolution of spider mites. In: Schuster R, Murphy PW (eds) The acari. Reproduction, development and life-history strategies. Chapman & Hall, London, pp 23–49 SAS (2006) SAS Enterprise Guide 4.1. SAS Institute Inc. SAS Campus Drive, Cary NC 27513 Takafuji A, Yokotsuka T, Goka K, Kishimoto H (1996) Ecological performance of the spider mite, Tetranychus okinawanus Ehara (Acari, Tetranychidae), a species newly described from Okinawa island (1). J Acarol Soc Jpn 5:75–81 Tanigoshi LK, Hoyt SC, Browne RW, Logan JA (1975) Influence of temperature on population increase of Tetranychus mcdanieli (Acarina: Tetranychidae). Ann Entomol Soc Am 86:972–986 Uchida M (1982) Ecological studies on the abundance and diapauses of spider mites and the damage caused by the spider mites in Japanese pear orchards. Spec Bull Tottori Fru Tree Exp Stn 2:1–63 (in Japanese)

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