Exp Appl Acarol (2012) 56:33–41 DOI 10.1007/s10493-011-9481-1
Effect of temperature on development and reproduction of Neoseiulus barkeri (Acari: Phytoseiidae) fed on Aleuroglyphus ovatus Bin Xia • Zhiwen Zou • Pengxin Li • Peng Lin
Received: 13 August 2010 / Accepted: 17 July 2011 / Published online: 27 July 2011 Ó Springer Science+Business Media B.V. 2011
Abstract The effect of five constant temperatures (16, 20, 24, 28 and 32°C) on the development, survival and reproduction of Neoseiulus barkeri Hughes fed on Aleuroglyphus ovatus Toupeau (Acari: Acaridae) was examined in the laboratory at 85% relative humidity. Development time of different immature stages decreased with increasing temperature, total egg-to-adult development time varied from 5.0 ± 0.13 to 17.5 ± 0.29 days. The lower thermal threshold for development was 9.7 ± 2.48°C and the thermal constant from egg to adult was 111.1 ± 12.34 degree-days. Pre- and post-oviposition period and female longevity all shortened as temperature increased. The longest oviposition period was observed at 24°C with 20.4 ± 1.13 days. At 20, 24, 28 and 32°C, mated females laid on average 0.7 ± 0.08, 1.5 ± 0.04, 1.6 ± 0.11 and 1.5 ± 0.11 eggs per day, respectively, but no eggs were laid at 16°C. Both the maximum fecundity (30.9 eggs per female) and the highest intrinsic rate of increase (rm = 0.166) were obtained at 28°C. The results of this study indicated that a mass rearing of N. barkeri with A. ovatus as prey is feasible at the appropriate temperature. Keywords Temperature Neoseiulus barkeri Development Female longevity Demographic parameter Aleuroglyphus ovatus
Introduction Neoseiulus barkeri Hughes (Acari: Phytoseiidae) is a predatory mite, which can feed on a wide range of foods such as spider mites, tarsonemid mites, storage mites, small arthropods and plant pollen (Ramakers and Van Lieburg 1982; Bakker and Sabelis 1989; van Houten 1991; Fan and Petitt 1994a, b; Momen 1994; Pen˜a and Obsorne 1996). The predator has a
B. Xia (&) Z. Zou P. Li P. Lin College of Life Science, Nanchang University, Nanchang 330031, China e-mail:
[email protected] B. Xia Institute of Life Science, Nanchang University, Nanchang 330031, China
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worldwide distribution and is very common in China, Japan, Thailand, USA, the northern part of Africa and many European countries (Xin 1988), and often inhabits citrus trees, mango trees and other plants, as well as storage products (Wu et al. 1997). Neoseiulus barkeri has been used to control pests in greenhouses and orchards since the techniques of its mass-rearing were developed and refined. In Denmark, N. barkeri reared on storage mites was utilized to successfully control onion thrips, Thrip tabaci Lindeman, on cucumber crops in commercial glasshouses (Hansen 1988) and there are other reports in which N. barkeri has been used for thrips control, mainly in greenhouse crops (Van der Staay 1984; Gillespie 1989; Hoy and Glenister 1991). Fan and Petitt (1994c) reported that augmentative releases of N. barkeri provided control of broad mite, Polyphagotarsonemus latus Banks. It has also been reported to control spider mites (Karg et al. 1987; Fan and Petitt 1994b; Momen and El-Borolossy 1997). In 2005 and 2006, mass production of N. barkeri on the storage mite Aleuroglyphus ovatus as a substitute food was initiated in Ganzhou, a city in the south of Jiangxi province. A survey of the mite fauna in commercial citrus orchards in the south of China revealed that N. barkeri was the most abundant phytoseiid species found in the vast majority of these orchards (Li et al. 2007). Therefore it was considered a well established indigenous predator. A functional response experiment showed that N. barkeri fed on A. ovatus exhibited a strong predatory ability on the spider mite Panonychus citri McGregor (Ling et al. 2008). Moreover, preliminary control experiments conducted in commercial citrus orchards indicated that N. barkeri fed on A. ovatus could efficiently control P. citri (Shu et al. 2007). Some research reports on the development and reproduction of N. barkeri have been published. For instance, Bonde (1989) reported population growth parameters of N. barkeri fed on T. tabaci at 25°C in the laboratory. Momen (1994) found that the age of mating females and food deprivation periods have a significant effect on reproduction of N. barkeri. Zhang and Fan (2005) examined the developmental and reproductive response of N. barkeri on Rhizoglyphus echinopus Fumouze et Robin and Tyrophagus putrescentiae Schrank. To assess the potential of a predator in a certain environment, information about the effects of abiotic factors such as temperature and relative humidity on development and reproduction is very important. The objective of this present work is to study an appropriate temperature range for mass rearing of the predator with A. ovatus as prey in order to increase native predator populations in commercial citrus orchards.
Materials and methods Mite colony Neoseiulus barkeri was originally collected from citrus orchards in Ganzhou, Jiangxi province and had been acclimated and propagated on the storage mite A. ovatus for 5 years in closed plastic containers. In this study, mites were maintained in rearing units (McMurtry and Scriveri 1964), consisting of a Petri dish (5 cm diameter) with a watersoaked foam plastic pad (3 cm diameter, 1 cm thick). On top of the pad was a piece of filter paper (3 cm diameter) with plastic film (2 cm diameter). The rearing units were kept in climate-controlled incubators (RXZ-260B) at 24 ± 0.5°C, 16D:8L photoperiod and 85% RH (controlled by YADU ultrasonic humidifier).
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Development of immature stages To obtain synchronized eggs for the experiments, 100 adult females of N. barkeri from the stock colony were placed in the rearing units with some storage mites as prey. The rearing units with the mites were maintained at 24 ± 0.5°C, 85% RH and 16D:8L photoperiod. Eggs laid by N. barkeri within 6 h were transferred to new rearing units with a fine camel hair brush, one in each unit. Thereafter, these new units were placed in climate-controlled incubators and the development of immature stages was recorded at 85% RH and five constant temperatures ranging from 16 to 32°C, at 4°C interval. Every day A. ovatus were added to each rearing unit to provide abundant prey for N. barkeri. The developmental stage of each individual was recorded every 12 h until they molted to adults. The relationship between temperature (T) and developmental rate (r, the reciprocal of developmental time [days]) was determined by a linear regression model: r = a ? bT, where a and b are regression coefficients and estimated by least-squares regression techniques. The lower thermal threshold for development (C) was estimated by extrapolating the regression line to the x-axis. The thermal constant K (the sum of degree-days required for development to maturity, DD) was estimated for each case as the slope reciprocal of the regression line. Standard errors of C and K were computed as in Campbell et al. (1974). Effect of temperature on longevity and reproduction Newly-molted adult female N. barkeri at 16, 20, 24, 28 and 32°C were singly transferred into rearing units, together with a single young male. Egg laying and survival of females were recorded daily and storage mites were added every day. Males that escaped from the rearing units or died were replaced by new ones. Females that happened to drown in the wet filter paper or died because of improper handling were excluded from data analysis. Parameters noted at each temperature were: preoviposition, oviposition, postoviposition period, adult female longevity, mean oviposition rate per female per day (daily fecundity), total ovipostion per female (fecundity) and offspring sex ratio. Life table parameters A life table was constructed from the observed survival and fecundity rates for individuals. Parameters at constant temperatures were calculated by the methods of Andrewartha and Birch (1954). The P intrinsic rate of increase (rm) was estimated by non linear regression according to: ðexpðrm xÞlx mx Þ ¼ 1 (Birch 1948), where rm is the intrinsic rate of increase, x is female age in days, lx is the fraction of females surviving to age x (agespecific survival rate), and mx is the expected number of daughters produced per female alive at age x (age-specific fecundity rate), obtained by multiplying the number of eggs by the age-specific sex ratio, which is defined as the proportion ofPfemales in the progeny lx mx , mean generation (Roy et al. 2002). Net reproductive rate (R0) is given by: R0 ¼ time (t) in days by: t ¼ ln R0 =rm , finite rate of increase (k) by: k ¼ erm , and doubling time (DT) by: DT ¼ ln 2=rm . Data analysis ANOVAs were used to detect the effect of temperature on developmental time of immature stages, durations of preoviposition, oviposition and postoviposition, longevity and
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fecundity. The sex ratios of the progeny were compared using v2 tests. Analyses were conducted using SPSS 13.0 (SPSS, 1989–2004).
Results Development of immature stages Over the range of temperatures tested, N. barkeri reared on A. ovatus successfully developed from egg to adult, but development of immature stages was influenced by temperature (Table 1). Egg developmental times increased significantly as temperature decreased (F4,218 = 65.81, P \ 0.001). Larval developmental times of N. barkeri were significantly influenced by temperature (F4,218 = 42.67, P \ 0.001). The developmental rate of all immature stages increased linearly with temperature (Table 2). The correlation coefficient in all developmental stages was very high (R2 [ 0.90), suggesting that the linear model accurately described the effect of temperature on developmental rate of N. barkeri. The lower threshold temperatures for egg, larva, and protonymph varied from 9.5 ± 1.21 to 10.8 ± 2.34°C (Table 2), and the thermal constant for completion of egg, larva and protonymph ranged from 20.0 ± 3.20 to 41.7 ± 3.68 degree-days (Table 2). The lower developmental threshold temperature (9.1°C) and thermal constant (16.7 degree-days) for deutonymphs were the lowest of all stages. Reproduction Adult females of N. barkeri did not lay any eggs at 16°C—for this reason N. barkeri females at 16°C were excluded from the fertility and life table analyses—, and the total number of eggs laid per female was significantly lower at 20°C than at other temperatures (Table 3; Least-significant difference test: P \ 0.05). Duration of the preoviposition period was significantly influenced by temperature (F3,89 = 12.86, P \ 0.001). Females had a significantly longer preovipostion period at 20°C than at other temperatures. The oviposition period was similar at 20, 24 and 28°C, but it was significantly shorter at 32°C (F3,89 = 26.47, P \ 0.001). The postoviposition period varied from 20.3 ± 1.75 to 7.8 ± 0.69 and was also influenced by temperature (F3,89 = 17.47, P \ 0.001). Daily egg production at 24, 28 and 32°C was similar, but it was significantly lower at 16°C (F3,89 = 26.47, P \ 0.001). The sex ratio of N. barkeri was female biased and varied from Table 1 Mean (±SE) developmental durations (days) of Neoseiulus barkeri at five temperatures (85% RH) Temperature (°C)
n
Egg
Larva
Protonymph
Deutonymph
Total immature
16
36
3.78 ± 0.49a
2.05 ± 0.13a
6.17 ± 0.25a
5.50 ± 0.31a
17.51 ± 0.29a 11.66 ± 0.31b
20
50
2.64 ± 0.27b
1.78 ± 0.20a
3.68 ± 0.21b
3.56 ± 0.22b
24
38
1.21 ± 0.13c
1.18 ± 0.10b
2.84 ± 0.20c
2.63 ± 0.19c
7.86 ± 0.38c
28
46
1.19 ± 0.09c
0.81 ± 0.08c
1.96 ± 0.21d
1.86 ± 0.15d
5.82 ± 0.29d
32
54
0.92 ± 0.07c
0.74 ± 0.06c
1.67 ± 0.13d
1.61 ± 0.13d
4.98 ± 0.13e
n Number of individuals tested Means within a column followed by the same letter are not significantly different (ANOVA followed by LSD test: P [ 0.05)
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Table 2 Mean (±SE) lower thermal threshold (C) and thermal constant (K) and estimates of the linear regression of various stages of Neoseiulus barkeri on Aleuroglyphus ovatus Stage
C (°C)
Egg Larva
K (degree-days)
R2
Equation
9.5 ± 1.21
41.67 ± 3.68
R = -0.228 ? 0.024 T
0.903
9.89 ± 1.11
35.71 ± 2.55
R = -0.277 ? 0.028 T
0.982
Protonymph
10.78 ± 2.34
20.00 ± 3.20
R = -0.539 ? 0.050 T
0.922
Deutonymph
9.12 ± 1.88
16.67 ± 1.94
R = -0.547 ? 0.060 T
0.956
Total development
9.67 ± 2.48
111.11 ± 12.34
R = -0.087 ? 0.009 T
0.988
Table 3 Mean (±SE) preovipostional, ovipostional and postovipositional periods, longevity, fecundity and sex ratio of Neoseiulus barkeri at five constant temperatures (85% RH) Parameter
Temperature (°C) 16 (n = 30)
20 (n = 30)
24 (n = 28)
28 (n = 26)
32 (n = 25)
No. eggs/female
0
10.67 ± 0.65a
30.64 ± 1.67b
30.85 ± 1.56b
20.52 ± 2.23c
No. eggs/female/day
0
0.65 ± 0.08a
1.53 ± 0.04b
1.64 ± 0.11b
1.47 ± 0.11b
Preoviposition period
–
5.37 ± 0.49a
2.68 ± 0.25b
2.08 ± 0.21b
1.88 ± 0.25b
Oviposition period
–
19.33 ± 0.96a
20.39 ± 1.13a
19.81 ± 1.12a
13.84 ± 1.08b
Postoviposition period
–
20.27 ± 1.75a
11.50 ± 0.70b
8.65 ± 0.84c
7.84 ± 0.69c
Total adult longevity (days)
48.10 ± 4.14a
45.47 ± 1.53a
34.57 ± 1.53b
30.58 ± 1.10b
23.72 ± 1.09c
Sex ratio (% daughters)
–
64
66.67
60.87
59.26
n Number of individuals tested Means within a row followed by the same letters were not significantly different (LSD test: P [ 0.05)
59.3 to 66.7% daughters, with the highest value recorded at 24°C; it was not significantly influenced by temperature (v2 = 1.60, df = 3, P = 0.66; n = 224). Age-specific survival and fecundity rate The rates of age-specific survival (lx) and fecundity (mx) of N. barkeri were greatly influenced by temperature (Fig. 1). Age-specific survival rate (lx) started to drop at earlier ages as the temperature increased from 20 to 32°C (Fig. 1, dotted lines). The first death of an adult female occurred on day 33 at 16°C, which is earlier than at 20°C, but later than at the other three temperatures. Age-specific fecundity rate (mx) peaked at earlier ages as temperature increased from 20 to 32°C. At 20, 24, 28 and 32°C, the first oviposition occurred on days 15, 9, 7 and 6, respectively, and daily egg production peaked on days 21 (0.85 eggs), 16 (1.26), 11 (1.36) and 9 (0.95), respectively. Demographic parameters The intrinsic rate of increase (rm) and the finite rate of increase (k) reached the maximal value at 28°C followed by 32°C (Table 4). The value of rm varied from 0.050 to 0.166, and the finite rate of increase (k) from 1.051 to 1.181. Population doubling time was as long as
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1 0.8
lx mx
16°C
0.6 0.4
Age-specific survival rate (l x)
0.2 0
0
20
40
60
80
1 24°C
0.8
100 lx mx
0.6 0.4 0.2 0
0
20
40
60
80
1
lx mx
32°C
0.8
100
0.6 0.4 0.2 0
0
20
40
60
80
100
1.4 1.2 1 0.8 0.6 0.4 0.2 0 1.4 1.2 1 0.8 0.6 0.4 0.2 0
1 20°C
0.8
lx mx
0.6 0.4 0.2 0 0
20
40
60
80
1
100 lx mx
28°C
0.8 0.6 0.4 0.2 0
0
20
40
60
80
1.4 1.2 1 0.8 0.6 0.4 0.2 0
100
1.4 1.2 1 0.8 0.6 0.4 0.2 0
Age-specific fecundity (m x )
38
1.4 1.2 1 0.8 0.6 0.4 0.2 0
Age in days Fig. 1 Age-specific survival rate (lx) and age-specific fecundity rate (mx) curves of Neoseiulus barkeri at five different temperatures Table 4 Parameters of population increase of Neoseiulus barkeri at four constant temperatures (85% RH) Parameter
Temperature (°C) 20 (n = 30)
24 (n = 28)
28 (n = 26)
32 (n = 25)
Intrinsic rate of increase (rm)
0.050
0.136
0.166
0.165
Net reproductive rate (R0)
6.817
20.143
18.776
11.447
Mean generation time in days (t)
23.692
22.074
17.628
14.753
Population doubling time in days (DT)
13.811
5.095
4.167
4.195
1.051
1.146
1.181
1.180
Finite rate of increase (k) n Number of individuals tested
13.8 days at 20°C, whereas it was only 4.2 days at 28°C. Net reproductive rate (R0) was highest at 24°C and lowest at 20°C. Mean generation time decreased with increasing temperature.
Discussion The predatory mite N. barkeri fed on A. ovatus developed successfully over the range of 16–32°C, and temperature had a significant effect on developmental time of various immature stages. Total developmental time varied from 17.5 to 5.0 days when temperature increased from 16 to 32°C. Development of N. barkeri has been studied by many authors. Kolodochka (1985) reported that N. barkeri fed on Tetranychus sp. required 9.2 days for
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Table 5 Summary of lower threshold temperature (C), thermal constant (K, degree-days) and egg-to-adult developmental periods at 16–32°C for four commercial predatory mites and their diet (prey) Species
Neoseiulus barkeri
C (°C)
K (DD)
9.67
111.11
Amblyseius californicus
10.90
59.20
Amblyseius cucumeris
10.32
Phytoseiulus persimilis
11.6
Reference
Prey
Developmental period (days) 16 ± 1°C
20°C
25 ± 1°C
28 ± 2°C
32°C 4.98
Present study
A. ovatus
17.51
11.66
7.86
5.82
Gotoh et al. (2004)
T. urticae
14.10
7.20
4.30
3.00
117.54
Li and Fu (2007)
T. piercei
20.47
11.87
7.58
6.86
65.80
Hamamura et al. (1976)
T. kanzawai
18.90
7.20
4.9
3.50
7.21
complete juvenile development at 26°C and 90–95% RH. Total developmental time at 25°C reported for N. barkeri on T. tabaci (Bonde 1989) and on T. putrescentiae (Zhang and Fan 2005) was 6.2 and 6.8 days, respectively—much shorter than that determined at 24°C in this study. The diversity in development time of N. barkeri at similar temperature was attributed to factors such as diet (prey) and relative humidity. Among the four main predatory mites that have been mass-reared successfully and used widely in biocontrol practice (Table 5), the developmental time of N. barkeri was shorter than that of Amblyseius cucumeris, but longer than that of Amblyseius californicus and Phytoseiulus persimilis at similar temperature. Lower thermal threshold for development and thermal constant are useful indicators for an insect’s potential distribution (Campbell et al. 1974). The results in this study showed that a threshold temperature of 9.67°C and 111.11 accumulated day degrees were required for N. barkeri to complete one generation. Compared with the other three predatory mites, N. barkeri had the lowest threshold temperature, but an intermediate thermal constant, suggesting that N. barkeri remained active at lower temperature and has a potential to develop over a wide range of temperatures. The pre- and postoviposition periods and female longevity shortened as the temperature increased. The oviposition period of N. barkeri in this study was similar to that observed by Bonde (1989) but was much shorter than that of N. barkeri fed on thrips larvae (Momen and El-Borolossy 1997). Shahriar et al. (2010) reported the demographic response to constant temperatures of N. barkeri fed on T. urticae, indicating its potential for the control of two-spotted spider mite at 30–358C. These findings also point at the significant influence of diet (prey), apart from temperature, on the reproductive characteristics of N. barkeri. The ovipostion rate of N. barkeri was low at low temperatures: at 20°C few eggs were laid and 16°C none at all. The reason for this might be that the predator entered reproductive diapause at low temperatures with short photoperiod. Reproductive diapause induced by short-day photoperiods at low temperatures has been reported that both N. barkeri and A. cucumeris (Morewood and Gilkeson 1991; van Houten 1991; Gillespie and Quiring 1993). From 24 to 32°C, the daily egg production varied from 1.47 to 1.64, which agrees with Van Houten et al. (1995) who reported 1.50 eggs per day at 25°C and 70%RH for N. barkeri fed on first instar Frankliniella occidentalis. Higher oviposition rate (2.3–2.5 eggs per female per day) was also reported (Bonde 1989; Momen and El-Borolossy 1997). Offspring sex ratio of N. barkeri was not significantly affected by the temperature. Like in other predatory mites, whose sex ratios were characterized by female bias (Sabelis
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1985), the sex ratio of N. barkeri at all temperatures tested favored the female (59.3–66.7%). This ratio was in agreement with 60% reported by Momen (1994) for N. barkeri fed on T. urticae. The intrinsic rate of increase (rm) is a key demographic parameter useful for predicting the population growth potential of an animal under given environmental conditions (Andrewartha and Birch 1954). In a literature survey, Gotoh et al. (2004) found that the rm of 23 colonizing species of predatory mites around 25°C varied from 0.030 to 0.465, N. barkeri ranked in the middle of the group. Li and Fu (2007) examined the rm of A. cucumeris fed on Tetranychus piercei varied from 0.052 to 0.178 at 16–32°C, which was very close to the values for N. barkeri in the present work (0.050–0.166). Moreover, in both studies the highest rm was estimated at 28°C. The rm of N. barkeri in our study was much lower than the value (0.22) found by Bonde (1989) with thrips as prey for the mite at 25°C. This difference might be due to different preys, rearing methods and/or other environmental conditions. Although temperature has a great influence on the development and reproduction of N. barkeri fed on A. ovatus, the mites can develop successfully and propagate with a high fecundity rate over a broad range of temperatures (24–32°C), at which A. ovatus can be bred largely using wheat bran. Therefore, N. barkeri can be reared in large numbers at a relatively small cost, which is highly relevant for a biocontrol agent to be used in pest control practice. Acknowledgments The research was funded by the National Foundation of Nature Science of China (30860041) and the Major Scientific and Technical Supporting Project of Science and Technology Department of Jiangxi province.
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