Advances in Agricultural Science 04 (2016), 04: 35-44
Life Table Parameters of Opius dissitus Musebeck (Braconidae), A Parasitoid of Leafminer, Liriomyza sativae Blanchard
S. Azad 1 and Md. Wahedul Islam 1
1Institute of Biological Sciences, University of Rajshahi, Rajshahi, Bangladesh.
The leafminer, Liriomyza sativae Blanchard is a phytophagous fly infesting a wide range of vegetable and ornamental plants. Opius dissitus Musebeck is an endoparasitoid of larvae-pupae of L. sativae. The life history of parasitoid were assessed in different temperatures under laboratory conditions. The mean developmental time of O. dissitus from egg to adult was 15-22 days depending on the prevailing temperature. An average of 108.75 progenies were produced per female during her lifetime. O. dissitus adults emerge out of the leafminer pupae. One adult emerges from a single parasitized pupa. Mean adult longevity was 12.00 for females and 13.15 days for males. The highest mortality was 45% in June. Eggs laid by females were 22.85 per day. The net reproductive rate (R0) was highest 58.77 at 320C but lowest 15.45 at 200C. The intrinsic rate of increase (rm) was increased with increasing temperature from 20 to 320C but peaker (0.56 day-1) at 320C. Mean generation time (tG) decreased significantly with increasing temperature ranging from 14.13 days at 200C to 9.89 days at 320C. The finite rate of increase higher at 320C (1.67 day-1) and lower 1.21 day-1 at 200C. The results suggested that O. dissitus could develop and reproduce within a wide range of temperatures.
Keywords: Life table, Opius dissitus, Musebeck, Liriomyza sativae Blanchar
The construction of life tables is an important component in the understanding of the population dynamics of a species (Southwood 1978). Several criteria and diverse approaches exist for evaluating and selecting the best agents for controlling a pest (Waage 1990). The effectiveness of a parasitoid species as a biological control agent is linked to the quality of an individual parasitoid’s fitness (Ridgway and Morrison 1985). The life table enables one to best visualize the relative contributions of survival and reproduction to the mean fitness of a population, so that the more comprehensive the life table, the more accurately can these contributions be described. The key life history traits are fecundity, the age at first reproduction and the timing of peak reproduction, the interaction of reproductive effort with adult mortality and the variation in these traits among an individual’s progeny (Stearns 1976). The age of the female parasitoids may influence their fecundity and sex ratio, and knowledge of sex ratio is important in their use in biological control program (Luck and Podler 1982, Waage 1986).
Fecundity can be measured as potential or realized fecundity. The numbers of eggs present in the ovary is a conservative estimate of the potential fecundity for many species, particularly for pro-ovigenic insects and termed as egg load. In pro-ovigenic parasitoids, which emerge as adults with full lifetime complement of mature eggs, the egg load is simple a decreasing function of egg laid, and there is thus no distinction between egg-load limitation and fecundity limitation. In contrast, synovigenic parasitoids continue to mature eggs throughout their lifetime, often in conjunction with host feeding, and may thus experience short-term egg load limitation without incurring lifetime fecundity limitation (Lane et al. 1999). The lifetime fecundity or reproductive potential of a parasitoid has frequently been cited in the biological control literature as an important characteristic of successful biological control agents. High fecundity is considered necessary for parasitoids to be able to reproduce more rapidly than the pest population and to respond to changes in the abundance of the pest (Waage and Hessel 1982, Waage 1990, Ehler 1995).
As the synovigenic parasitoid emerges with fewer eggs than her full complements, dissection of ovaries at a certain age could only provide an estimate of egg-holding capacity of the parasitoid at that age and may not reflect potential or real fecundity of the parasitoid (Leather 1988). Life table parameter study can provide the following information:
the egg holding capacity of the parasitoid at a certain age as a measure of their potential fecundity at that age;
age specific survival and progeny production pattern of the parasitoids and
the intrinsic rate of population increase (rm) of the parasitoids under laboratory conditions
The rate of population increase of insects be expressed as the intrinsic rate of increase (rm). The intrinsic rate of increase depends on fecundity, rate of development and survival. Population changes, on the other hand, are caused by many factors including parasitism, predation, food availability and diseases.
The aim of this study was, therefore, to investigate the biological life table and intrinsic rate of natural increased of O. dissitus at four constant temperatures. Knowledge of the life table and intrinsic rate of natural increase will enhance the possibilities for its more effective use as a biological control agent under temperature conditions.
Materials and Methods
Effect of temperature on parasitism
Knowledge of developmental rates of host and parasitoid is useful in analysis of population level impacts of parasitoids where total numbers entering different stages must be determined from stage frequency data, or where trends of percentage parasitism are to be interpreted in terms of underlying causal processes such as differential developmental periods of host and parasitoid (van Driesche and Bellows 1996). For poikilothermal organisms, basic information on developmental and reproduction characteristics as affected by temperature and host are needed for estimates of parameters that are used in population models (Gutierrez et al. 1977). Temperature is the most important factor affected development in poikilotherm organisms (Sharpe and DeMichele 1977). When the rate of development is plotted against temperature, the result is usually a sigmoid curve with a straight line at the intermediate temperatures (Campbell et al. 1974, Wagner et al. 1984, Highley et al. 1986).
The life tables of O. dissitus at different temperatures were constructed from the life history and fecundity data. The actual death occurred in the egg and immature stages were taken into account when the female survival rate at each temperature was determined. Life-tables of an insect can be constructed using the survival data of a specific age class (lx) and the female offspring produced per female offspring produced per female in each class (mx). On the basis of lx and values, the following population parameters were calculated (Messenger 1964).
Gross reproductive rate (GRR) is the mean total number of eggs produced by a female over its life time, (GRR = ∑mx) measured in female eggs/female/generation.
The net reproductive rate (R0) is the number of times a population will multiply per generation, (R0 = ∑lxmx) measured in females/female/generation.
Finite rate of increase (λ) is the number of times the population will multiply itself per unit time, (λ = e) measured in females/female/day.
Hence the finite rate of increase (λ) is the natural antilogarithm of the intrinsic rate of increase. Therefore, any statement about the rate of increase of a population is incomplete without reference to the age distribution of that population, unless every female in it is producing offspring at the same rate at all ages, and at the same time is exposed to similar chances of dying at all ages (Birch 1948).
The mean generation time (T): The comparison of two or more populations by means of their net reproductive rates may be quite misleading unless the mean length of the generation is the same.
The relation between numbers and time in a population growing exponentially is given by NT = N0et. When T = the mean length of the generation, and then from the definition of net reproductive rate NT/N0 = 0r, hence 0r = ert and T = loge 0r/rm. measured in days.
It follows that an accurate estimate of the mean length of a generation cannot be obtained until the value of rm is known. Therefore, for estimation purposes, T may be calculated as
T = ∑xlxmx/∑lxmx.
The doubling time (DT) is the time required for a given population to double its number, (DT = loge2/rm), measured in days.
The capacity for increase (rc) is an approximation for rm. It is calculated as follows: rc = loge R0/Tc, where Tc is the cohort generation time, defined as the mean age of maternal parents in the cohort at birth of the female offspring, Tc = ∑lxmx/R0.
Different life table parameters of O. dissitus were calculated using the adult survival (lx), number of female progeny per day (mx) and female sex ratio with the help of QBASIC siftware (Jervis and Copland 1996).
Parasitism, egg laying, offspring production and sex ratio
The highest parasitsm of O. dissitus was observed at 260C which differed significantly from that of 20, 24, 28 and 320C (P<0.01). The lowest parasitization was recorded at low (200C) and high (320C) temperature 79.85 and 108.75 eggs/female respectively. The daily fecundity (egg/female/day) was strongly affected by the temperature (Figure 1). Total fecundity and offspring production per female was highest at 320C which had significant difference from the temperature of 20, 24, 28 and 320C.
Significantly fewer eggs and offspring production per female was found at low (200C) and high (300C) temperature. Most of the eggs were laid by O. dissitus female with in first day of emergence and only few eggs were deposited on the 5th days. There was no significant difference for offspring production per female among the temperature 20 and 300C. Offspring sex ratio of O. dissitus vaired with temperature and was female biased throughout the entire range of temperatures, showing a maximum 70% female at 280C, and had significant difference with low and high temperature but was similar at 22 and 300C. The effects of temperature on the sex ratio and offspring production was highly significant (P<0.01). In most cases, performance increased with increasing temperature up to 280C. When it reached in peak then declined again with further rise of temperature 300C (Figures 1-6).
Egg to adult development
Temperature had significant effect on the egg to adult development duration of O. dissitus. Developmental period of O. dissitus ranged from 15 to 22 days depending on the prevailing temperature.
Life table parameters
Age specific survibal (lx) and fecundity rate (mx) of O. dissitus were determined through studying the number of egg laid, their hatchability, survival rate and the proportion of female offspring. The age specific survival rate (lx) started to drop at earlier ages as the temperature increased from 20 to 320C (Figures 5 and 6). The age specific fecundity rate ((mx) showed its peak at 320C which decreased with increasing temperature of 28 and 320C. Fecundity of the parasitoid remained low at the lower level of temperature of 18 and 240C (Figure 6).
The net reproductive rate (R0), the intrinsic rate of natural increase (rm) and the mean generation time (tG) were affected by the temperature and there were significance differences among the temperature responses (Table 1). The net reproductive rate significantly differed with variable temperature (F=12.35, df=3, P<0.01). The highest (R0) value 58.77 was observed at 320C whereas lowest 15.45 was found at 200C. The intrinsic rate of increase (rm) of O. dissitus was found to be significantly different (F= 270.49, df=3, P<0.01), depending on the different temperatures, at which they were reared. The rm values increased with increasing temperature from 20 to 320C but peaked at 320C (0.56 day-1). Mean generation time (tG), decreased significantly with increasing temperature ranging from 14.13 days at 200C to 9.89 days at 320C. So, maximum value for the mean generation time was observed as 14.13 days at 200C. Doubling time (tD) differed significantly and found to decrease with increasing temperatures showing 3.58 days at 200C to 1.34 days at 320C (F=198.13, df=3, P<0.01) (Table 1).
Table 1. Life table parameters (mean ± S.E.) of Opius dissitus at different temperatures: intrinsic rate of natural increase (rm, day-1), net reproductive rate (R0), mean generation time (tG, day), finite rate of increase (λ), doubling time (tD, day)
0.193 ± 0.01d
15.45 ± 0.01d
14.13 ± 0.34a
1.21 ± 0.01c
3.58 ± 0.01a
0. 255 ± 0.01c
22.38 ± 0.01c
12.18 ± 0.12b
1.29 ± 0.01c
2.72 ± 0.01b
0.380 ± 0.01b
43.56 ± 0.01b
9.93 ± 0.02c
1.46 ± 0.01b
1.82 ± 0.01c
0.516 ± 0.01a
58.77 ± 0.01a
9.89 ± 0.01c
1.67 ± 0.01a
1.34 ± 0.01c
Level of significance
P < 0.01
P < 0.01
P < 0.01
P < 0.01
P < 0.01
aNumber of females tested Values within the column followed different letter are significantly different at 1% level of Tukey´s Post-hoc Test.
Figure 1. Life time egg laying and hatching of instars Opius dissitus
Figure 2. Percent survival of different of Opius dissitus
Figure 3. Egg to adult development of male and female Opius dissitus
The cohorts at 200C temperature had the highest tD value of 3.58 days indicating that a population of the parasitoid would be double in this period of time. This parameter had significant differences among 20 to 320C temperature. In addition, the finite rate of increase was significantly affected (F=123.81, df=3, and P<0.01) at the temperature between 20 to 320C but reached at 1.67 day-1) and the lowest value of was 1.21 day-1 at 200C (Figures.7 -8).
Temperature is one of the most determining abiotic factors affecting the development rate, cumulative fertility, longevity, sex ratio and emergence rate of Opius spp. A temperature dependable life table of O. dissitus was estimated using the biological characterstics such as rate of parasitism, development, sex ratio, emergence rate and adult longevity. Temperature was found to influence all the parameters studied. Rate of parasitism, emergence and female sex were maximum at the temperature of 320C. Longevity of the parasitoid decreased with increasing temperature. The effect of temperature on parasitism and other biological parameters of many species of Opius has been elsewhere (Rustam 2014).
The authors demonstrated increased development of different Opius with decreasing temperature and higher longevity of female wasp with lower temperature.
Temperature and host plants play an important role in population growth. Rustam et al. (2014) showed that the mean generation time of O. chromatomyiae, a parasitoid of vegetable leafminer L. huidobrensis was shorter at a higher temperature than at a lower one. They also mentioned an increased intrinsic rate of increase with increasing temperature. Mean generation time of O. chromatomyiae was found to be shortened with increasing temperature and at lower temperature below 150C, there was a long developmental time coupled with the fact that eggs were laid more slowly early in the life of insect Rustam et al. (2014). This supports the conclusion of Birch (1948) as one of the major effects of temperature on the intrinsic rate of increase of insect population.
Figure 4. Temperature effects on oviposition rate (eggs/female) of Opius dissitus
Figure 5. Percent survival and female ratio of Opius dissitus
Figure 6. Temperature effects on survival rate of Opius dissitus
Temperature simultaneously affects several component variables in the calculation of rm. An increase in temperature within the limit of observed temperatures consistently lowers both the survival rate and the oviposition period of O. chromatomyiae, while on the other hand, an increase in temperature increases mean total and mean daily fecundity up to a peak of 320C. Above 320C, the acceleration of egg output at the onset of oviposition continues; however, at such a high temperature, age specific survival (lx) declines rapidly and limits the rm. The lowest rm values observed can be attributed to a low oviposition rate at 200C and the high mortality at 320C (Rustam et al. 2014).
The size and growth stages also affect the life history parasmeters of insect parasitoids. The faster development of daughters in large hosts decreases generation time (T), which is inversely related to the intrinsic rate of increase (rm) of the parasitoid population (Tripathi and Singh 1990).
Fertility life table studies provide a powerful technique for evaluation of population dynamics because they provide a detailed description of age-specific mortality of individuals in the population. Fertility life table parameters differed significantly in response to the different temperature treatments showing a varied net reproduction rate (Ro) of O. dissitus from 15.45 to 58.77 according to the temperature variation. The maximum increase in net reproduction rate (58.77) was found at 320C. Haghani et al. (2006) found that the net reproduction rate varied according to the temperature variation for O. dissitus. Rustam et al. (2014) related the reproduction of the net reproductive rate at high temperatures to the production of both males and females at these temperatures. This can explain the present results, where the Ro was reduced at higher temperature.
The intrinsic rates of increase (rm) of the parasitoid O. dissitus for the different temperatures varied significantly and the highest rate was found at 320C. Cohort generation time (tG) differed significantly at variant temperatures. The finite capacity for increase (λ) of the parasitoids increased as with increasing temperature. Doubling time (tD) decreased with the increase of temperature, the longest time required occurring at 200C and the shortest time at 320C. The results of these life tables parameters were in agreement with different authors (Bordat 1995, Li et al. 2011, Rustam et al. 2014) and reflect positive attributes for O. dissitus as potential biocontrol agent of leaf miner.
Ferility life table is used to calculate biological parameters and evaluate biological performance and to compare fitness of insects such as Opius wasps. As a general conclusion, biological parameters obtained in laboratory studies can be used as part of a selection process to identify the best biological control agents for augmentation programs (Bellows et al. 1992).
Results obtained in the study of life table parameters of the parasitoid O. dissitus, showed the temperature range from 28 to 320C is favorable for its growth, development and survival. The particular range of temperature prevails in Bangladesh for most of the vegetable growing seasons indicating that it is a well suited species in the locality. Moreover, parasitism performance of O. dissitus on leaf miner larvae and successful offspring production in the laboratory condition also indicates that this species could be a promising biocontrol agent for its rearing. Growers and pest management advisors must carefully evaluate this Opius spp. determine if and how this temperature dependent life table data can best fit into their Integrated Pest Management programs. This laboratory data would definitely be a base in evaluating its field performance through to semi filed and field experiments. Therefore, this finding is expected to provide important information in designing a comparahensive program for IPM of leafminer in Bangladesh. However, further studies on the parameters such as searching behaviour, diapauses and dispersal, suitable alternate hosts for rearing need to be undertaken for it’s beter use in IPM program.
Institute of Biological Sciences, University of Rajshahi has provided the laboratory facility and University Grants Commission of Bangladesh for financial support for their approved project.
Bellows Jr, T.S., Van Driesche, R.G. and Elkinton, J.S., 1992. Life-table construction and analysis in the evaluation of natural enemies. Annual review of entomology, 37(1), pp.587-612.
Bordat, D., Coly, E.V. and Roux-Olivera, C., 1995. Morphometric, biological and behavioural differences between Hemiptarsenus varicornis (Hym., Eulophidae) and Opius dissitus (Hym., Braconidae) parasitoids of Liriomyza trifolii (Dipt., Agromyzidae). Journal of Applied Entomology, 119(1-5), pp.423-427.
Birch L C 1948. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol.17: 15-26
Campbell A, Frazer B D, Gilbert N, Guitierez A P and Mackauer M 1974. Temperature requirement of some aphids and their parasites. J. App. Entomol. 11: 431-438
Ehler L E 1995. Biological control of obscure scale (Homoptera: Diaspidae) in California. An experimental approach. Environ. Entomol.24: 779-795
Gutierrez A P, Butler G D, Wang Y and Westphal D 1977. The interaction of pink ball worm (Lepidoptera: Gelechidae), cotto and weather: A detailed model. The Can. Entomol. 109: 1457-1468
Higley L G, Pedigo L P and Ostlie K P 1986. Degday: A program for calculating degree-day and assumption behind the degree day approach. Environ. Entomol.15: 999-1016
Jervis M A and Copland M J W 1996. The life cycle. Pp 63-161 In Jervis M A, Kidd N A C (eds). Insect Natural Enemies: Practical Approaches to their Study and Evaluation. London, Chapman and Hall. Pp. 491
Lane S D, Mills N J and Getz W M 1999. The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data. Ecol. Entomol. 24: 181-190
Leather S R 1988. Size in reproduction potential and fecundity in insects: things are not as simple as they seem. Oikos51: 386-388
Li Jian, Seal D and Leibee G 2014. Leafminer parasitoid Opius dissitus Muesbeck (Insecta: Hymenoptera: Braconidae). University of Florida IFAS Extension EENY 501-502.
Luck R F and Podler H 1982. Competitive displacement of Aphytis lignanensis by Aphytis melinus, the role of host size and female progeny production. Ecol. Entomol. 7: 409-421
Messenger P S 1964. Use of life tables in a bio-climatic study of an experimental aphid-braconid wasp host-parasite system. Ecology45: 119-131
Ridgway R L and Morrison R K 1985. Word-wide perspective on pratical utilization of Trichogramma with special reference to control of Heliothis on Cotton. The Southwestern Entomologist8: 190-198
Rustam R, Pudjianto, Maryana N, Rauf A, Shepard M and Hammig M 2014. Biology of Opius chromatomyiae (Hymenoptera: Braconidae), an increasingly important parasitoid of leafminers in West Java, Indonesia. USAID, Clemson University
Sharpe D J H and DeMichele D W 1977. Reaction kineties of poikilothermal development. J. Theor. Biol.64: 649-670
Southwood T R E 1978. Ecological Methods, with Particular Reference to the Study of Insect Populations. Chaoman and Hall, London pp. 524
Stearns S C 1976. Life history tactics: a review of the insects. The Quar. Rev. Biol. 51: 79-85
Tripathi R N and Singh R 1990. Fecundity, reproductive rate, longevity and intrinsic rate of increase of an aphidiid parasitoid Lysiphlebia mirzai Shuja-Uddin. Entomophaga34: 601-610
Waage J K 1986. Family planning in parasitoids adaptive patterns of progeny sex allocation pp 63-95 In Waage J and Greathead D (Eds) Insect parasitoids. Academic Press, London pp 389
Waage J K 1990. Ecological theory and selection of biological control agents. Pp 135-157 In Mackauer M, Ehler L E and Ronald J (eds). Critical Issues in Biological Control. Intercept, Andover, Hants pp 330
Waage J K and Hassel 1982. Parasitoids as biological control agents – a fundamental approach. Parasitology84: 241-268
Wagner T, Sharp P G H, School R M and Coulson R N 1984. Modeling insect development rates: a literature review and application of a biophysical model. Ann. Entomol. Soc. Am. 77: 2008-2025