Abstract: The two-spotted spider mite (TSSM), Tetranychus urticae Koch and onion thrips (OT), Thrips tabaci Lindeman, are two serious pests of potato and Orius niger (Wolff) and O. minutus (Linnaeus) are major predators of these pests in the potato fields in Ardabil region. Therefore, we compared the predation potential and fecundity of these predator when they fed on 2nd instar larvae of thrips and female mites on potato leaves in the no-choice and choice experiments in a growth chamber that was set at 24 ± 1 °C, 50 ± 5% RH and 16: 8 h (L:D) photoperiod. In the no-choice tests, O. niger showed lower nymphal mortality percentage, higher fecundity and higher killing rate (km) when fed on 2nd instar larvae of thrips than female mites. O. minutus showed lower nymphal mortality percentage, higher fecundity and higher killing rate (km) on female mites than 2nd instar larvae of thrips. In the choice tests, the number of 2nd instar larvae of thrips consumed by different nymphal instars and the adult pairs of O. niger were significantly higher than the number of female mites consumed. Different nymphal instars and the adult pairs of O. minutus consumed significantly more female mites compare to 2nd instar larvae of thrips. Based on these results it can be concluded that O. niger and O. minutus are effective natural enemies of OT and TSSM in the potato fields, respectively.
INTRODUCTION
The Two-Spotted Spider Mite (TSSM), Tetranychus urticae Koch and Onion Thrips (OT), Thrips tabaci Lindeman, are important crop pests throughout the world (Lewis, 1997; Venzon et al., 2001; Deligeorgidis et al., 2006, 2007). These pests regularly cause economic damage to potato crop in Ardabil region. Potato growers in the region use insecticides heavily at high doses and short intervals to control of these pests. Continuous use of pesticides resulted in resistance to most of the available pesticides in many parts of the world (Lewis, 1997). Thus, there has been an increasing interest in using biological control agents, especially Orius species, against these pests (Tommasini and Nicoli, 1993; Yasunaga, 1997; Kohno and Kashio, 1998; Lattin, 1999; Zhang et al., 2006). Yano et al. (2002) mentioned that the use of indigenous species of the predators is preferred than the imported species.
Orius niger (Wolff) and O. minutus (Linnaeus.) are major predators of OT and TSSM in the potato fields of Ardabil region. Also O. niger is a common predator in eastern Europe and northern Asia and O. minutus is common in Palearctic region (Pericart, 1996). The predation potential and fecundity of Orius species vary depending on the preys species (Kiman and Yeargan, 1985; Venzon et al., 2001, 2002; Deligeorgidis, 2002). If the predator species is not monophagous when tested in the no-choice situation, it is useful to assess prey preference through the choice experiments with more than one prey species present. In this study the predation potential, nymphal mortality and fecundity of O. niger and O. minutus was investigated when they fed on OT and TSSM on potato leaf in the no-choice and choice experiments.
MATERIALS AND METHODS
Insect Colonies
Adults of O. niger and O. minutus were collected by
sweep net from unsprayed potato fields (cv. Agria) in the Ardabil plain
(elevation 1332 m; longitude 48° 17` E; latitude 38° 15` N) during
July-2007. Samples were transferred to the laboratory at the University
of Mohaghegh Ardabili and then adults of O. niger and O. minutus
were separated under stereomicroscope by their morphological characters
(Pericart, 1996). These predators were reared on alfalfa (cv. Hamadan)
planted in plastic pots that were placed inside a Plexiglas cage, 10 L
size and the top the cages were covered with fine mesh silk screen and
kept in a growth chamber at 24 ± 1 °C, 50 ± 5% RH and
a photoperiod of 16: 8 h (L: D). Eggs of Ephestia kuheniella Zeller
and corn pollen were provided on a piece of napkin every day and were
placed on the top of the soil inside the cage as the food source for the
predator. Eggs of E. kuheniella in conjunction with corn pollen
has been used for rearing many Orius species as the food source
by many investigators (Cocuzza et al., 1997; Steiner and Goodwin,
1998; Honda et al., 1998; Kakimoto et al., 2005). Newly
hatched nymphs of O. niger and O. minutus were used in the
no-choice and choice tests.
Onion thrips and two-spotted spider mite were collected from the same potato fields and reared on bean, Phaseolus vulgaris Linnaeus, planted in pots that were placed inside a Plexiglas cage, 10l size and the top of the cages were covered with fine mesh silk screen and kept in a growth chamber at 24 ± 1 °C, 50 ± 5% RH and a photoperiod of 16: 08 h (L:D). Newly emerged 2nd instar larvae of thrips and female mites were collected from the colony and used in the experiments as preys.
Preference Tests
The no-choice tests were conducted to demonstrate the suitability
of 2nd instar larvae of thrips and female mites to the O. niger and
O. minutus. In the no-choice tests thirty 2nd instar larvae of
thrips and thirty female mites were transferred separately with a fine
hair brush on the lower surface of potato leaf (with 5 leaflets). These
potato leaves were placed, from petiole, on a piece of moist cotton wool
inside the transparent cylindrical plastic cage (10 cm diameter and 25
cm high). Then one newly hatched nymph of O. niger and O. minutus
were separately transferred on potato leaf with one type of prey (thirty
2nd instar larvae of thrips or thirty female mites) inside a transparent
cylindrical plastic cage. The transparent cylindrical plastic cages with
a meshed lid were kept in a growth chamber at 24 ± 1 °C, 50
± 5% RH and a photoperiod of 16:08 h (L:D). Potato leaves were
renewed every 24 h for all treatments and the number of remained prey
on these leaves was counted under stereomicroscope to determine the number
of prey consumed by one nymph/day. The predation potential of five different
nymphal instars of two predators were determined every 24 h until the
adult emergence. The status of the predator`s nymphs (the death or completion
of their development to the adult stage and gender) was recorded in all
cages. Twenty-four hour after the adult emerged, one adult pair of O.
niger and O. minutus separately were presented with thirty
2nd instar larvae of thrips and thirty female mites inside the transparent
cylindrical plastic cages using similar protocol that was mentioned above.
Potato leaves were renewed every 24 h for all treatments. Survival of
Orius females, the number of prey consumed and the number of eggs
laid were counted under stereomicroscope every 24 h until the death of
the predator`s females. If the male of O. niger and O. minutus
died before the mated females began to oviposit, another newly emerged
male from the same treatment would be introduced into the transparent
cylindrical plastic cage. Non-ovipositing females were also included in
calculations of longevity, fecundity and predation potential of each predator
species. Each adult pair of O. niger and O. minutus feeding
on one of the two prey species was considered as an experimental unit.
Each treatment was replicated 40 times.
The choice test was used to delineate the preferred prey for each predator. In these tests fifteen 2nd instar larvae of thrips+fifteen female mites were presented to one newly hatched nymph and the adult pair of O. niger and O. minutus. These tests were assessed using similar protocols to the no-choice test experiment.
Data Analysis
The coefficients of variation of data in the no-choice and choice
tests were high (>30). Therefore, the data was log transformed to meet
the assumptions of normality and homogeneity of variances. In the no-choice
tests, the differences of the number of prey consumed by five different
nymphal instars and the adult pairs of predators were compared by ANOVA
and Tukey`s HSD test (PROC ANOVA, SAS Institute 1999). The performance
of the same predator species when fed on different prey was compared by
using the Mann-White U test (SAS Institute 1999). Also in these experiments
the killing rate (km = ln (K0)/Tk), the
net predation rate (K0 = Σxlx Kx)
and predation period (Tk = Σxlx
Kxx/K0), were calculated for two Orius species
when they fed on 2nd instar larvae of thrips and female mites. In these
formulas, x is day age (including the nymphal and the adult stages), l
is the age-specific survival (including the nymphal and the adult stages)
and Kx is the age-specific predation (both during the nymphal
and the adult stages) (extraction from formula of the intrinsic rate of
natural increase explained by Birch (1948) and Laughlin (1965)). In the
choice tests the differences of the number of prey consumed by five different
nymphal instars and the adult pairs of predators were compared by ANOVA
and Tukey`s HSD test and the performance of the same predator species
when fed on combination of 2 prey species was compared by using the TTEST
(SAS Institute 1999).
RESULTS
In the no choice tests, the number of 2nd instar larvae of thrips consumed by different nymphal instars and the adult pairs of O. niger were not significantly different compare to the number of female mites consumed, but different nymphal instars and the adult pairs of O. minutus consumed significantly more female mites than the 2nd instar larvae of thrips (Table 1).
Also the number of 2nd instar larvae of thrips consumed by different nymphal instars and the adult pairs of O. niger were significantly higher than O. minutus and the number of female mites consumed by different nymphal instars and the adult pairs of O. minutus were significantly higher than O. niger (Table 1).
Nymphal development time of O. niger was not significantly different
when fed on 2nd instar larvae of thrips and female mites. Also nymphal
development time of O. minutus was not significantly different
when fed on 2nd instar larvae of thrips and female mites (Table
2). O. niger showed lower nymphal mortality percentage, higher
fecundity and sex ratio and longer female and male longevity when fed
on 2nd instar larvae of thrips than female mites and O. minutus showed
lower nymphal mortality percentage, higher fecundity and sex ratio and
longer female and male longevity on female mites than 2nd instar larvae
of thrips (Table 2).
| Table 1: | The number of prey consumed by different nymphal instars and the adult pairs of two Orius species when they fed on two prey species in the no-choice tests |
| Different letters in the same column show significant differences at p 0.05 | |
The nymphal mortality percentage of O. niger was significantly lower in comparison with O. minutus when they fed on 2nd instar larvae of thrips (Table 2). Also fecundity, sex ratio, female and male longevity of O. niger was significantly higher than fecundity, female and male longevity of O. minutus when they fed on 2nd instar larvae of thrips (Table 2). On the other hand O. minutus showed significantly lower nymphal mortality percentage, higher fecundity and sex ratio and longer female and male longevity than O. niger when they fed on female mites (Table 2).
In these tests, the killing rate and the net predation rate of O.
minutus were higher when fed on female mites compare to the 2nd instar
larvae of thrips and the killing rate (km) and the net predation
rate (K0) of O. niger were higher when fed on
2nd instar larvae of thrips than female mites (Table 3).
Also the killing rate and the net predation rate of O. niger were
higher than O. minutus when they fed on 2nd instar larvae of thrips
and the killing rate and the net predation rate of O. minutus were
higher than O. niger when they fed on female mites (Table
3). Predation period (Tk) of O. niger and O.
minutus was shorter on 2nd instar larvae of thrips and female mites
respectively (Table 3).
| Table 2: | Comparison of means ( ± SE) of nymphal development time, nymphal mortality percentage, female and male longevity, fecundity and sex ratio of two Orius species when fed on two prey species in the no-choice tests |
| Different letter(s) in the same column show significant differences at p 0.05 | |
| Table 3: | Net predation rate (K0), predation period (Tk) and killing rate (km) of two Orius species when fed on two prey species in the no-choice tests |
| Table 4: | The number of prey eaten by different nymphal instars and the adult pairs of two Orius species when fed on two prey species in the choice tests |
| Different letter(s) in the same column show significant differences at p 0.05 | |
| Table 5: | Comparison of means ( ± SE) of nymphal development time, nymphal mortality percentage, female and male longevity, fecundity and sex ratio in two Orius species when they fed on two prey species in the choice tests |
| Different letter(s) in the same column show significant differences at p 0.05 | |
In the choice tests, the number of 2nd instar larvae of thrips consumed by different nymphal instars and the adult pairs of O. niger was significantly higher than the number of female mites consumed and the number of female mites consumed by different nymphal instars and the adult pairs of O. minutus was significantly higher than the number of 2nd instar larvae of thrips consumed (Table 4).
Also in the choice tests, O. niger showed significantly shorter female and male longevity and lower fecundity compare to O. minutus when they fed on the combination of 2nd instar larvae of thrips and female mites . But, nymphal development time, nymphal mortality percentage and sex ratio of O. niger and O. minutus were not significantly different when they fed on the combination of 2nd instar larvae of thrips and female mites (Table 5).
DISCUSSION
Prey preference in the no-choice and choice tests under controlled conditions is an important intermediate step in the risk assessment of biological control agents. The killing rate, km, is the important characteristic of a predator to obtain an indication for its capability in biological control.
This study showed that the type of prey could strongly influence the predation potential, fecundity and mortality of Orius species. In the no-choice and choice tests, O. niger preferred feeding on 2nd instar larvae of thrips, km = 0.241, than female mites, km = 0.204, while O. minutus preferred feeding on female mites, km = 0.249, than 2nd instar larvae of thrips, km = 0.196. Also analysis of the nymphal development time, nymphal mortality percentage and fecundity indicated that the population growth of O. niger was restricted mostly by high nymphal mortality and low fecundity when fed on females of TSSM and the population growth of O. minutus was restricted mostly by high nymphal mortality and low fecundity when fed on 2nd instar larvae of OT.
Few data are available about the predatory rate and fecundity of O. niger and O. minutus when fed on OT and TSSM. Deligeogidis (2002) demonstrated that O. niger strongly preferred 2nd instar larvae of OT compare to 2nd instar larvae of Frankliniella occidentalis (Pergande) and recorded that O. niger is suitable predator in control of OT. Atakan and Gencer (2008) concluded that populations of O. niger were more abundant and also significantly correlated with F. occidentalis population in normal-planted cotton fields. With regard to predator-thrips interactions, they suggested that O. niger may be an efficient biological control agent regulating Frankliniella flower thrips especially in normal-planted cotton. Baniameri et al. (2005) estimated high rm (0.113) for O. niger at 26 °C on a diet of E. kuehniella eggs and suggested that the population growth rate of O. niger was restricted mostly by juvenile mortality. Toyoshima (2006) reported that O. minutus had the potential to control of TSSM population.
The killing rate of O. niger and O. minutus on adults of thrips can be varied by the different species of prey offered and the greater difficulty for Orius species to catch adults than nymphs of thrips (Salas-Aguilar and Ehler, 1977; Teeriling et al., 1993). For example, Teeriling et al. (1993) showed that Orius tristicolor (White) responds to specific semiochemical cues from western flower thrips and preferred feeding on it in comparison with other thrips species. Lichtenauer and Sell (1993) concluded that in the no-choice tests, O. insidiosus (Say) and O. minutus consumed more thrips larvae than adults.
It has been reported that dietary differences of various prey species affects the longevity and fecundity of Orius species (Kiman and Yeargan, 1985; Chyzik et al., 1995). Fecundity of O. insidiosus varied when it consumed from thrips, mites and the eggs of moths (Kiman and Yeargan, 1985). Venzon et al. (2001, 2002) reported that O. laevigatus (Fieber) was attracted more to the two-spotted spider mite infected cucumber than western flower thrips infected plants. Fritsche and Tamo (2000) found that the efficiency of O. albidipennis (Reuter) in control of Megalurothrips sjostedti Trybom was lower than the Ceratothripoides cameroni (Priesner) and F. schultzei Trybom.
Present results indicated that O. niger and O. minutus, that are common in Ardabil potato fields, can be useful in the biological control of onion thrips and two-spotted spider mite respectively.
ACKNOWLEDGMENT
The Research Council of Mohaghegh Ardabili University (Iran) is gratefully acknowledged for their financial support of this research.