Effects of air temperature and water vapor pressure deficit on storage of the predatory mite Neoseiulus californicus (Acari: Phytoseiidae)

Effects of air temperature and water vapor pressuredeficit on storage of the predatory mite Neoseiuluscalifornicus (Acari: Phytoseiidae)

Noureldin Abuelfadl Ghazy • Takeshi Suzuki • Hiroshi Amano •

Katsumi Ohyama

Received: 7 March 2012 / Accepted: 9 April 2012 / Published online: 21 April 2012� Springer Science+Business Media B.V. 2012

Abstract To determine the optimum air temperature and water vapor pressure deficit

(VPD) for the storage of the predatory mite, Neoseiulus californicus, 3-day-old mated

females were stored at air temperatures of 0, 5, 10, or 15 �C and VPDs of 0.1, 0.3, or

0.5 kPa for 10, 20, or 30 days. At 10 �C and 0.1 kPa, 83 % of females survived after

30 days of storage; this percentage was the highest among all conditions. VPDs of 0.3 and

0.5 kPa regardless of air temperature, and an air temperature of 0 �C regardless of VPD

were detrimental to the survival of the females during storage. Since the highest survival

was observed at 10 �C and 0.1 kPa, the effect of the storage duration on the post-storage

quality of the stored females and their progeny was investigated at 25 �C to evaluate the

effectiveness of the storage condition. The oviposition ability of the stored females,

hatchability, and sex ratio of their progeny were not affected even when the storage

duration was extended to 30 days. Although a slight decrease in the survival during the

immature stages of progeny was observed when the storage duration was C20 days, the

population growth of N. californicus may not be affected when individuals stored in these

conditions are applied to greenhouses and agricultural fields. The results indicate that

mated N. californicus females can be stored at 10 �C and 0.1 kPa VPD for at least 30 days.

Keywords Biological control � Cold storage � Natural enemies � Neoseiulus californicus �Post-storage quality � Vapor pressure deficit

N. A. Ghazy � K. OhyamaGraduate School of Horticulture, Chiba University, Matsudo 648, Chiba 271-8510, Japan

N. A. Ghazy (&) � T. Suzuki � K. OhyamaCenter for Environment, Health and Field Sciences, Chiba University,Kashiwanoha 6-2-1, Chiba 277-0882, Japane-mail: [email protected]

T. SuzukiJapan Society for the Promotion of Science, Ichiban-cho 8, Chiyoda, Tokyo 102-8472, Japan

H. AmanoGraduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake,Sakyo, Kyoto 606-8502, Japan

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Exp Appl Acarol (2012) 58:111–120DOI 10.1007/s10493-012-9556-7

Introduction

Integrated pest management (IPM) involves different control approaches to reduce agricul-

tural pest populations effectively, economically, and environment-friendly. Biological control

using natural enemies such as predators, parasitoids, and pathogens is one of the mainstays of

IPM. Despite the successful use of natural enemies, there is still great potential for research into

reducing the costs and increasing the availability of their commercial products. An efficient

storage method can substantially reduce the costs and increase the availability of natural

enemies to the end-users. Such storage methods can also allow flexibility in the release time to

synchronize with optimum weather conditions and pest outbreaks (Morrison and King 1977;

Stinner 1977; Bueno and van Cleave 1997; Leopold 1998; Lopez and Botto 2005).

Storage at low air temperatures (i.e., cold storage) is a valuable approach for extending

the life duration of natural enemies and is widely recommended for cost-effective bio-

logical control programs (Morewood 1992; Leopold 1998). Responses of natural enemies

to cold storage have received considerable interest with the majority of studies focusing on

the air temperature and the storage duration (e.g., Pitcher et al. 2002; Lysyk 2004; Tezze

and Botto 2004; Bayram et al. 2005; Kivan and Kilic 2005; Hackermann et al. 2008;

Riddick and Wu 2010). However, the role of other environmental factors such as water

vapor conditions is not well understood (Colinet and Boivin 2011).

In biological studies, water vapor conditions are commonly expressed as relative

humidity (RH; %) that is the percentage of the vapor pressure (VP; Pa) in the saturated

vapor pressure (SVP; Pa) at an air temperature, or as a vapor pressure deficit (VPD; Pa)

that is the difference between SVP and VP. As the evaporative water loss from organisms

is generally proportional to VPD even at different air temperatures, VPD should be used

instead of RH when the air temperature varies (Anderson 1936; Ferro and Chapman 1979;

Perring et al. 1984; Eaton and Kells 2009).

Recently, we found that RH close to 100 % (i.e., VPD of 0.0 kPa) at an air temperature

of 5 �C was effective for extending the life duration of the predatory mite, Neoseiuluscalifornicus (McGregor), which is a biological control agent used for a broad range of

phytophagous mites (Ghazy et al. 2012a, b). However, the responses of N. californicus to

wider ranges of air temperatures and VPDs during storage remain unclear. In the present

study, we attempted to explore such responses to find out the optimal storage condition by

considering both air temperature and VPD. For this purpose, we stored adult females of N.californicus in different combinations of air temperatures and VPDs, and investigated the

storage survival as well as the post-storage survival, oviposition, and the quality of their

progeny.

Materials and methods

Mites

A population of N. californicus was originally collected in a Japanese pear orchard in

Chiba, Japan (35�N and 139�E) and has been maintained in the laboratory since 1995. The

population was reared on kidney bean (Phaseolus vulgaris L.) leaf disks placed on water-

soaked cotton in Petri dishes (9 cm diameter, 1 cm deep). The dishes were placed in small

plastic cups (10 cm diameter, 5 cm deep) in which the upper border was covered with

sticky resin (Tanglefoot; Contech Enterprises, Victoria, Canada) to prevent escape. Each

small cup was then placed into a larger one (14.5 cm diameter, 8 cm deep) partially filled

112 Exp Appl Acarol (2012) 58:111–120

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with water (ca. 1 cm deep) as a further precaution. The two-spotted spider mite, Tetr-anychus urticae Koch, was supplied as food every 3–4 days. In the laboratory, air tem-

perature, RH, and photoperiod were set at 25 �C, 70 %, and LD 16:8 h, respectively.

Storage

Three-day-old mated N. californicus females were used. To obtain females of the same

age, egg-laying females were picked up from the stock population and allowed to lay eggs

for 24 h under the laboratory conditions. The females were then removed, and the eggs

were reared at the same conditions until the adult stage. The newly emerged adult females

were allowed to mate for 24 h. The mating success of the females was confirmed by

observing oviposition.

The females were confined separately in polypropylene vials (1.5 ml). Each vial had a 0.8-

cm hole drilled in the cap and was covered with a gas-permeable filter (MillisealTM; Nippon

Millipore, Tokyo, Japan). The vials were arranged in a plastic tray for each treatment and

transferred into a system for controlling water vapor conditions (Suzuki et al. unpublished). In

this system, the streams of humidified and dehumidified air were combined in an acrylic

container (7 l, 30 cm wide, 30 cm deep, 17 cm high; Model VS; As One, Osaka, Japan) and

each flow rate was independently controlled to maintain water vapor conditions inside the

container. To control the air temperature, the container was placed inside an incubator (123 l,

70 cm wide, 58 cm deep, 102 cm high; MIR-154; Sanyo Electric, Osaka, Japan). In the

system, 12 combinations of 4 air temperatures (0, 5, 10, and 15 �C) and 3 VPDs (0.1, 0.3, and

0.5 kPa) were evaluated for the storage of females under continuous darkness.

The environmental conditions inside the vials were measured once a minute with an air

temperature and water vapor sensor (SHT75; Sensirion, Zurich, Switzerland) as described

by Ghazy et al. (2012a). The survival of the females was determined after 10, 20, and

30 days of storage.

Post-storage

Once the optimum conditions for storage were determined, the effects of storage duration

on the post-storage quality of stored females and their progeny were investigated. After 10,

20, and 30 days of storage, the surviving females were released from the vials and

transferred individually onto a P. vulgaris leaf disk (2.5 cm diameter) infested with T.urticae in the laboratory conditions mentioned above. The leaf disks were placed on water-

soaked cotton in Petri dishes (4 leaf disks/dish). The Petri dishes were placed in a small cup

with 10 holes 0.8 cm in diameter punched into the lid for ventilation.

The stored females were observed daily to determine the post-storage survival, time

required for resuming oviposition, and the number of eggs laid until the last oviposition.

The eggs laid by the stored females were transferred onto detached P. vulgaris leaves

infested with T. urticae daily, and the hatchability, survival during the immature stages,

and sex ratio were observed. Unstored 3-day-old mated females (storage dura-

tion = 0 days) were used as controls, and the same observations were performed.

Statistical analysis

The differences in the survival percentages at the end of storage and during post-storage

were analyzed by Fisher’s exact test. For multiple comparisons, the level of significance

Exp Appl Acarol (2012) 58:111–120 113

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(a = 0.05) was adjusted using a Bonferroni correction (a/k, where k is the number of pairs

in the multiple comparison). Linear regression analysis was conducted to assess the effect

of storage duration on the time required for the stored females to resume oviposition. To

analyze the differences among the different storage durations, the data for oviposition

period, daily rate of eggs laid, and total number of eggs laid by the stored and unstored

females as well as the hatchability, survival during the immature stages, and sex ratio of

their progeny were normalized by square root transformation and then subjected to one-

way analysis of variance (ANOVA) followed by Scheffe’s post hoc test. All data presented

in the Tables and Figures are untransformed. All analyses were performed using SigmaPlot

11.0 (Systat Software, Chicago, IL, USA) and SPSS 18.0 (SPSS, Chicago, IL, USA).

Results

Air temperature and VPD during storage

The air temperature and VPD measurements inside the storage vials were consistent with

each set point (Table 1). The fluctuations (±SD) in the measured air temperatures were

within ±0.1 �C; those of VPD were smaller than the detectable level of the sensor.

Survival during storage

After 10 days of storage, 100 % of females survived at air temperatures from 5 to 15 �C

and 0.1 kPa VPD; the survival percentages were significantly higher than those in the other

conditions (P \ 0.05/66, Fisher’s exact test with a Bonferroni correction) (Fig. 1a). After

20 days of storage, [80 % of females survived at 5–15 �C and 0.1 kPa VPD; the per-

centages were significantly higher than those in the other treatments (P \ 0.05/66)

(Fig. 1b). After 30 days of storage, 83 % of females survived at 10 �C and 0.1 kPa VPD;

Table 1 The set points and measurement (mean ± SD) of air temperatures and vapor pressure deficits(VPDs) in each treatment during the storage of Neoseiulus californicus females

Set point Measurement

Air temperature (�C) VPD (kPa) Air temperature (�C) VPD (kPa)

0 0.1 (84)a 0.3 ± 0.1 0.1 ± 0.0 (84.5 ± 1.2)

0 0.3 (51) 0.2 ± 0.0 0.3 ± 0.0 (51.4 ± 0.5)

0 0.5 (18) 0.2 ± 0.0 0.5 ± 0.0 (18.3 ± 0.2)

5 0.1 (89) 5.1 ± 0.0 0.1 ± 0.0 (89.0 ± 0.3)

5 0.3 (66) 4.9 ± 0.0 0.3 ± 0.0 (66.3 ± 0.2)

5 0.5 (43) 4.6 ± 0.1 0.5 ± 0.0 (44.6 ± 0.2)

10 0.1 (92) 9.9 ± 0.1 0.1 ± 0.0 (92.1 ± 0.1)

10 0.3 (76) 10.1 ± 0.0 0.3 ± 0.0 (76.1 ± 0.9)

10 0.5 (59) 10.6 ± 0.0 0.5 ± 0.0 (59.3 ± 0.2)

15 0.1 (94) 15.4 ± 0.1 0.1 ± 0.0 (94.1 ± 0.2)

15 0.3 (82) 15.2 ± 0.0 0.3 ± 0.0 (82.5 ± 0.1)

15 0.5 (71) 15.6 ± 0.0 0.5 ± 0.0 (71.2 ± 0.5)

a Values in the parentheses indicate the corresponding relative humidity in each condition

114 Exp Appl Acarol (2012) 58:111–120

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the percentage was significantly higher than that in other conditions (P \ 0.05/66) except

that at 15 �C and 0.1 kPa VPD (Fig. 1c). Almost no females survived at 0 �C and VPD of

0.1–0.5 kPa, and 15 �C and VPD of 0.3 or 0.5 kPa, even when the storage duration was as

short as 10 days (Fig. 1a).

Post-storage quality

No significant differences in the survival percentage during post-storage were observed

among the stored and unstored females until the end of the last oviposition (Table 2;

P [ 0.05/6, Fisher’s exact test with a Bonferroni correction). The time required for the

stored females to resume oviposition increased as the storage duration increased

(R2 = 0.741, P \ 0.001, linear regression analysis) (Fig. 2). There were no significant

differences in the oviposition period [F(3,80) = 2.04, P = 0.116, one-way ANOVA],

number of eggs laid daily [F(3,80) = 0.57, P = 0.636], or total number of eggs laid

[F(3,80) = 1.94, P = 0.130] among the females stored for 0–30 days (Table 3).

There were no significant differences in the hatchability [F(3,21) = 0.49, P = 0.687] or

sex ratio [F(3,21) = 0.34, P = 0.793] among the progeny of females stored for 0–30 days

(Table 4). There was a significant difference in survival percentages during the immature

stages among progeny from the females stored for 0–30 days [F(3,21) = 5.751, P = 0.005];

the survival percentages of progeny from the females stored for C20 days were 5 % lower

than those from unstored females (P \ 0.05, Scheffe’s post hoc test).

Discussion

Water loss, energy depletion, and chilling injury are the major problems for the survival of

natural enemies during cold storage (De Bach 1943). In particular, maintaining adequate

water balance in the body is essential for the survival of tiny organisms such as phytoseiid

mites (Gaede 1992). The present study attempted to find out the most suitable air temper-

ature and VPD conditions that minimize the problems associated with cold storage of N.californicus. This objective was obtained when the females stored at 10 �C and VPD of

0.1 kPa where the survival during storage was markedly improved. It can be expected that at

this condition both water loss and chilling injury were mitigated. This result highlights the

importance of controlling air temperature and water vapor conditions during cold storage.

Survival was lower at 15 �C than at 5–10 �C after 10 days of storage at 0.3 kPa VPD.

As the respiration rate normally increases as air temperature increases, respiratory water

loss might have increased at 15 �C. Moreover, as the threshold temperature for the

development (T0) of N. californicus is approximately 10 �C (Raworth et al. 1994; Canlas

et al. 2006), the energy depletion accompanying metabolic activity might also increase at

15 �C.

Few females survived at 0 �C regardless of the VPD even when the storage duration

was as short as 10 days; this can be attributed to chilling injury that occurs due to exposure

to low air temperatures of approximately 0 �C (Lee 1991; Denlinger and Lee 1998; Storey

and Storey 2010; Yang et al. 2010; Lalouette et al. 2011). After 30 days of storage at

0.1 kPa VPD, [80 % females survived at 10 �C, whereas only 30 % survived at 5 �C.

Previous studies report that storage at temperatures below the T0 promptly decreases

survival as a result of chilling injury (Kostal et al. 2001; Pandey and Johnson 2005).

Therefore, the higher survival at 10 �C would be caused by the less chilling injury than at

5 �C. Hence, T0 is an indicator for the selection of optimum air temperatures for cold

Exp Appl Acarol (2012) 58:111–120 115

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0

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116 Exp Appl Acarol (2012) 58:111–120

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Fig. 1 Survival at the end of storage of Neoseiulus californicus females stored at air temperatures of0–15 �C and vapor pressure deficits (VPD) of 0.1–0.5 kPa for a 10, b 20, and c 30 days. N = 46–68.Different letters show significant differences in survival percentages among the treatments (P \ 0.05/66,Fisher’s exact test with a Bonferroni correction)

Table 2 Effect of storage duration at an air temperature of 10 �C and vapor pressure deficit (VPD) of0.1 kPa on the post-storage survival of Neoseiulus californicus females

Storage duration (days) Na Survival (%)

1–13b 14 15 16 17 18 19 20 21

0 15 100 100 100 100 100 100 93 87 87

10 23 100 100 100 100 100 100 100 100 100

20 22 100 100 100 95 95 95 95 95 95

30 24 100 96 96 96 96 96 96 96 96

a Number of females observed. b Post-storage days. Survival was observed daily until the end of the lastoviposition. No significant differences in the survival percentage were observed between the stored andunstored females on each day (P [ 0.05/6, Fisher’s exact test with a Bonferroni correction)

Fig. 2 Time required by Neoseiulus californicus females to resume oviposition with respect to storageduration. The females were stored at an air temperature of 10 �C and a vapor pressure deficit (VPD) of0.1 kPa for 10, 20, and 30 days. N = 22–24

Table 3 Post-storage oviposition ability of Neoseiulus californicus females stored at an air temperature of10 �C and vapor pressure deficit (VPD) of 0.1 kPa for 10, 20, and 30 days

Storage duration (days) Na Oviposition period (days) Number of eggs/day/$ Total number of eggs/$

0 15 15.7 ± 0.8 3.0 ± 0.1 47.3 ± 2.2

10 23 14.3 ± 0.6 3.0 ± 0.0 43.1 ± 2.0

20 22 14.3 ± 0.5 3.1 ± 0.0 43.7 ± 1.4

30 24 13.4 ± 0.6 2.9 ± 0.1 40.2 ± 2.2

a Number of females observed. Data are expressed as mean ± SE. No significant differences in the ovi-position ability were observed among the females stored for 0–30 days (P [ 0.05, one-way ANOVA)

b

Exp Appl Acarol (2012) 58:111–120 117

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storage, which is corroborated by several reports (Drukker et al. 1993; Gagne and Coderre

2001; Fisher and Edwards 2002; Pandey and Johnson 2005).

Post-storage quality is of great concern when determining a storage method for natural

enemies (Chen et al. 2008). In cold storage, prolonging the storage duration often reduces

the post-storage survival and oviposition ability of natural enemies as a consequence of

water loss, energy depletion, and chilling injury (Pitcher et al. 2002; Colinet et al. 2006;

Chen et al. 2008; Renault 2011). The storage conditions of 10 �C and 0.1 kPa VPD had no

negative effects on the post-storage survival or oviposition ability of the stored females

even when the storage duration was extended to 30 days. These results indicate that post-

storage problems in cold storage methods can be resolved by minimizing the VPD during

storage.

The females stored for 10 days needed 1 day to resume oviposition after being released

from the storage condition of 10 �C and 0.1 kPa VPD, whereas those stored for C20 days

needed 2 days. These results can probably be attributed to the delay in recovering to a

normal oviposition state after prolonged storage duration (Nicoli and Galazzi 1998;

Larentzaki et al. 2007; Luczynski et al. 2008; Lee 2010; Dantas-Torres and Otranto 2011).

However, such a small difference of 1 day in resuming oviposition might be less important

in population growth when applying stored N. californicus to agricultural fields

We also found that neither the hatchability nor sex ratio of progeny from the stored

females was affected by the storage condition of 10 �C and 0.1 kPa VPD even when the

storage duration was extended to 30 days. However, the survival during the immature

stages of progeny was slightly affected by the storage conditions when the storage duration

was C20 days. Although the mechanisms for passing maternal effects of cold stress to the

progeny are poorly understood, a few reports suggest that damage from storage somehow

affects the quality of progeny (Chen et al. 2011; Colinet and Boivin 2011). However, in the

present study, the reduction in survival during the immature stages of progeny from the

stored females did not exceed 5 % in comparison to that from the unstored females,

suggesting that storage has minor effects on future population growth.

For biological control programs to work efficiently, storage methods should maintain

the high quality of natural enemies after storage with respect to survival and reproduction

(Tauber et al. 1993). Although previous studies have investigated various air temperatures

to develop efficient cold storage methods, considerations for water vapor conditions during

cold storage remain limited. The results of the present study indicate that N. californicusfemales can be stored with survival rates exceeding 80 % at an air temperature of 10 �C

and 0.1 kPa VPD for at least 30 days. Although the storage at this condition had a minor

Table 4 Hatchability, survival during the immature stages, and sex ratio of the progeny from Neoseiuluscalifornicus females stored at an air temperature of 10 �C and vapor pressure deficit (VPD) of 0.1 kPa for10, 20, and 30 days

Storage duration (days) Na Hatchability (%) Nb Survival (%) Nc $ ratio (%)

0 885 99.7 ± 0.2a 883 97.3 ± 0.9a 826 73.0 ± 3.3a

10 1,006 99.3 ± 0.3a 999 95.0 ± 0.8ab 956 74.1 ± 1.6a

20 967 99.6 ± 0.4a 964 91.9 ± 1.2b 894 72.5 ± 2.5a

30 953 99.3 ± 0.4a 944 92.5 ± 1.3b 873 70.4 ± 1.9a

a Number of eggs examined for hatchability. b Number of progeny examined for survival. c Number ofadults observed for sex identification. Data are expressed as mean ± SE. Different letters indicate a sig-nificant difference between progeny from the females stored for 0–30 days (P \ 0.05, Scheffe’s test afterone-way ANOVA)

118 Exp Appl Acarol (2012) 58:111–120

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negative effect on the progeny quality, the performance of stored N. californicus may be

comparable to that of unstored individuals when applying the mites to agricultural fields.

The results suggest that controlling air temperature and water vapor conditions can dis-

tinctly improve the cold storage of N. californicus. Our storage method can be used to

establish the scheduled production of high-quality N. californicus in sufficient quantities

for effective use in biological control programs. Further studies investigating possible

application of this storage condition to the commercial products of N. californicus as well

as the implementation of stored females in greenhouses and agricultural fields are needed

to indicate the practical effectiveness of our storage method.

Acknowledgments This study was supported by Grants-in-Aid for Scientific Research (C) (21580062)and JSPS Fellows (22-2650) from the Japan Society for the Promotion of Science. We are grateful to Dr.T. Kozai and Dr. M. Shah for their kind support as well as M. Ohyama for technical assistance.

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