A Life Table for Liriomyza trifolii (Diptera: Agromyzidae) in a Temperate Zone of Northeast Egypt With Key Factor Analysis

A Life Table for Liriomyza trifolii (Diptera: Agromyzidae) in a Temperate Zone of Northeast Egypt... Abstract The American serpentine leaf miner, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae), is a perennial pest of leguminous crops in the Mediterranean region. A life table was constructed for L. trifolii infesting broad bean, Vicia faba L., in northern Egypt. Key factor analysis was used to rank sources of immature mortality over two seasons. Leaf miners had three successive generations, and a partial fourth, in each year, with peak abundance in March–April. Less than 15 and 22% of L. trifolii survived to adult in seasons one and two, respectively. The largest contributor of immature leaf miner mortality in both seasons was unknown (41.2 and 39.1% of total mortality, respectively), and likely comprised a combination of abiotic factors, parasitoid-inflicted mortality (host-feeding), and predation. Parasitism was second, contributing 36.2 and 35.6% of total mortality in the two seasons, respectively, primarily due to larval parasitism by Diglyphus isaea (Walker) (Hymenoptera: Eulophidae), and low levels of larval–pupal parasitism by Opius pallipes Wesmael (Hymenoptera: Braconidae) and Halticoptera circulus (Walker) (Hymenoptera: Pteromalidae). Residual mortality resulted from malformed pupae or failed adult emergence. Key factor analysis revealed malformation to be the major cause of pupal mortality. Sequential regression confirmed that unknown mortality and D. isaea were the top stage-specific factors, both acting on larvae. Parasitoid abundance tracked host abundance across generations, but density dependence was not observed for any mortality factor, and the magnitudes of regression slopes were small. The results indicate the potential importance of conservation biological control in management of L. trifolii, given that naturally occurring parasitoids and other biotic/abiotic factors exert significant mortality on immature leaf miners. Diglyphus isaea, Halticoptera circulus, mortality, Opius pallipes, Vicia faba Flies of the genus Liriomyza (Diptera: Agromyzidae) are leaf miners and cosmopolitan pests of various vegetable and horticultural crops (Chabi-Olaye et al. 2008). The genus includes more than 300 species worldwide, with 23 considered to be economically important pests (Wei et al. 2006, Kang et al. 2009). The American serpentine leaf miner, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae), feeds on a wide range of plants and is a key pest of vegetable crops worldwide (e.g., Kang et al. 2009, Hernández et al. 2011), including in Egypt (Metwally 1991, El-Serwy 1993, Ibrahim 1995). It is highly adaptable and has spread through both temperate and tropical regions, becoming increasingly difficult to control (Supartha et al. 2005, Gao et al. 2011). Heavy infestations of L. trifolii have resulted in the closure of flower farms, the loss of jobs, and the loss of overseas markets due to quarantine restrictions (Spencer 1985, IPPC 2005). More than 150 species of parasitoids have been recorded attacking various life stages of Liriomyza species (Waterhouse and Norris 1987, Murphy and LaSalle 1999, Claudio and Welter 2001), of which the genus Diglyphus (Hymenoptera: Eulophidae) is one of the most important groups (Liu et al. 2009, Mujica and Kroschel 2011). A survey of hymenopterous parasitoids attacking Liriomyza spp. in Egypt identified 12 species (Metwally 1991), the dominant ones being Opius pallipes Wesmael (Hymenoptera: Braconidae), Halticoptera circulus (Walker) (Hymenoptera: Pteromalidae), and Diglyphus isaea (Walker) (Hymenoptera: Eulophidae) (El-Serwy 1993, Ibrahim 1995). Opius pallipes is a solitary larval–pupal endoparasitoid of both L. trifolii and Liriomyza bryoniae (Kaltenbach) (Diptera: Agromyzidae), although it prefers the former species (Elkhouly et al. 2017). Parasitism of L. trifolii by O. pallipes in Egypt is low early in the season, and peaks during March (Saleh et al. 1983). This species has been successfully established in Dutch greenhouses where, in combination with Dacnusa sibirica Telenga (Hymenoptera: Braconidae), it maintains L. trifolii populations at very low levels and inflicts up to 100% parasitism (Yu et al. 2004). Halticoptera circulus is a larval–pupal endoparasitoid that has been successfully introduced and established throughout North America, including Hawaii (Johnson and Hara 1987, Schuster et al. 1991). Diglyphus isaea is a solitary ectoparasitoid of agromyzid leaf miner larvae, including those of the pea leaf miner, Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae), the vegetable leaf miner, Liriomyza sativae Blanchard (Diptera: Agromyzidae), as well as L. trifolii (Ode and Heinz 2002, Liu et al. 2009). It has been recorded attacking Liriomyza species on vegetable crops and ornamental plants in the United States, Europe, Asia, and some parts of Africa (Ode and Heinz 2002, Liu et al. 2009, Musundire et al. 2012). Ozawa et al. (2001) found D. isaea to be the dominant parasitoid of L. trifolii larvae on tomato in Japan, where it is now effectively used in augmentation biological control in greenhouses. In a greenhouse survey in southern Portugal, Goncalves and Almeida (2005) reported that two ectoparasitoids, Diglyphus poppoea Walker (Hymenoptera: Eulophidae) and D. isaea, achieved up to parasitism of 80–85% of Liriomyza spp. However, the role of parasitoids in naturally controlling L. trifolii in Egypt has been largely neglected, even though knowledge of the contribution of parasitism to pest mortality could provide valuable insights to aid the development of management strategies and tailor them to local conditions. Despite the importance of L. trifolii as a pest of legume production in Egypt, local information is lacking on its population dynamics and parasitism levels. Estimates of leaf miner population cycles are required to assess the current status of the pest in Egypt and knowledge of its patterns of seasonal abundance would be useful to focus management efforts. Rapid increases in leaf miner populations can result from insecticide applications that disrupt natural biological control (Saito et al. 1996), and management can be complicated by the evolution of insecticide resistance in fly populations (Hofsvang et al. 2005). Egyptian agriculture could benefit from biological control programs that utilize locally effective parasitoid species, similar to those that have been established in other countries (Murphy and La Salle 1999, Chow and Heinz 2004). Quantitative information on key sources of natural pest mortality can be useful for improving the efficacy of augmentation or conservation biological control in integrated pest management programs. Life tables provide one method for partitioning mortality among life stages in insect populations (Morris and Miller 1954). From an ecological perspective, life tables provide valuable insights into intrinsic vulnerabilities in pest life history, in addition to detailed information on pest population dynamics. Life tables provide a comprehensive analysis of survivorship and life expectancy (Ali and Rizvi 2007; Yzdani and Samih 2012) as well as a means of partitioning the relative contributions of various mortality factors to pest population suppression (Bellows et al. 1992; Mohapatra 2007). The objective of this study was to construct a stage-specific life table for L. trifolii (sensuSouthwood 1978) that would enable: 1) characterization of the population dynamics of L. trifolii on broad bean over two successive growing seasons in northern Egypt, 2) calculation of the percentage of larvae parasitized, and 3) determination of parasitism’s relative contribution to total mortality of the pest. Materials and Methods Sampling This study was carried out at the experimental farm of the Faculty of Agriculture, Mansoura University during two successive seasons (2015/2016 and 2016/2017). A cultivated area of 200 m2 was divided into four equal plots. Broad bean, Vicia faba L., cv Giza 843, was planted in all during the third week of November in the first year, and in the last week of November in the second year. Recommended agricultural practices were followed in managing the field and no insecticide applications were made. Beginning 3 wk after planting, samples of broad bean leaflets were taken weekly until the end of the season (harvest). Each sample consisted of 100 leaflets (25 leaflets from each quarter of the field), collected randomly from different plant heights. The samples were collected in plastic bags and transferred to the laboratory for examination under a binocular microscope (Optika ST-40B-2L). The numbers of living leaf miner larvae, larvae parasitized by the ectoparasitoid D. isaea, and larvae dead from unknown causes, were all recorded. All live larvae of L. trifolii were isolated in Petri dishes in the laboratory under ambient laboratory conditions (24 ± 2°C, 55–65 RH) until emergence of either the fly or one of its larval–pupal endoparasitoids, O. pallipes or H. circulus. Pupation of L. trifolii was recorded as either successful or unsuccessful. The total numbers of live L. trifolii larvae, numbers of malformed pupae, numbers of emerged flies, percentages of larvae succumbing to unknown causes, and larval parasitism by each parasitoid species were all estimated for each week’s samples. Thus, the factor levels in the ANOVA were ‘parasitism’, ‘unknown mortality’, ‘malformed pupae’, and ‘failed emergence’. The contribution of each mortality factor to total fly mortality was estimated, and the various proportional mortalities were subjected to one-way ANOVA followed by Fisher’s LSD test (α = 0.05) to separate means. Construction of Life Tables The data from L. trifolii field samples were pooled for each fly generation during each growing season to construct partial, stage-specific, life tables. The following notation was used: x = the age classification; a0 = the initial number of larvae, ax = the number of individuals initially alive at age x; lx = the proportion alive at the start of each life stage, (ax divided by a0); dx = proportion dying during the age interval, obtained by subtracting lx + 1 from lx; and Sx = the survival rate during a stage. Apparent mortality (100qx), represents the amount of mortality occurring in each age class, and is equal to dx divided by the corresponding lx. Real mortality (100rx) is mortality relative to the original population at the beginning of the generation, and is calculated by dividing all dx values by lx at the start of the generation. The marginal attack rate (Mx) calculates the proportion of individuals killed by a single factor in a particular stage, assuming that particular factor was acting alone (Bellows et al. 1992). The marginal death rate becomes equal to apparent mortality if multiple mortality factors operate in sequence, without overlap, or if there is only one source of mortality that is significant. When different sources of mortality act together, and information is lacking about possible interactions between these mortality factors, the marginal death rate is calculated as: Mx = 1 − (1 − q)qx/q, where qx is the apparent mortality caused by factor x, and q is the stage mortality caused by all factors (Elkinton et al. 1992). Mortality factors (dxF) were categorized as parasitism (in cases where parasitoids were identified), unformed and malformed pupae (whenever these were recovered), and unknown mortality (all individuals dying or disappearing due to undetermined causes, whether biotic or abiotic) (Bonhof 2000). Life expectancy (ex) expresses the probability of living to age “x.” The average proportion alive (Lx) between age x and x + 1 is calculated as follows: Lx=lx+ lx+12 The number of individuals living to age ‘x’ or older (Tx) is: Tx=Lx+Lx+1+Lx+2........+Lx+n The mean additional life expectancy of individuals that survive to a particular age (ex) is: ex=Txlx Key Factor and Density Dependence Analyses Key factor (k-value) analysis was estimated for factors affecting the survival of L. trifolii larvae and pupae. Note that the total k-value does not encompass the entire life cycle, but rather represents the total K exerted only on the life stages analyzed. For this analysis, data were first transformed to natural logarithms. Then, individual sources of mortality (k), and total mortality (K) were calculated for each generation according to Varley and Gradwell (1960), where k = loge (number before mortality / number after mortality). The latter value then represents the fraction of individuals killed by that particular mortality factor. Key mortality factors are those that are primarily responsible for altering population density (Morris, 1959). Total mortality (K) in any generation is the sum of all k-values in the life table. A graphical approach to key factor analysis (Varley and Gradwell (1960) was then conducted to compare patterns of total mortality (total K = Σk) to individual k-values. A regression of individual k-values on total K then permits a quantitative evaluation of key factors (Podoler and Rogers 1975), the steepest regression slope indicating the most significant factor. Finally, the relative importance of all factors was assessed by iterative sequential elimination of each key factor as described by Smith (1973), which can help resolve the relative contributions of factors that may be obscured because of their correlation with the key factor. The k-value of the key factor was subtracted from K and regressions were calculated for the remaining factors in a process that continued stepwise until all factors were eliminated except for the last two remaining. Regressions of the individual k-values on the natural logarithms of the various life stage densities at the beginning of each generation facilitates detection of density dependence in the action of particular mortality factors, whereas estimations based on insect densities at the beginning of the prior generation allow for the detection of delayed density dependence. Ranged-major axis regression analysis was used to evaluate the strength of any density dependence, given the error associated with measurement of insect densities (Legendre 2001). Results Population and Mortality Factor Estimates Life stages of L. trifolii exhibited three peaks of abundance on broad bean plants in each season. These occurred during January, February, and March in the first year (2015/2016), and in January, February, and April in the second year (2016/2016). The highest numbers of larvae occurred at the end of the crop growth period, whereas both pupal and adult stages peaked at the beginning of plant development (Fig. 1). Fig. 1. View largeDownload slide Seasonal population trajectories of Liriomyza trifolii life stages on broad bean plants over two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Fig. 1. View largeDownload slide Seasonal population trajectories of Liriomyza trifolii life stages on broad bean plants over two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. The larval parasitoid D. isaea was the most abundant parasitoid species emerging from L. trifolii, whereas the numbers of the larval–pupal parasitoids, O. pallipes and H. circulus, were very low. Diglyphus isaea exhibited three peaks of abundance that were synchronized with those of L. trifolii larvae during both years of study. Populations of D. isaea were lowest in December and highest in April in both years (Fig. 2). Fig. 2. View largeDownload slide Seasonal abundance of hymenopterous parasitoids attacking larval stages of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Fig. 2. View largeDownload slide Seasonal abundance of hymenopterous parasitoids attacking larval stages of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Larval parasitism ranged from 8.2 to 47.0% during the first year, and from 18.0 to 38.1% in the second year. Pupal parasitism ranged from 2.6 to 12.9% in the first year, and from 3.6 to 10.7% in the second. Mortality caused by unknown factors in both larval and pupal stages ranged from 25.7 to 58.8% in the first year, and from 23.5 to 47.2% in the second year. The total number of L. trifolii larvae was inversely correlated with the number that died for unknown reasons. The total numbers of parasitized and dead larvae exhibited three peaks during each year of the study, the highest occurring during the final period of plant growth in both cases (Fig. 3). Fig. 3. View largeDownload slide Seasonal population mortalities of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Fig. 3. View largeDownload slide Seasonal population mortalities of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Unknown factors contributed the most to total L. trifolii mortality in both the first (41.2%) and second (39.1%) years. Parasitism ranked second, causing 36.2 and 35.6% mortality in years one and two, respectively, whereas failed pupation and pupal malformation caused 9.7 and 12.1%, respectively (Fig. 4). Analysis revealed that the differences among mortality factors were significant (F3,72 = 49.10; P < 0.001), and that unknown factors had a greater effect on mortality than did parasitoids. Fig. 4. View largeDownload slide Percentage contribution of various mortality factors to total population mortality of Liriomyza trifolii on broad bean plants during two growing seasons in Mansoura district, Egypt. Fig. 4. View largeDownload slide Percentage contribution of various mortality factors to total population mortality of Liriomyza trifolii on broad bean plants during two growing seasons in Mansoura district, Egypt. Life Tables and Demographic Parameters The larval stage experienced the highest mortality in every generation, and the total mortality of both larval and pupal stages increased across successive generations in both seasons. However, larval mortality was higher in the first season, causing survival rates to decline more in the first season than in the second (Tables 1 and 2). Life expectancy (ex) for the larval stage was 1.18, 0.93, 0.74, and 0.75 wk for the four generations (G1, G2, G3, and G4, respectively), in the first season, and 1.12, 1.05, 0.88, and 0.80 wk for G1, G2, G3, and G4, respectively, in the second season. Thus, larval life expectancy decreased as the number of generations increased during both seasons of study. The trend for pupal life expectancy was similar in the first season of study, but in the second season, pupae in G2 had greater life expectancy than those in G1 (Tables 1 and 2). Larval stages of L. trifolii experienced the greatest real generation mortality (100rx) in every generation in both seasons, and the total real generation mortality of both larval and pupal stages increased from G1 to G3 in both seasons (Table 3). Table 1. Partial life table demographic parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2015/2016 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — ax, number alive at each stage; lx, proportion entering each stage; dx, number dying in stage; sx, survival rate within a stage; qx, apparent mortality; mx, marginal mortality; Lx, no. of individuals alive between age x and x+1; Tx, total number of living individuals at age x and beyond (Tx); ex, life expectancy. View Large Table 1. Partial life table demographic parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2015/2016 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — ax, number alive at each stage; lx, proportion entering each stage; dx, number dying in stage; sx, survival rate within a stage; qx, apparent mortality; mx, marginal mortality; Lx, no. of individuals alive between age x and x+1; Tx, total number of living individuals at age x and beyond (Tx); ex, life expectancy. View Large Table 2. Partial life table parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2016/2017 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — ax = number alive at each stage; lx = proportion entering each stage; dx = number dying in stag/e; sx = survival rate within a stage; qx = apparent mortality; mx = marginal mortality; Lx = number of individuals alive between age x and x+1; Tx = total number of living individuals at age x and beyond (Tx); ex = life expectancy. View Large Table 2. Partial life table parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2016/2017 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — ax = number alive at each stage; lx = proportion entering each stage; dx = number dying in stag/e; sx = survival rate within a stage; qx = apparent mortality; mx = marginal mortality; Lx = number of individuals alive between age x and x+1; Tx = total number of living individuals at age x and beyond (Tx); ex = life expectancy. View Large Table 3. Real generational mortality (100rx) of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 View Large Table 3. Real generational mortality (100rx) of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 View Large Key Factor Analysis and Density Dependence The larval stage experienced the highest k-values with G3 suffering the highest mortality in the first season, and G4 in the second. Key mortality factors during the first, second, third, and fourth generations were unformed and malformed pupae (k4), unknown mortality (k3), D. isaea (k2), and unknown mortality (k3), respectively. Thus, key mortality factors varied among generations, but were similar between seasons (Table 4). Table 4. Summary of k-values obtained from the partial budgets of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 View Large Table 4. Summary of k-values obtained from the partial budgets of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 View Large Variation in generational mortality appeared to reflect larval mortality more closely than other factors (Fig. 5) and this inference appeared supported by key factor regression (Table 5). Mortality due to D. isaea and unknown larval mortality were the two highest key factors in both seasons, followed by unformed and malformed pupae, whereas parasitism by H. circulus was the lowest. Thus, key factors associated with the larval stage emerged as most important, although density dependence was not indicated for any mortality factors, and regression slopes, although significant, were shallow. Similarly, there was no indication that any mortality factor acted in a delayed density-dependent manner, except for unknown mortality of the larval stage during the first growing season that was inversely density dependent (slope = −0.13, P = 0.04). Fig. 5. View largeDownload slide Comparison of total K to individual k-values for each Liriomyza trifolii generation in each of two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Fig. 5. View largeDownload slide Comparison of total K to individual k-values for each Liriomyza trifolii generation in each of two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Table 5. Key factor analysis of Liriomyza trifolii mortality in broad bean plants over four generations during the 2015/2016 and 2016/2017 growing seasons, using the methods of Smith (1973), and Podoler and Rogers (1975) Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Values represent the slope of the regression of individual k-values on total K (ln of generational survival). The factor with the highest slope (key factor, in bold face) is eliminated in each subsequent step in order to estimate the relative effect of each factor on overall variation in generational survival. The top portion of each season examines all mortality factors pooled by stage; the bottom portion examines stage- and key-specific mortalities. View Large Table 5. Key factor analysis of Liriomyza trifolii mortality in broad bean plants over four generations during the 2015/2016 and 2016/2017 growing seasons, using the methods of Smith (1973), and Podoler and Rogers (1975) Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Values represent the slope of the regression of individual k-values on total K (ln of generational survival). The factor with the highest slope (key factor, in bold face) is eliminated in each subsequent step in order to estimate the relative effect of each factor on overall variation in generational survival. The top portion of each season examines all mortality factors pooled by stage; the bottom portion examines stage- and key-specific mortalities. View Large Discussion The L. trifolii population exhibited three peaks of abundance on broad bean plants, which occurred during January, February, and March–April in each season of the study, the largest population of larvae occurring in April. This appears typical for agromyzid leaf miners at this latitude. In Libya, L. bryoniae (Kaltenbach) recorded three to four peaks of abundance on various host plants, including broad bean (Albasha and Elkhouly 2014). In sub-tropical Florida, populations of L. trifolii peak during December–January (Li et al. 2012), whereas on the Indian subcontinent, they peak January–February (Hemalatha and Maheswari 2004, Galande and Ghorpade 2010, Variya and Bhut 2014). Diglyphus isaea was, by far, the most abundant parasitoid species emerging from L. trifolii infesting broad bean in this study, with O. pallipes and H. circulus occurring in very low abundance. Noyes (2004) listed more than 80 species of parasitoids attacking various stages of Liriomyza species, of which the genus Diglyphus constitutes a primary group. For example, D. isaea was the most widely distributed parasitoid of L. trifolii on onion in Luzon Province, Philippines, and the second highest in overall abundance (Arida 2013). Opius spp. have been reported as the most abundant parasitoid of L. trifolii on lettuce in Arizona (Palumbo et al. 1994). In contrast, the primary parasitoids attacking L. huidobrensis on onions in Hawaii were H. circulus and Chrysocharis parksi Crawford (Hymenoptera: Eulophidae), whereas Diglyphus begini (Ashmead) (Hymenoptera: Eulophidae) and Diglyphus intermedius (Girault) (Hymenoptera: Eulophidae) largely focused their activity on parasitizing L. trifolii on bordering bean plants (Johnson and Mau 1986). Similarly, Kemmochi et al. (2016) collected few H. circulus from L. trifolii in Japan and found that, although the parasitoid readily accepts L. trifolii as a host, larval hemocytes can encapsulate the parasitoid’s eggs or small larvae. The authors concluded that this parasitoid may control Liriomyza chinensis (Kato) (Diptera: Agromyzidae), but is unlikely to be useful against L. trifolii. There were three generations of D. isaea in both growing seasons, each achieving higher numbers than the previous one. Thus, its annual cycle of abundance followed that of its host population, being lowest in December and highest in April in both years. Elkhouly and Alhririg (2015) reported that D. isaea was effective in controlling L. trifolii in pesticide-free tomato greenhouses in Libya, with peak abundance of the parasitoid occurring in April. In the field, Elkhouly et al. (2015) found that D. isaea tracked L. trifolii across four different winter host plants in Libya, peaking in abundance on broad bean in December. Similarly, Palumbo et al. (1994) reported that populations of L. trifolii parasitoids, particularly D. isaea and Opius dissitus Muesebeck (Hymenoptera: Braconidae), showed seasonal fluctuations that mirrored those of their host; they were abundant when leaf miner density was high, and sparse when leaf miner density was low. Seasonal fluctuations of leaf miner parasitoids in Argentina appear to follow similar patterns, driven by cycles of host abundance (Valladares and Salvo 2001). Arida (2013) studied L. trifolii on onion in the Philippines and reported overall levels of parasitism similar to those we observed in this study; six parasitoid species contributed mortality, with D. isaea the most abundant. Parasitism of L. trifolii larvae and pupae was relatively high in this study compared with others (e.g., Bahlai et al. 2006), possibly because our estimates were based on living immature stages of parasitoids, rather than on numbers of emerged adults. Whereas some studies have reported Liriomyza parasitism exceeding 80% (Poe and Montz 1981, Asadi et al. 2006), L. trifolii parasitism averages 30% in Kenya (Foba et al. 2015) and can be less than 6% in South Africa (Chabi-Olaye et al. 2008). It is important to note that our estimates of D. isaea parasitism represent only a portion of the total mortality contributed by this wasp, as “unknown mortality” would have included hosts killed by parasitoid host-feeding, and hosts stung without oviposition (Liu et al. 2013, Akutse et al. 2015), likely contributing to high mortality in this category in both seasons. For example, both D. intermedius and D. begini may kill more hosts than they actually parasitize (Heinz and Parrella 1989, Patel et al. 2003). These parasitoid behaviors may have contributed to the observed synchrony between host density and unknown mortality. This category would also include any undetected mortality due to ants, predatory Hemiptera, and other generalist predators that, in other leaf miner systems, can inflict more mortality than parasitoids (e.g., Xiao et al. 2007, Xiao and Fadamiro 2010). This is one of very few stage-specific life table studies of L. trifolii to employ field data and separate mortality factors acting on larval and pupal stages. Key factor analysis is widely used as the first step in analyzing life table data, despite the conceptual difficulties outlined by Royama (1996), and this analysis provided inferences consistent with the life table data. Unknown mortality was identified as a key factor in larval stage L. trifolii mortality and both larval and pupal stages suffered significant mortality from parasitism and malformation, respectively. Comparisons among mortality factors acting on both stages of L. trifolii, using the methods of Smith (1973) and Podoler and Rogers (1975), revealed that parasitism by D. isaea had a bigger effect on larval survival than did malformation of pupae (Table 5). Larval L. trifolii mortality was closely associated with variation in generational mortality, both graphically and in regression analysis. The key factor regression method confirmed these stage-specific patterns. In both seasons, after removal of mortality factors during each developmental period, unknown larval stage mortality emerged as the key factor, followed by D. isaea larval parasitism. Similarly, life table analyses of the coffee leaf miner, Leucoptera coffeella (Guerin-Ménéville) (Lepidoptera: Lyonetiidae) in Chiapas, Mexico revealed that death by “factors other than predation and parasitism,” followed by parasitism, were the most important sources of apparent larval mortality (Refugio 2007). The lowest key factor acting on L. trifolii larvae was H. circulus during both seasons of study, possibly due to encapsulation of this species by the host (Kemmochi et al. 2016). Many studies fail to identify density-dependent processes acting on insect populations (Stiling 1988), but this does not necessarily mean that they are not present. Studies of only a few generations rarely detect density-dependent processes, as population regulation is more easily identified when studies span many generations (Hassell el al. 1989). There was a slight indication of delayed density dependence for unknown mortality during the first season of study, possibly due to host-feeding by female parasitoids (Patel et al. 2003, Liu et al. 2013, Akutse et al. 2015). Such host-induced mortality is difficult to quantify within the mines because leaflets are small and individual mines are narrow and may converge on one another. Density dependence between L. trifolii and its parasitoids was also weak in the study of Li et al. (2012). Nelson and Roitberg (1995) reported that the foraging behavior of the parasitoid, Opius dimidiatus (Ashmead) (Hymenoptera: Braconidae) on chrysanthemum became density dependent when L. trifolii mine density was high. Some authors have suggested that an aggregated host distribution increases parasitoid foraging efficiency, and can then lead to density dependent parasitism (e.g., Heads and Lawton 1983, Bayoumy 2011). Our results have some practical implications for management of L. trifolii in beans. Management programs should develop tactics aimed at reducing the survival of larval and pupal stages in winter when pest abundance is high, as these stages already suffer the most natural mortality. Conservation biological control tactics should be considered, such as the improvement of surrounding habitat with floral resources for key natural enemies, given the importance of naturally occurring parasitoids (Fragoso et al. 2001). In particular, the conservation of Diglyphus parasitoids should be a priority when making decisions to control other pests; the use of broad-spectrum insecticides should be avoided in favor of more selective compounds. 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A Life Table for Liriomyza trifolii (Diptera: Agromyzidae) in a Temperate Zone of Northeast Egypt With Key Factor Analysis

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Entomological Society of America
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© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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0046-225X
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1938-2936
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10.1093/ee/nvy086
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Abstract

Abstract The American serpentine leaf miner, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae), is a perennial pest of leguminous crops in the Mediterranean region. A life table was constructed for L. trifolii infesting broad bean, Vicia faba L., in northern Egypt. Key factor analysis was used to rank sources of immature mortality over two seasons. Leaf miners had three successive generations, and a partial fourth, in each year, with peak abundance in March–April. Less than 15 and 22% of L. trifolii survived to adult in seasons one and two, respectively. The largest contributor of immature leaf miner mortality in both seasons was unknown (41.2 and 39.1% of total mortality, respectively), and likely comprised a combination of abiotic factors, parasitoid-inflicted mortality (host-feeding), and predation. Parasitism was second, contributing 36.2 and 35.6% of total mortality in the two seasons, respectively, primarily due to larval parasitism by Diglyphus isaea (Walker) (Hymenoptera: Eulophidae), and low levels of larval–pupal parasitism by Opius pallipes Wesmael (Hymenoptera: Braconidae) and Halticoptera circulus (Walker) (Hymenoptera: Pteromalidae). Residual mortality resulted from malformed pupae or failed adult emergence. Key factor analysis revealed malformation to be the major cause of pupal mortality. Sequential regression confirmed that unknown mortality and D. isaea were the top stage-specific factors, both acting on larvae. Parasitoid abundance tracked host abundance across generations, but density dependence was not observed for any mortality factor, and the magnitudes of regression slopes were small. The results indicate the potential importance of conservation biological control in management of L. trifolii, given that naturally occurring parasitoids and other biotic/abiotic factors exert significant mortality on immature leaf miners. Diglyphus isaea, Halticoptera circulus, mortality, Opius pallipes, Vicia faba Flies of the genus Liriomyza (Diptera: Agromyzidae) are leaf miners and cosmopolitan pests of various vegetable and horticultural crops (Chabi-Olaye et al. 2008). The genus includes more than 300 species worldwide, with 23 considered to be economically important pests (Wei et al. 2006, Kang et al. 2009). The American serpentine leaf miner, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae), feeds on a wide range of plants and is a key pest of vegetable crops worldwide (e.g., Kang et al. 2009, Hernández et al. 2011), including in Egypt (Metwally 1991, El-Serwy 1993, Ibrahim 1995). It is highly adaptable and has spread through both temperate and tropical regions, becoming increasingly difficult to control (Supartha et al. 2005, Gao et al. 2011). Heavy infestations of L. trifolii have resulted in the closure of flower farms, the loss of jobs, and the loss of overseas markets due to quarantine restrictions (Spencer 1985, IPPC 2005). More than 150 species of parasitoids have been recorded attacking various life stages of Liriomyza species (Waterhouse and Norris 1987, Murphy and LaSalle 1999, Claudio and Welter 2001), of which the genus Diglyphus (Hymenoptera: Eulophidae) is one of the most important groups (Liu et al. 2009, Mujica and Kroschel 2011). A survey of hymenopterous parasitoids attacking Liriomyza spp. in Egypt identified 12 species (Metwally 1991), the dominant ones being Opius pallipes Wesmael (Hymenoptera: Braconidae), Halticoptera circulus (Walker) (Hymenoptera: Pteromalidae), and Diglyphus isaea (Walker) (Hymenoptera: Eulophidae) (El-Serwy 1993, Ibrahim 1995). Opius pallipes is a solitary larval–pupal endoparasitoid of both L. trifolii and Liriomyza bryoniae (Kaltenbach) (Diptera: Agromyzidae), although it prefers the former species (Elkhouly et al. 2017). Parasitism of L. trifolii by O. pallipes in Egypt is low early in the season, and peaks during March (Saleh et al. 1983). This species has been successfully established in Dutch greenhouses where, in combination with Dacnusa sibirica Telenga (Hymenoptera: Braconidae), it maintains L. trifolii populations at very low levels and inflicts up to 100% parasitism (Yu et al. 2004). Halticoptera circulus is a larval–pupal endoparasitoid that has been successfully introduced and established throughout North America, including Hawaii (Johnson and Hara 1987, Schuster et al. 1991). Diglyphus isaea is a solitary ectoparasitoid of agromyzid leaf miner larvae, including those of the pea leaf miner, Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae), the vegetable leaf miner, Liriomyza sativae Blanchard (Diptera: Agromyzidae), as well as L. trifolii (Ode and Heinz 2002, Liu et al. 2009). It has been recorded attacking Liriomyza species on vegetable crops and ornamental plants in the United States, Europe, Asia, and some parts of Africa (Ode and Heinz 2002, Liu et al. 2009, Musundire et al. 2012). Ozawa et al. (2001) found D. isaea to be the dominant parasitoid of L. trifolii larvae on tomato in Japan, where it is now effectively used in augmentation biological control in greenhouses. In a greenhouse survey in southern Portugal, Goncalves and Almeida (2005) reported that two ectoparasitoids, Diglyphus poppoea Walker (Hymenoptera: Eulophidae) and D. isaea, achieved up to parasitism of 80–85% of Liriomyza spp. However, the role of parasitoids in naturally controlling L. trifolii in Egypt has been largely neglected, even though knowledge of the contribution of parasitism to pest mortality could provide valuable insights to aid the development of management strategies and tailor them to local conditions. Despite the importance of L. trifolii as a pest of legume production in Egypt, local information is lacking on its population dynamics and parasitism levels. Estimates of leaf miner population cycles are required to assess the current status of the pest in Egypt and knowledge of its patterns of seasonal abundance would be useful to focus management efforts. Rapid increases in leaf miner populations can result from insecticide applications that disrupt natural biological control (Saito et al. 1996), and management can be complicated by the evolution of insecticide resistance in fly populations (Hofsvang et al. 2005). Egyptian agriculture could benefit from biological control programs that utilize locally effective parasitoid species, similar to those that have been established in other countries (Murphy and La Salle 1999, Chow and Heinz 2004). Quantitative information on key sources of natural pest mortality can be useful for improving the efficacy of augmentation or conservation biological control in integrated pest management programs. Life tables provide one method for partitioning mortality among life stages in insect populations (Morris and Miller 1954). From an ecological perspective, life tables provide valuable insights into intrinsic vulnerabilities in pest life history, in addition to detailed information on pest population dynamics. Life tables provide a comprehensive analysis of survivorship and life expectancy (Ali and Rizvi 2007; Yzdani and Samih 2012) as well as a means of partitioning the relative contributions of various mortality factors to pest population suppression (Bellows et al. 1992; Mohapatra 2007). The objective of this study was to construct a stage-specific life table for L. trifolii (sensuSouthwood 1978) that would enable: 1) characterization of the population dynamics of L. trifolii on broad bean over two successive growing seasons in northern Egypt, 2) calculation of the percentage of larvae parasitized, and 3) determination of parasitism’s relative contribution to total mortality of the pest. Materials and Methods Sampling This study was carried out at the experimental farm of the Faculty of Agriculture, Mansoura University during two successive seasons (2015/2016 and 2016/2017). A cultivated area of 200 m2 was divided into four equal plots. Broad bean, Vicia faba L., cv Giza 843, was planted in all during the third week of November in the first year, and in the last week of November in the second year. Recommended agricultural practices were followed in managing the field and no insecticide applications were made. Beginning 3 wk after planting, samples of broad bean leaflets were taken weekly until the end of the season (harvest). Each sample consisted of 100 leaflets (25 leaflets from each quarter of the field), collected randomly from different plant heights. The samples were collected in plastic bags and transferred to the laboratory for examination under a binocular microscope (Optika ST-40B-2L). The numbers of living leaf miner larvae, larvae parasitized by the ectoparasitoid D. isaea, and larvae dead from unknown causes, were all recorded. All live larvae of L. trifolii were isolated in Petri dishes in the laboratory under ambient laboratory conditions (24 ± 2°C, 55–65 RH) until emergence of either the fly or one of its larval–pupal endoparasitoids, O. pallipes or H. circulus. Pupation of L. trifolii was recorded as either successful or unsuccessful. The total numbers of live L. trifolii larvae, numbers of malformed pupae, numbers of emerged flies, percentages of larvae succumbing to unknown causes, and larval parasitism by each parasitoid species were all estimated for each week’s samples. Thus, the factor levels in the ANOVA were ‘parasitism’, ‘unknown mortality’, ‘malformed pupae’, and ‘failed emergence’. The contribution of each mortality factor to total fly mortality was estimated, and the various proportional mortalities were subjected to one-way ANOVA followed by Fisher’s LSD test (α = 0.05) to separate means. Construction of Life Tables The data from L. trifolii field samples were pooled for each fly generation during each growing season to construct partial, stage-specific, life tables. The following notation was used: x = the age classification; a0 = the initial number of larvae, ax = the number of individuals initially alive at age x; lx = the proportion alive at the start of each life stage, (ax divided by a0); dx = proportion dying during the age interval, obtained by subtracting lx + 1 from lx; and Sx = the survival rate during a stage. Apparent mortality (100qx), represents the amount of mortality occurring in each age class, and is equal to dx divided by the corresponding lx. Real mortality (100rx) is mortality relative to the original population at the beginning of the generation, and is calculated by dividing all dx values by lx at the start of the generation. The marginal attack rate (Mx) calculates the proportion of individuals killed by a single factor in a particular stage, assuming that particular factor was acting alone (Bellows et al. 1992). The marginal death rate becomes equal to apparent mortality if multiple mortality factors operate in sequence, without overlap, or if there is only one source of mortality that is significant. When different sources of mortality act together, and information is lacking about possible interactions between these mortality factors, the marginal death rate is calculated as: Mx = 1 − (1 − q)qx/q, where qx is the apparent mortality caused by factor x, and q is the stage mortality caused by all factors (Elkinton et al. 1992). Mortality factors (dxF) were categorized as parasitism (in cases where parasitoids were identified), unformed and malformed pupae (whenever these were recovered), and unknown mortality (all individuals dying or disappearing due to undetermined causes, whether biotic or abiotic) (Bonhof 2000). Life expectancy (ex) expresses the probability of living to age “x.” The average proportion alive (Lx) between age x and x + 1 is calculated as follows: Lx=lx+ lx+12 The number of individuals living to age ‘x’ or older (Tx) is: Tx=Lx+Lx+1+Lx+2........+Lx+n The mean additional life expectancy of individuals that survive to a particular age (ex) is: ex=Txlx Key Factor and Density Dependence Analyses Key factor (k-value) analysis was estimated for factors affecting the survival of L. trifolii larvae and pupae. Note that the total k-value does not encompass the entire life cycle, but rather represents the total K exerted only on the life stages analyzed. For this analysis, data were first transformed to natural logarithms. Then, individual sources of mortality (k), and total mortality (K) were calculated for each generation according to Varley and Gradwell (1960), where k = loge (number before mortality / number after mortality). The latter value then represents the fraction of individuals killed by that particular mortality factor. Key mortality factors are those that are primarily responsible for altering population density (Morris, 1959). Total mortality (K) in any generation is the sum of all k-values in the life table. A graphical approach to key factor analysis (Varley and Gradwell (1960) was then conducted to compare patterns of total mortality (total K = Σk) to individual k-values. A regression of individual k-values on total K then permits a quantitative evaluation of key factors (Podoler and Rogers 1975), the steepest regression slope indicating the most significant factor. Finally, the relative importance of all factors was assessed by iterative sequential elimination of each key factor as described by Smith (1973), which can help resolve the relative contributions of factors that may be obscured because of their correlation with the key factor. The k-value of the key factor was subtracted from K and regressions were calculated for the remaining factors in a process that continued stepwise until all factors were eliminated except for the last two remaining. Regressions of the individual k-values on the natural logarithms of the various life stage densities at the beginning of each generation facilitates detection of density dependence in the action of particular mortality factors, whereas estimations based on insect densities at the beginning of the prior generation allow for the detection of delayed density dependence. Ranged-major axis regression analysis was used to evaluate the strength of any density dependence, given the error associated with measurement of insect densities (Legendre 2001). Results Population and Mortality Factor Estimates Life stages of L. trifolii exhibited three peaks of abundance on broad bean plants in each season. These occurred during January, February, and March in the first year (2015/2016), and in January, February, and April in the second year (2016/2016). The highest numbers of larvae occurred at the end of the crop growth period, whereas both pupal and adult stages peaked at the beginning of plant development (Fig. 1). Fig. 1. View largeDownload slide Seasonal population trajectories of Liriomyza trifolii life stages on broad bean plants over two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Fig. 1. View largeDownload slide Seasonal population trajectories of Liriomyza trifolii life stages on broad bean plants over two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. The larval parasitoid D. isaea was the most abundant parasitoid species emerging from L. trifolii, whereas the numbers of the larval–pupal parasitoids, O. pallipes and H. circulus, were very low. Diglyphus isaea exhibited three peaks of abundance that were synchronized with those of L. trifolii larvae during both years of study. Populations of D. isaea were lowest in December and highest in April in both years (Fig. 2). Fig. 2. View largeDownload slide Seasonal abundance of hymenopterous parasitoids attacking larval stages of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Fig. 2. View largeDownload slide Seasonal abundance of hymenopterous parasitoids attacking larval stages of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Larval parasitism ranged from 8.2 to 47.0% during the first year, and from 18.0 to 38.1% in the second year. Pupal parasitism ranged from 2.6 to 12.9% in the first year, and from 3.6 to 10.7% in the second. Mortality caused by unknown factors in both larval and pupal stages ranged from 25.7 to 58.8% in the first year, and from 23.5 to 47.2% in the second year. The total number of L. trifolii larvae was inversely correlated with the number that died for unknown reasons. The total numbers of parasitized and dead larvae exhibited three peaks during each year of the study, the highest occurring during the final period of plant growth in both cases (Fig. 3). Fig. 3. View largeDownload slide Seasonal population mortalities of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Fig. 3. View largeDownload slide Seasonal population mortalities of Liriomyza trifolii on broad bean plants during two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura district, Egypt. Unknown factors contributed the most to total L. trifolii mortality in both the first (41.2%) and second (39.1%) years. Parasitism ranked second, causing 36.2 and 35.6% mortality in years one and two, respectively, whereas failed pupation and pupal malformation caused 9.7 and 12.1%, respectively (Fig. 4). Analysis revealed that the differences among mortality factors were significant (F3,72 = 49.10; P < 0.001), and that unknown factors had a greater effect on mortality than did parasitoids. Fig. 4. View largeDownload slide Percentage contribution of various mortality factors to total population mortality of Liriomyza trifolii on broad bean plants during two growing seasons in Mansoura district, Egypt. Fig. 4. View largeDownload slide Percentage contribution of various mortality factors to total population mortality of Liriomyza trifolii on broad bean plants during two growing seasons in Mansoura district, Egypt. Life Tables and Demographic Parameters The larval stage experienced the highest mortality in every generation, and the total mortality of both larval and pupal stages increased across successive generations in both seasons. However, larval mortality was higher in the first season, causing survival rates to decline more in the first season than in the second (Tables 1 and 2). Life expectancy (ex) for the larval stage was 1.18, 0.93, 0.74, and 0.75 wk for the four generations (G1, G2, G3, and G4, respectively), in the first season, and 1.12, 1.05, 0.88, and 0.80 wk for G1, G2, G3, and G4, respectively, in the second season. Thus, larval life expectancy decreased as the number of generations increased during both seasons of study. The trend for pupal life expectancy was similar in the first season of study, but in the second season, pupae in G2 had greater life expectancy than those in G1 (Tables 1 and 2). Larval stages of L. trifolii experienced the greatest real generation mortality (100rx) in every generation in both seasons, and the total real generation mortality of both larval and pupal stages increased from G1 to G3 in both seasons (Table 3). Table 1. Partial life table demographic parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2015/2016 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — ax, number alive at each stage; lx, proportion entering each stage; dx, number dying in stage; sx, survival rate within a stage; qx, apparent mortality; mx, marginal mortality; Lx, no. of individuals alive between age x and x+1; Tx, total number of living individuals at age x and beyond (Tx); ex, life expectancy. View Large Table 1. Partial life table demographic parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2015/2016 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larva 649 1.00 K2 Diglyphus isaea 123 18.95 81.05 18.9 18.9 16.28 0.77 1.18 1.18 K3 Unknown mortality 174 26.81 73.19 26.8 26.8 24.03 Total 297 45.76 54.24 45.70 45.8 47.29 Pupa 352 0.542 K4 Unformed and malformed pupae 103 15.87 84.13 29.28 29.3 26.36 0.41 0.41 0.76 K5a Opius palipes 35 5.39 94.61 9.94 9.90 7.75 K5b Halticoptera circulus 5 0.77 99.23 1.42 1.30 0.78 K6 Unknown mortality 30 4.62 95.38 8.52 8.50 6.98 Total 173 26.66 73.34 49.19 4.94 52.71 Adult 179 0.275 Total population mortality 470 72.42 27.58 — — 100.0 — — — G2 Larva 968 1 K2 Diglyphus isaea 314 32.43 67.57 32.43 3.24 22.66 0.67 0.93 0.93 K3 Unknown mortality 316 32.64 67.36 32.64 3.26 22.83 Total 630 65.08 34.92 65.08 6.51 60.69 Pupa 338 0.349 K4 Unformed and malformed pupae 84 8.68 91.32 24.87 2.49 8.67 0.26 0.26 0.74 K5a Opius palipes 34 3.51 96.49 10.06 1.00 6.36 K5b Halticoptera circulus 21 2.17 97.83 6.22 6.30 3.47 K6 Unknown mortality 28 2.89 97.11 8.28 8.30 5.20 Total 167 17.25 82.75 49.43 4.96 39.31 Adult 171 0.177 Total population mortality 797 82.33 17.67 — — 100.0 — — — G3 Larval 1233 1.00 K2 Diglyphus isaea 540 43.79 56.21 43.79 4.38 22.39 0.6 0.74 0.74 K3 Unknown mortality 450 36.49 63.51 36.49 3.65 17.37 Total 990 80.29 19.71 80.29 8.03 62.55 Pupal 243 0.197 K4 Unformed and malformed pupae 74 6.00 94.00 30.46 3.05 13.89 0.14 0.14 0.71 K5a Opius palipes 42 3.41 96.59 17.30 17.30 7.34 K5b Halticoptera circulus 20 1.62 98.38 8.22 8.10 3.47 K6 Unknown mortality 15 1.22 98.78 6.19 6.10 2.70 Total 151 12.25 87.75 62.18 6.19 30.50 Adult 92 0.075 Total population mortality 1141 92.54 7.46 — — 100.0 — — — Partial G4 Larval 347 1.00 K2 Diglyphus isaea 121 34.87 65.13 34.87 3.49 17.34 0.6 0.75 0.75 K3 Unknown mortality 153 44.09 55.91 44.09 4.41 23.39 Total 274 78.96 21.04 78.96 7.89 50.00 Pupal 73 0.21 K4 Unformed and malformed pupae 28 8.07 91.93 38.42 3.86 19.35 0.15 0.15 0.71 K5a Opius palipes 9 2.59 97.41 12.33 1.24 5.24 K5b Halticoptera circulus 3 0.86 99.14 4.09 4.30 1.61 K6 Unknown mortality 4 1.15 98.85 5.48 5.70 2.42 Total 44 12.68 87.32 60.38 6.05 37.09 Adult 29 0.084 Total population mortality 318 91.64 8.36 --- 91.64 100.0 — — — ax, number alive at each stage; lx, proportion entering each stage; dx, number dying in stage; sx, survival rate within a stage; qx, apparent mortality; mx, marginal mortality; Lx, no. of individuals alive between age x and x+1; Tx, total number of living individuals at age x and beyond (Tx); ex, life expectancy. View Large Table 2. Partial life table parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2016/2017 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — ax = number alive at each stage; lx = proportion entering each stage; dx = number dying in stag/e; sx = survival rate within a stage; qx = apparent mortality; mx = marginal mortality; Lx = number of individuals alive between age x and x+1; Tx = total number of living individuals at age x and beyond (Tx); ex = life expectancy. View Large Table 2. Partial life table parameters and life expectancy for Liriomyza trifolii populations on broad bean plants during the 2016/2017 growing season in Mansoura, Egypt Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — Generation Stage (x) ax lx Mortality factors (dxF) dx dx (%) Sx 100qx Mx Generational mortality (%) Lx Tx ex G1 Larval 258 1.00 K2 Diglyphus isaea 46 17.80 82.20 17.80 17.80 20.21 0.81 1.12 1.12 K3 Unknown mortality 51 19.80 80.20 19.80 19.80 22.68 Total 97 37.60 62.40 37.60 37.60 48.45 Pupal 161 0.62 K4 Unformed and malformed pupae 32 12.40 87.60 20.00 20.00 22.68 0.50 0.50 0.81 K5a Opius palipes 13 5.00 95.00 8.06 8.50 8.25 K5b Halticoptera circulus 0 0.00 100.0 0.00 0.00 0.00 K6 Unknown mortality 18 6.90 93.10 11.13 11.10 12.37 Total 63 24.40 75.60 39.35 39.40 50.51 Adult 98 0.38 Total population mortality 160 62.20 37.80 — — 100.0 — — — G2 Larval 519 1.00 K2 Diglyphus isaea 153 29.50 70.50 29.50 29.50 26.64 0.71 1.05 1.05 K3 Unknown mortality 152 29.30 70.70 29.30 29.30 26.41 Total 305 58.80 41.20 58.80 58.80 67.94 Pupal 214 0.41 K4 Unformed and malformed pupae 43 8.30 91.70 20.24 20.20 16.79 0.34 0.34 0.83 K5a Opius palipes 13 2.50 97.50 6.09 6.10 4.58 K5b Halticoptera circulus 7 1.30 98.70 3.17 3.20 2.29 K6 Unknown mortality 11 2.10 97.90 5.12 5.10 3.82 Total 74 14.30 85.70 34.87 34.90 32.06 Adult 140 0.27 Total population mortality 379 73.30 26.70 — — 100.0 — — — G3 Larval 1244 1 K2 Diglyphus isaea 457 36.70 63.30 36.70 36.70 22.77 0.65 0.88 0.88 K3 Unknown mortality 390 31.40 68.60 31.40 31.40 18.81 Total 847 68.10 31.90 68.10 68.10 56.44 Pupal 397 0.32 K4 Unformed and malformed pupae 85 6.80 93.20 21.25 21.30 11.88 0.23 0.23 0.72 K5a Opius palipes 90 7.20 92.80 22.50 22.50 12.87 K5b Halticoptera circulus 28 2.30 97.70 7.19 7.20 3.46 K6 Unknown mortality 30 2.40 97.60 7.50 7.50 3.96 Total 233 18.70 81.30 58.44 58.40 4.36 Adult 164 0.13 Total population mortality 1080 86.80 13.20 — — 100.0 — — — Partial G4 Larval 355 1.00 K2 Diglyphus isaea 122 34.40 65.60 34.40 34.40 18.10 0.63 0.80 0.80 K3 Unknown mortality 143 40.30 59.70 40.30 40.30 22.41 Total 265 74.60 25.40 74.60 74.60 59.05 Pupal 90 0.25 K4 Unformed and malformed pupae 19 5.40 94.60 21.60 21.60 10.34 0.17 0.17 0.68 K5a Opius palipes 17 4.80 95.20 19.20 19.20 9.05 K5b Halticoptera circulus 10 2.80 97.20 11.20 11.20 5.17 K6 Unknown mortality 9 2.50 97.50 10.00 10.00 4.74 Total 55 15.50 84.50 62.00 62.00 40.52 Adult 35 0.09 Total population mortality 320 90.10 9.90 — — 100.0 — — — ax = number alive at each stage; lx = proportion entering each stage; dx = number dying in stag/e; sx = survival rate within a stage; qx = apparent mortality; mx = marginal mortality; Lx = number of individuals alive between age x and x+1; Tx = total number of living individuals at age x and beyond (Tx); ex = life expectancy. View Large Table 3. Real generational mortality (100rx) of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 View Large Table 3. Real generational mortality (100rx) of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 Season Generation Life stage 1 2 3 Partial 4 Mean SE 2015/2016 Larvae 45.70 65.08 80.29 78.96 67.51 8.04 Pupae 26.66 17.25 12.25 12.68 17.21 3.35 Total 72.36 82.33 92.54 91.64 84.72 4.72 2016/2017 Larvae 37.60 58.80 68.10 74.60 59.78 8.07 Pupae 24.40 14.30 18.70 15.50 18.23 2.26 Total 62.00 73.30 86.80 90.10 78.05 6.47 View Large Key Factor Analysis and Density Dependence The larval stage experienced the highest k-values with G3 suffering the highest mortality in the first season, and G4 in the second. Key mortality factors during the first, second, third, and fourth generations were unformed and malformed pupae (k4), unknown mortality (k3), D. isaea (k2), and unknown mortality (k3), respectively. Thus, key mortality factors varied among generations, but were similar between seasons (Table 4). Table 4. Summary of k-values obtained from the partial budgets of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 View Large Table 4. Summary of k-values obtained from the partial budgets of Liriomyza trifolii on broad bean plants during the 2015/2016 and 2016/2017 growing seasons in Mansoura, Egypt Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 Generation Season Life stage Mortality factor 1 2 3 Partial 4 2015/2016 Larvae K2Diglyphu isaea 0.21 0.39 0.58 0.43 K3 Unknown mortality 0.31 0.40 0.45 0.58 Total K within stage 0.61 1.05 1.62 1.56 Pupae K4 Unformed and malformed pupae 0.35 0.29 0.36 0.48 K5aOpius pallipes 0.10 0.11 0.19 0.13 K5bHalticoptera circulus 0.01 0.06 0.09 0.04 K6 Unknown mortality 0.09 0.09 0.06 0.06 Total K within stage 0.68 0.68 0.97 0.92 Total generation K 1.73 1.73 2.59 2.48 2016/2017 Larval K2Diglyphu isaea 0.19 0.35 0.46 0.42 K3 Unknown mortality 0.22 0.35 0.38 0.52 Total K within stage 0.47 0.89 1.14 1.37 Pupal K4 Unformed and malformed pupae 0.22 0.22 0.24 0.24 K5aOpius palipes 0.08 0.06 0.26 0.21 K5bHalticoptera circulus 0 0.03 0.07 0.12 K6 Unknown mortality 0.12 0.05 0.08 0.11 Total K within stage 0.49 0.42 0.88 0.94 Total generation K 0.97 1.31 2.02 2.32 View Large Variation in generational mortality appeared to reflect larval mortality more closely than other factors (Fig. 5) and this inference appeared supported by key factor regression (Table 5). Mortality due to D. isaea and unknown larval mortality were the two highest key factors in both seasons, followed by unformed and malformed pupae, whereas parasitism by H. circulus was the lowest. Thus, key factors associated with the larval stage emerged as most important, although density dependence was not indicated for any mortality factors, and regression slopes, although significant, were shallow. Similarly, there was no indication that any mortality factor acted in a delayed density-dependent manner, except for unknown mortality of the larval stage during the first growing season that was inversely density dependent (slope = −0.13, P = 0.04). Fig. 5. View largeDownload slide Comparison of total K to individual k-values for each Liriomyza trifolii generation in each of two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Fig. 5. View largeDownload slide Comparison of total K to individual k-values for each Liriomyza trifolii generation in each of two growing seasons (A, 2015/2016; B, 2016/2017) in Mansoura, Egypt. Table 5. Key factor analysis of Liriomyza trifolii mortality in broad bean plants over four generations during the 2015/2016 and 2016/2017 growing seasons, using the methods of Smith (1973), and Podoler and Rogers (1975) Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Values represent the slope of the regression of individual k-values on total K (ln of generational survival). The factor with the highest slope (key factor, in bold face) is eliminated in each subsequent step in order to estimate the relative effect of each factor on overall variation in generational survival. The top portion of each season examines all mortality factors pooled by stage; the bottom portion examines stage- and key-specific mortalities. View Large Table 5. Key factor analysis of Liriomyza trifolii mortality in broad bean plants over four generations during the 2015/2016 and 2016/2017 growing seasons, using the methods of Smith (1973), and Podoler and Rogers (1975) Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Season Life stage / Mortality factor Step 1 2 3 4 5 2015/2016 Larvae 0.940 Pupae 0.330 Larvae   K2Diglyphus isaea  K3 Unknown mortality 0.186 0.627 0.265 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.113 0.513 0.58 0.072 0.021 0.17 0.48 0.96 0.041 −0.083 −0.08 −0.14 −0.16 0.037 0.018 0.22 0.66 2016/2017 Larvae 0.600 Pupae 0.400 Larvae  K2Diglyphus isaea  K3 Unknown mortality 0.169 0.850 0.183 Pupae  K4 Unformed and malformed pupae  K5aOpius pallipes  K5bHalticoptera circulus  K6 Unknown mortality 0.018 0.162 0.397 0.137 0.271 0.291 0.496 0.082 0.140 0.137 −0.015 −0.02 0.002 0.110 0.359 0.351 0.60 Values represent the slope of the regression of individual k-values on total K (ln of generational survival). The factor with the highest slope (key factor, in bold face) is eliminated in each subsequent step in order to estimate the relative effect of each factor on overall variation in generational survival. The top portion of each season examines all mortality factors pooled by stage; the bottom portion examines stage- and key-specific mortalities. View Large Discussion The L. trifolii population exhibited three peaks of abundance on broad bean plants, which occurred during January, February, and March–April in each season of the study, the largest population of larvae occurring in April. This appears typical for agromyzid leaf miners at this latitude. In Libya, L. bryoniae (Kaltenbach) recorded three to four peaks of abundance on various host plants, including broad bean (Albasha and Elkhouly 2014). In sub-tropical Florida, populations of L. trifolii peak during December–January (Li et al. 2012), whereas on the Indian subcontinent, they peak January–February (Hemalatha and Maheswari 2004, Galande and Ghorpade 2010, Variya and Bhut 2014). Diglyphus isaea was, by far, the most abundant parasitoid species emerging from L. trifolii infesting broad bean in this study, with O. pallipes and H. circulus occurring in very low abundance. Noyes (2004) listed more than 80 species of parasitoids attacking various stages of Liriomyza species, of which the genus Diglyphus constitutes a primary group. For example, D. isaea was the most widely distributed parasitoid of L. trifolii on onion in Luzon Province, Philippines, and the second highest in overall abundance (Arida 2013). Opius spp. have been reported as the most abundant parasitoid of L. trifolii on lettuce in Arizona (Palumbo et al. 1994). In contrast, the primary parasitoids attacking L. huidobrensis on onions in Hawaii were H. circulus and Chrysocharis parksi Crawford (Hymenoptera: Eulophidae), whereas Diglyphus begini (Ashmead) (Hymenoptera: Eulophidae) and Diglyphus intermedius (Girault) (Hymenoptera: Eulophidae) largely focused their activity on parasitizing L. trifolii on bordering bean plants (Johnson and Mau 1986). Similarly, Kemmochi et al. (2016) collected few H. circulus from L. trifolii in Japan and found that, although the parasitoid readily accepts L. trifolii as a host, larval hemocytes can encapsulate the parasitoid’s eggs or small larvae. The authors concluded that this parasitoid may control Liriomyza chinensis (Kato) (Diptera: Agromyzidae), but is unlikely to be useful against L. trifolii. There were three generations of D. isaea in both growing seasons, each achieving higher numbers than the previous one. Thus, its annual cycle of abundance followed that of its host population, being lowest in December and highest in April in both years. Elkhouly and Alhririg (2015) reported that D. isaea was effective in controlling L. trifolii in pesticide-free tomato greenhouses in Libya, with peak abundance of the parasitoid occurring in April. In the field, Elkhouly et al. (2015) found that D. isaea tracked L. trifolii across four different winter host plants in Libya, peaking in abundance on broad bean in December. Similarly, Palumbo et al. (1994) reported that populations of L. trifolii parasitoids, particularly D. isaea and Opius dissitus Muesebeck (Hymenoptera: Braconidae), showed seasonal fluctuations that mirrored those of their host; they were abundant when leaf miner density was high, and sparse when leaf miner density was low. Seasonal fluctuations of leaf miner parasitoids in Argentina appear to follow similar patterns, driven by cycles of host abundance (Valladares and Salvo 2001). Arida (2013) studied L. trifolii on onion in the Philippines and reported overall levels of parasitism similar to those we observed in this study; six parasitoid species contributed mortality, with D. isaea the most abundant. Parasitism of L. trifolii larvae and pupae was relatively high in this study compared with others (e.g., Bahlai et al. 2006), possibly because our estimates were based on living immature stages of parasitoids, rather than on numbers of emerged adults. Whereas some studies have reported Liriomyza parasitism exceeding 80% (Poe and Montz 1981, Asadi et al. 2006), L. trifolii parasitism averages 30% in Kenya (Foba et al. 2015) and can be less than 6% in South Africa (Chabi-Olaye et al. 2008). It is important to note that our estimates of D. isaea parasitism represent only a portion of the total mortality contributed by this wasp, as “unknown mortality” would have included hosts killed by parasitoid host-feeding, and hosts stung without oviposition (Liu et al. 2013, Akutse et al. 2015), likely contributing to high mortality in this category in both seasons. For example, both D. intermedius and D. begini may kill more hosts than they actually parasitize (Heinz and Parrella 1989, Patel et al. 2003). These parasitoid behaviors may have contributed to the observed synchrony between host density and unknown mortality. This category would also include any undetected mortality due to ants, predatory Hemiptera, and other generalist predators that, in other leaf miner systems, can inflict more mortality than parasitoids (e.g., Xiao et al. 2007, Xiao and Fadamiro 2010). This is one of very few stage-specific life table studies of L. trifolii to employ field data and separate mortality factors acting on larval and pupal stages. Key factor analysis is widely used as the first step in analyzing life table data, despite the conceptual difficulties outlined by Royama (1996), and this analysis provided inferences consistent with the life table data. Unknown mortality was identified as a key factor in larval stage L. trifolii mortality and both larval and pupal stages suffered significant mortality from parasitism and malformation, respectively. Comparisons among mortality factors acting on both stages of L. trifolii, using the methods of Smith (1973) and Podoler and Rogers (1975), revealed that parasitism by D. isaea had a bigger effect on larval survival than did malformation of pupae (Table 5). Larval L. trifolii mortality was closely associated with variation in generational mortality, both graphically and in regression analysis. The key factor regression method confirmed these stage-specific patterns. In both seasons, after removal of mortality factors during each developmental period, unknown larval stage mortality emerged as the key factor, followed by D. isaea larval parasitism. Similarly, life table analyses of the coffee leaf miner, Leucoptera coffeella (Guerin-Ménéville) (Lepidoptera: Lyonetiidae) in Chiapas, Mexico revealed that death by “factors other than predation and parasitism,” followed by parasitism, were the most important sources of apparent larval mortality (Refugio 2007). The lowest key factor acting on L. trifolii larvae was H. circulus during both seasons of study, possibly due to encapsulation of this species by the host (Kemmochi et al. 2016). Many studies fail to identify density-dependent processes acting on insect populations (Stiling 1988), but this does not necessarily mean that they are not present. Studies of only a few generations rarely detect density-dependent processes, as population regulation is more easily identified when studies span many generations (Hassell el al. 1989). There was a slight indication of delayed density dependence for unknown mortality during the first season of study, possibly due to host-feeding by female parasitoids (Patel et al. 2003, Liu et al. 2013, Akutse et al. 2015). Such host-induced mortality is difficult to quantify within the mines because leaflets are small and individual mines are narrow and may converge on one another. Density dependence between L. trifolii and its parasitoids was also weak in the study of Li et al. (2012). Nelson and Roitberg (1995) reported that the foraging behavior of the parasitoid, Opius dimidiatus (Ashmead) (Hymenoptera: Braconidae) on chrysanthemum became density dependent when L. trifolii mine density was high. Some authors have suggested that an aggregated host distribution increases parasitoid foraging efficiency, and can then lead to density dependent parasitism (e.g., Heads and Lawton 1983, Bayoumy 2011). Our results have some practical implications for management of L. trifolii in beans. Management programs should develop tactics aimed at reducing the survival of larval and pupal stages in winter when pest abundance is high, as these stages already suffer the most natural mortality. Conservation biological control tactics should be considered, such as the improvement of surrounding habitat with floral resources for key natural enemies, given the importance of naturally occurring parasitoids (Fragoso et al. 2001). In particular, the conservation of Diglyphus parasitoids should be a priority when making decisions to control other pests; the use of broad-spectrum insecticides should be avoided in favor of more selective compounds. 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Environmental EntomologyOxford University Press

Published: Jun 7, 2018

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