Translator Disclaimer
1 June 2013 Age Preference and Fitness of Microplitis manilae (Hymenoptera: Braconidae) Reared on Spodoptera exigua (Lepidoptera: Noctuidae)
Author Affiliations +
Abstract

The larval parasitoid Microplitis manilae Ashmead (Hymenoptera: Braconidae) is a potential biological control agent of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). To understand the preference and fitness of M. manilae on larval instars of S. exigua, we compared host choice, development, and life table parameters when different larval instars of S. exigua were supplied in the laboratory. Results showed that parasitism of 2nd or 3rd instar larvae was significantly higher compared with other instars. The intrinsic rate of increase (r), finite rate of increase (λ), net reproduction rate (R0) and mean length of a generation (T) were significantly affected by which larval instars were attacked. The maximum values of r, λ, R0 and T were observed when M. manilae parasitized 2nd instar S. exigua larvae. Therefore, we conclude that the 2nd larval instar of S. exigua represents the optimum host stage and suggest that 2nd larval instar of S. exigua will be the most suitable host stage for mass production of M. manilae as well as the best instar to target for biological control in the field.

The beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) originated in Southeast Asia, and is an important pest that defoliates crops causing crop losses (Lara et al. 2000; Bajpaiet al. 2006; Deshmukhe et al. 2010). Female moths lay eggs on crop leaves on which newly emerged larvae feed (Wilson 1932). The larva is the only stage that can injure crop leaves, and this stage has 5 instars (Wilson 1932). Crop plants were completely destroyed by the larvae when populations reached or exceeded a critical density (Luo et al. 2000; Bajpai et al. 2006). Pesticides have been extensively used for controlling this pest, but many negative impacts have been widely observed and associated with this control method (Elzen et al. 1989; Foster 1989; All et al. 1996; Yeh et al. 1997; Kranthi et al. 2002).

Microplitis manilae Ashmead (Hymenoptera: Braconidae) is one of the major larval endoparasitoids of Spodoptera species (Rajapakse et al. 1985), and it has served as a potent biological control agent of S. exigua (Sun & Huang 2010; Qiu et al. 2012). It can also parasitize S. litura (F.) and S. frugiperda (Smith) larvae in the field (Rajapakse et al. 1985, 1992; Ando et al. 2006; Qiu et al. 2012). The biology, ecology and interspecific competition between M. manilae and other parasitoid species (e.g. Chelonus insularis Cresson) have been investigated (Rajapakse et al. 1985, 1992; Ando et al. 2006; Sun & Huang 2010; Qiu et al. 2012). The female parasitoid can lay an average of more than 300 eggs during her lifespan under optimum conditions (Ando et al. 2006; Qiu et al. 2012).

Previous studies suggested that the development and fecundity of parasitoids were closely related to the age of their hosts, and thus when given a choice of different host ages, female parasitoids can choose their preferred host ages (Li et al. 2006; Kant et al. 2012). The differences in host quality are often very significant among various host ages, which can influence the choice of a host based on age by the parasitoid and the subsequent development of parasitoid larvae in bodies of hosts (Li et al. 2006). A suitable host can provide enough nutrition for the development of the parasitoid offspring (Salt 1938). The selection by the parasitoid of suitable hosts is critical to the development of the parasitoid (Vinson 1990; Godfray 1994; Beckage & Gelman 2004). Fitness of the parasitoid is often assessed by survival, fecundity, development duration and sex ratio (Godfray 1994; Roitberg et al. 2001). Therefore, hosts of the optimum age can significantly facilitate mass rearing of a parasitoid. Life table parameters have been applied to evaluate the population development and fitness of an insect (Tanigoshi & McMurtry 1977; Chi & Liu 1985; Chi 1988; Zhou et al. 2010).

The present experiment focused on the choice of different S. exigua instars by M. manilae and the differences in fitness of its progeny depending on the host instar that was parasitized in laboratory bioassays. The results could offer valuable information on the best age to use for rearing M. manilae and for controlling S. exigua in the field.

MATERIALS AND METHODS

Host and Parasitoid Cultures

Spodoptera exigua larvae were collected from a vegetable field in the suburb of Guangzhou City, Guangdong Province and reared on a standard artificial diet developed for Lepidotpera (Raulston & Lingren 1972) at constant temperature (26 ± 1 °C), 65 ± 5% RH and at 14:10 h L:D in the laboratory of the Department of Entomology, South China Agricultural University, Guangzhou, Guangdong Province. First through fifth S. exigua instars were used for these experiments.

Spodoptera exigua larvae parasitized by M. manilae were collected from a vegetable field in the suburb of Guangzhou City, Guangdong Province. Newly emerged female and male M. manilae adults were paired, and each pair was provided with S. exigua larvae for oviposition. For these experiments, newly emerged adult parasitoids were individually maintained in glass vials (7 × 2 cm diam) when they emerged from pupae under the same laboratory conditions as above. Microplitis manilae adults from the culture described above were fed 10% fresh honey solution and then paired for a 2-day mating period prior to being exposed to S. exigua larvae.

Preferences of M. manilae Adult Females for Different S. exigua Instars

To determine the preferences of M. manilae adult females for different larval instars of S. exigua, 2-day-old mated female parasitoids were exposed to larvae in a cage (30 × 30 × 25 cm) containing 10% honey water for 24 h. This experiment was replicated 10 times. Each cage contained 10 mated female parasitoids and 150 larvae (ca. 30 of each of the 5 instars). After a 24h exposure period, the different host instars were separated and placed in a clean transparent plastic box (15.5 × 11 × 5 cm) covered with organdy cloth and provided the standard artificial diet for host larvae under the laboratory conditions. The host larvae were checked daily until they pupated or died. The host larvae that died prior to pupation were dissected to ascertain if they had been parasitized. Parasitism was confirmed by the presence in the cadaver of an egg or immature parastoid. The date and the numbers of different S. exigua instars parasitized were recorded.

Development of M. manilae Immature Stages Parasitized on Different S. exigua Instars

Since the parasitoid did not accept 5th S. exigua instars in the age preference experiment, only 1st to 4th host instars were provided for developmental studies. Each treatment included 30 mated female parasitoids, and each female was provided with 40 S. exigua larvae of each stadium from the 1st to the 4th instar. Host larvae and adult parasitoids were kept together for 24 h in a clean transparent plastic box covered with mesh as above, and subsequently the exposed host larvae were transferred to separate boxes and provided with artificial diet and randomly placed in environmental chambers (PQX-330A-12WM; Ningbo Laifu Experimental Equipment, Zhejiang, China) set at 25 ± 1 °C, 65 ± 5% RH and 14:10 h L:D. The development of the M. manilae eggs was assessed by dissecting a batch of 30 parasitized larvae of each larval stage on each consecutive day. Another batch of 40 S. exigua larvae at each larval stage exposed to M. manilae was left intact until the parasitoid larvae had fully developed. The parasitized host larvae were collected 24 h after parasitism and each was held individually in an unsealed cuvette covered with organdy until the M. manilae larva crawled out of the S. exigua larva and pupated. The M. manilae pupae were monitored daily until the adults emerged. The next cohort of S. exigua larvae was exposed to parasitoids when all parasitoid larvae in the previous treatment had become pupae. Duration of parasitoid development and pupal weights were recorded. The experiment was repeated 10 times.

Longevities and Fecundities of M. manilae Adults Derived from S. exigua Parasitized in Different Instars

Microplitis manilae adult cohorts, derived from S. exigua parasitized in different instars as described above, were paired and fed 10% fresh honey solution. Two days after mating, M. manilae mated females were used for the experiment. Each female was provided 40 second instars of S. exigua from the culture described, and these 2nd instars were fed artificial diet in clean transparent mesh-covered plastic boxes held in the environmental chambers. The number of parasitoid pupae from each box were then recorded as female's fecundity. Dead parasitoids and dead host larvae were discarded.

Data Analysis

Data were checked for normality and homoscedasticity and, if needed, were arcsine, square-root or log-transformed. The developmental durations were first transformed by log10(x+1), and the survival rates were first transformed by arcsine square-root when the data did not fit a normal distribution. A one-way analysis of variance (ANOVA) was conducted in comparing the overall differences of the data among treatments when significant treatment differences were indicated by a significant F-test at P < 0.05. The Fisher protected least significant difference (LSD) test was used as an one way-ANOVA test in comparing the means between treatments (SAS Institute 2004).

We used life table parameters to evaluate the population development of the parasitoid derived from different host instars. The computational formulas of life table parameters were described as:

e01_602.gif

where x is the age in days of parasitoid; lx is the age-specific survival rate; mx is age-specific fecundity; T is the mean generation time; R0 is the net reproductive rate; r is the intrinsic rate of increase estimated by using the Euler-Lotka formula (Eq. 2) with age indexed from 0 (Goodman 1982; Chi & Liu 1985; Chi 1988); λis the finite rate of increase. The computer program TWOSEXMSChart was used to analyze the life history raw data (Chi & Liu 1985; Chi 2005).

RESULTS

Preferences of M. manilae Adult Females for Different S. exigua Instars

There were significant differences in the M. manilae parasitization rates among the various S. exigua instars when 1st to 5th instars were exposed simultaneously to the parasitoid (F4,45 = 201.82, P < 0.0001). The parasitization rates of female parasitoids on 2nd and 3rd instar larvae were significantly higher than those of any other instars, and the rates on these 2 instars did not differ from each other. No parasitism was recorded in 5th instars (Fig. 1).

Development of M. manilae Immature Stages Parasitized on Different S. exigua Instars

Host larval instars affected significantly the parasitoid's development (egg: F3,36 = 80.78, P < 0.0001), (larva: F3,36 = 20.68, P < 0.0001), (pupa: F3,36 = 11.95, P < 0.0001) and (all immature stages: F3,36 = 6.16, P = 0.0017). The developmental duration for the entire immature stage parasitized on 4th instar host larvae was the shortest (Table 1). The particular larval instars that were parasitized also affected significantly the pupal weight of M. manilae (F3,36 = 2.90, P = 0.0481). The parasitoid achieved the lowest pupal weight when it developed in larvae that had been parasitized as 1st instars (Fig. 2).

Fig. 1.

Preferences of Microplitis manilae adult females for the different Spodoptera exigua instars. Shown are the average percent parasitization (± SE) by female parasitoids of 1st through 5th host larval instars when given 40 host larvae of each instar. Letters above the bars represent significant differences between treatments of the different host instars (LSD, P < 0.05).

f01_602.jpg

TABLE 1.

DURATIONS OF THE DEVELOPMENTAL PERIODS OF IMMATURE STAGES OF MICROPLITUS MANILAE PARASITIZED ON DIFFERENT INSTARS OF SPODOPTERA EXIGUA .

t01_602.gif

Life Table Parameters of M. manilae Parasitized on Different Instars of S. exigua

The intrinsic rate of increase (r) (F3,36 = 6.79, P = 0.0036), finite rate of increase (λ) (F3,36 = 6.62, P = 0.0041), net reproduction rate (R0) (F3,36 = 1117.82, P < 0.0001) and mean length of a generation (T) (F3,36 = 4.94, P = 0.0129) of M. manilae were significantly affected by which of the instars had been parasitized. The maximum values of r, λ, R0 and T were achieved when 2nd instars were parasitized. However, r, λ, R0 and T of M. manilae all reached their minimum values when 4th instars of S. exigua were parasitized (Table 2).

Fig. 2.

The weights of Microplitis manilae pupae that developed on different larval instars of Spodoptera exigua. Shown are the average percent parasitization rates (± SE) by female parasitoids of 1st through 4th host larval instars when given 40 host larvae of each instar. Letters above the bars represent significant differences between treatments of the different host instars (LSD, P < 0.05).

f02_602.jpg

Age-Stage Survival Rates, Age-Specific Survival Rates and Age-Specific Fecundities of M. manilae Parasitized on Different S. exigua Instars

The trend in age-stage survival rate (Sxj) of M. manilae reflected developmental rates and survivorship of the parasitoid during various stages of its life cycle in different S. exigua instars. The overall developmental rate of the parasitoid was the fastest when it was parasitized on the 4th instar larvae (Fig. 3).

The maximum daily fecundities of female parasitoids were 11.3, 16.0, 11.5 and 4.4 eggs per female when they parasitized the 1st, 2nd, 3rd and 4th instar larvae, respectively. The longest ovipositional period was observed when they parasitized 2nd instar larvae. The age-specific survival rate (lx) of M. manilae was maintained at a high level (≥ 80%) during 25 days after adult emergence when M. manilae was parasitized the 2nd instars, and thereafter it decreased precipitously. Decreasing trends in age-specific survival rate were significant within 20 days after adult emergence when M. manilae parasitized the first through the fourth instars (Fig. 4).

DISCUSSION

In general, host evaluation and selection of parasitoids are very important because a highquality host can promote the fitness of the parasitoid (e.g., development and fecundity) (Vinson 1990; Godfray 1994; Beckage & Gelman 2004; Li et al. 2006; Murillo et al. 2013). In nature, most parasitoid species can accept or reject hosts for oviposition based on assessment of host qualities (Strand & Pech 1995; Harvey & Strand 2002; Li et al. 2006; Murillo et al. 2013). Therefore, a parasitoid can often select the optimum host age for improving the population quality of the offspring (Wang et al. 1984; Li et al. 2006; Murillo et al. 2013). For example, the early 2nd instar of Tricho- plusia ni (Hübner) was considered to be the most suitable host age for the development of the larval endoparasitoid Campoletis sonorensis (Cameron), because this host age resulted in more parasitized larvae, a higher emergence rate, a higher female ratio of adult parasitoids, and a higher survival rate of immature parasitoids (Murillo et al. 2013). Another study (Li et al. 2006) revealed that 2nd and 3rd instars of M. separate provide the optimum environmental and nutritional conditions for the development of a related species, Microplitis mediator (Haliday). Therefore the percent parasitism and the development of the parasitoid could be optimized when M. separate chose to parasitize 2nd and 3rd host instars (Li et al. 2006).

TABLE 2.

EFFECTS OF THE HOST (SPODOPTERA EXIGUA) INSTAR ON THE LIFE TABLE PARAMETERS OF MICROPLITIS MANILAE.

t02_602.gif

Fig. 3.

Age-stage survival rate (S ij) of Microplitis manilae that developed on different larval instars of Spodoptera exigua.

f03_602.jpg

A earlier study found that M. manilae preferred parasitizing the 49–72 h-old larvae of S. frugiperda, but did not accept larvae older than 130 h (Rajapakse et al. 1985). The results of our study suggested that M. manilae females preferred to parasitize earlier instars of S. exigua, i.e., 2nd or 3rd instars, but never 5th instars. Based on our study and the study of Rajapakse et al. (1985), acceptance of M. manilae to hosts — except that of newly-hatched larvae — decreased with host age. Although the developmental duration for the entire immature stage of M. manilae parasitized on 2nd or 3rd larval S. exigua instars was longer than that on 1st or 4th host instars, the 2nd instar represented the most suitable host stage for high fitness of the parasitoid because on this instar the parasitoid exhibited the longer ovipositional period, the greater age-specific survival rate, and the greater pupal weight.

Fig. 4.

Age-specific survival rate (lx) and age-specific fecundity (mx) of Microplitis manilae that developed on different larval instars of Spodoptera exigua.

f04_602.jpg

A previous study suggested that a larger host larva might be the best nutritional source for M. mediator because the highest pupal weight of the parasitoid was attained on the 4th instar (Li et al. 2006). Other studies reported that preferences for larger hosts had been observed in several parasitoid species (Elzinga et al. 2003; Harvey et al. 2004; Sandanayaka et al. 2009; Kant et al. 2012). Do larger hosts really provide better nutrition for parasitoids? In fact, the optimal host acceptance of a parasitoid may be based on a combination of host qualities, e.g., quality and quantity of nutrition, host defenses and host endocrine changes (Lawrence 1990; Li et al. 2006; Kant et al. 2012; Murillo et al. 2013). Therefore, the host age preference of parasitoid species seems consistent with the theory of optimal host stage (Vinson & Iwantsch 1980; Charnov 1982; Stephens & Krebs 1986; Islam & Copland 1997; Bennett & Hoffmann 1998; Jervis et al. 2008). Several previous studies focused on life table parameters such as intrinsic rate of increase (r), finite rate of increase (λ), and net reproduction rate (R0) have revealed that the population development of an insect natural enemy depends on the nature and quality of its hosts (Tanigoshi & McMurtry 1977; Mo & Liu 2006; McClay & Hughes 2007; Farhadiet al. 2011). In this study, we found that the values of r, λ, and R0 of M. manilae were highest when it parasitized 2nd instars and that r, λ and R0 values were lowest when it parasitized 4th instars. Therefore, we concluded that 2nd instar larvae are the most suitable for the development of M. manilae. This also implies that 2nd larval instar of S. exigua have the best nutritional and endocrine conditions and levels available for the parasitoid.

The selection of the optimal host instar is essential for mass rearing and field release of a parasitoid (Pu 1978; Li et al. 2006). Based on the present study, the 2nd instar of S. exigua is optimal for mass rearing M. manilae because it assures optimum selection, development and fecundity for the parasitoid reared in an insectary. In addition, if biological control of S. exigua relies on field release of M. manilae, the parasitoid should be released when 2nd instars of the host are prevalent in the field.

ENDNOTES

We are very grateful to Dr. Yi-Jing Cen and Dr. Jing-Xian Liu (South China Agricultural University) and Assoc. Prof. Qi-Jin Chen (Zhongshan University) for their help during the experiment, and to several anonymous reviewers for their good suggestions to improve the manuscript. This work was funded by National Natural Science Foundation of China (No. 31071733) and the Special Fund for Agro-Scientific Research in the Public Interest (No. 200803007). Bo Qui and Zhogshi Zhou made equal contributions and both are joint first authors.

REFERENCES CITED

1.

J. N. All , J. D. Stancil , T. B. Johnson , and R. Gouger 1996. Controlling fall armyworm (Lepidoptera: Noctuidae) infestations in whorl stage corn with genetically modified Bacillus thuringiensis formulations. Florida Entomol. 79: 311–317. Google Scholar

2.

K. Ando , R. Inoue , K Maeto , and S. Tojo 2006. Effects of temperature on the life history traits of endoparasitoid Microplitis manilae Ashmead (Hymenoptera: Braconidae), parasitizing the larvae of the common cutworm, Spodopteralitura Fabricius (Lepidoptera: Noctuidae). Japanese J. Appl. Entomol. Zool. 50: 201–210. Google Scholar

3.

N. K Bajpai , C. R. Ballal , N. S. Rao , S. P. Singh , and T. V. Bhaskaran 2006. Competitive interaction between two ichneumonid parasitoids of Spodoptera litura. BioControl 51: 419–438. Google Scholar

4.

N. E. Beckage , and D. B. Gelman 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49: 299–330. Google Scholar

5.

D. M. Bennett , and A. A. Hoffmann 1998. Effects of size and fluctuating asymmetry on field fitness of the parasitoid Trichogramma carverae (Hymenoptera: Trichogrammatidae). J. Anim. Ecol. 67: 580–591. Google Scholar

6.

E. L. Charnov 1982. The theory of sex allocation. Princeton University Press, Princeton, NJ. Google Scholar

7.

H. Chi 1988. Life-table analysis incorporating both sexes and variable development rate among individuals. Environ. Entomol. 17: 26–34. Google Scholar

8.

H. Chi 2005. TWOSEX-MSChart: computer program for agestage, two-sex life table analysis. National Chung Hsing University, Taichung, Taiwan. ( http://140.120.197.173/Ecology/prod02.htm). Google Scholar

9.

H. Chi , and H. Liu 1985. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sinica 24: 225–240. Google Scholar

10.

P. V. Deshmukhe , A. A. Hooli , and S. N. Holihosur 2010. Bioinsecticidal potential of Vinca rosea against the tobacco caterpillar, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Recent Res. Sci. Technol. 2: 1–5. Google Scholar

11.

G. W. Elzen , and P. J. O'brien 1989. Toxic and behavioral effects of selected insecticides on the heliothis parasitoid Microplitis croceipes (Cresson). Entomophaga 34: 87–94. Google Scholar

12.

J. A. Elzinga , J. A. Harvey , and A. Biere 2003. The effects of host weight at parasitism on fitness correlates of the gregarious koinobiont parasitoid Microplitis tristis and consequences for food consumption by its host, Hadena bicruris. Entomol. Exp. Appl. 108: 95–106. Google Scholar

13.

R. E. Foster 1989. Strategies for protecting sweet corn ears from damage by fall armyworms (Lepidoptera: Noctuidae) in southern Florida. Florida Entomol. 72: 146–51. Google Scholar

14.

H. C. J. Godfray 1994. Parasitoids behavioral and evolutionary ecology. Princeton University Press, Princeton, N.J. Google Scholar

15.

D. Goodman 1982. Optimal life histories, optimal notation, and the value of reproductive value. American Nat. 119: 803–823. Google Scholar

16.

J. A. Harvey , T. M. Bezemer , A. Elzinga , and M. R. Strand 2004. Development of the solitary endoparasitoid Microplitis demolitor: Host quality does not increase with host age and size. Ecol. Entomol. 29: 35–43. Google Scholar

17.

J. A. Harvey , and M. R. Strand 2002. The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology 83: 2439–2451. Google Scholar

18.

K. S. Islam , and M. J. W. Copland 1997. Host preference and progeny sex ratio in a solitary koinobiont mealybug endoparasitoid, Anagyrus pseudococci (Girault), in response to its host stage. Biocontrol Sci. Technol. 7: 449–456. Google Scholar

19.

M. A. Jervis , J. Ellers , and J. A. Harvey 2008. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53: 361–385. Google Scholar

20.

R. Kant , M. A. Minor , and S. A. Trewick 2012. Fitness gain in a koinobiont parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) by parasitising hosts of different ages. J. Asia-Pacific Entomol. 15: 83–87. Google Scholar

21.

K. R. Kranthi , D. R. Jadhav , S. Kranthi , R. R. Wanjari , S. S. Ali , and D. A. Russell 2002. Insecticide resistance in five major insect pests of cotton in India. Crop Prot. 21: 449–460. Google Scholar

22.

P. Lara , F. Ortego , E. Gonzalez-Hidalgo , P. Castañera , P. Carbonero , I. And Diaz 2000. Adaptation of Spodoptera exigua (Lepidoptera: Noctuidae) to barley trypsin inhibitor BTI-CMe expressed in transgenic tobacco. Transgenic Res. 9: 169–178. Google Scholar

23.

P. O. Lawrence 1990. The biochemical and physiological effects of insect hosts on the development and ecology of their insect parasites: an overview. Arch Insect Biochem. Physiol. 13: 217–228. Google Scholar

24.

J. C. Li , T. A. Coudron , W. L. Pan , X. X. Liu , Z. Y. Lu , and Q. W. Zhang 2006. Host age preference of Microplitis mediator (Hymenoptera: Braconidae), an endoparasitoid of Mythimna separata (Lepidoptera: Noctuidae). Biol. Control 39: 257–261. Google Scholar

25.

L. Z. Luo , Y. Z. Cao , and X. F. Jiang 2000. Analysis on occurrence characteristic and population dynamics of Spodoptera litura. Plant Prot. 26: 37–39. Google Scholar

26.

A. S. McClay , and R. B. Hughes 2007. Temperature and host-plant effects on development and population growth of Mecinus janthinus (Coleoptera: Curculionidae), a biological control agent for invasive Linaria spp.Biol. Control 40: 405–410. Google Scholar

27.

T. L. Mo , and T. X. Liu 2006. Biology, life table and predation of Feltiella acarisuga (Diptera: Cecidomyiidae) feeding on Tetranychus cinnabarinus eggs (Acari: Tetranychidae). Biol. Control. 39: 418–426. Google Scholar

28.

H. Murillo , D. W. A. Hunt , and S. L. VanLaerhoven 2013. Host suitability and fitness-related parameters of Campoletis sonorensis (Hymenoptera: Ichneumonidae) as a parasitoid of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Biol. Control 64: 10–15. Google Scholar

29.

Z. L. Pu 1978. Theory and Technique of Biological Pest Control. China Science Press, Beijing, China. Google Scholar

30.

B. Qiu , Z. S. Zhou , S. P. Luo , and Z. F. Xu 2012. Effect of temperature on development, survival, and fecundity of Microplitis manilae (Hymenoptera: Braconidae). Environ. Entomol. 41: 433–-730. Google Scholar

31.

R. H. S. Rajapakse , V. H. Waddill , and T. R. Ashley 1992. Effect of host age, parasitoid age and temperature on interspecific competition between Chelonus insularis Cresson, Cotesia marginiventris Cresson and Microplitis manila Ashmead. Intl. J. Trop. Insect Sci. 13(1): 87–94. Google Scholar

32.

R. H. S. Rajapakse , T. R. Ashley , and V. H. Waddill 1985. Biology and host acceptance of Microplitis manilae (Hymenoptera: Braconidae) raised on fall armyworm larvae Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomol. 68(4): 653–657. Google Scholar

33.

J. R. Raulston , and P. D. Lingren 1972. Methods for large-scale rearing of the tobacco budworm. U.S. Dept. Agr. Prod. Res. Rept. Google Scholar

34.

B. D. Roitberg , G. Boivin , and L. E. M. Vet 2001. Fitness, parasitoids, and biologicalcontrol: an opinion. Canadian Entomol. 133: 429–438. Google Scholar

35.

G. Salt 1938. Experimental studies in insect parasitism. VI. Host suitability. Bull. Entomol. Res. 29: 223–246. Google Scholar

36.

W. R. M. Sandanayaka , J. G. Charles , and D. J. Allan 2009. Aspects of the reproductive biology of Pseudaphycus maculipennis (Hym: Encyrtidae), a parasitoid of obscure mealybug, Pseudococcus viburni (Hem: Pseudococcidae). Biol. Control 48: 30–35. Google Scholar

37.

SAS Institute. 2004. SAS User's Guide: Statistics. SAS Institute, Cary, NC. Google Scholar

38.

D. W. Stephens , and J. R. Krebs 1986. Foraging theory. Princeton, New Jersey. Google Scholar

39.

M. R. Strand , and L. L. Pech 1995. Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40: 31–56. Google Scholar

40.

J. S. Sun , and S. S. Huang 2010. Evaluation of potential control ability of Snellenius manilae (Ashmead) against Spodoptera exigua (Hübner). Act. Ecol. Sin. 30: 1494–1499. Google Scholar

41.

L. K Tanigoshi , and J. A. McMurtry 1977. The dynamics of predation of Stethorus picopes (Coleoptera: Coccinellidae) and Typhlodromus floridanus on the prey Oligonychus punicae (Acarina: Phytoseiidae, Tetranychidae) I. Comparative life history and life table studies. Hilgardia 8: 237–288. Google Scholar

42.

S. B. Vinson 1990. Physiological interactions between the host genus Heliothis and its guild of parasitoid. Arch. Insect Biochem. 13: 63–81. Google Scholar

43.

S. B. Vinson , and G. F. Iwantsch 1980. Host suitability for insect parasitoids. Annu. Rev. Entomol. 25: 397–419. Google Scholar

44.

D. A. Wang , L. Z. Nan , X. Sun , and X. Z. Li 1984. Study on a bionomics of Microplitis spp., larval parasitic wasp of Helicoverpa armigera. Nat. Enemies Insect 6: 211–218. Google Scholar

45.

J. W. Wilson 1932. Notes on the biology of Laphygma exigua Hübner. Florida Entomol. 16: 33–39. Google Scholar

46.

K. W. Yeh , M. I. Lin , S. J. Tuan , Y. M. Chen , C. J. Lin , and S. S. Kao 1997. Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confers resistance against Spodoptera litura. Plant Cell Rept. 16: 696–699. Google Scholar

47.

Z. S. Zhou , J. Y. Guo , H. S. Chen , and F. H. Wan 2010. Effects of temperature on survival, development, longevity and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a biological control agent against invasive ragweed, Ambrosia artemisiifolia L. (Asterales: Asteraceae). Environ. Entomol. 39: 1021–1027. Google Scholar
Bo Qiu, Zhongshi Zhou, and Zaifu Xu "Age Preference and Fitness of Microplitis manilae (Hymenoptera: Braconidae) Reared on Spodoptera exigua (Lepidoptera: Noctuidae)," Florida Entomologist 96(2), 602-609, (1 June 2013). https://doi.org/10.1653/024.096.0227
Published: 1 June 2013
JOURNAL ARTICLE
8 PAGES


SHARE
ARTICLE IMPACT
Back to Top