Resistance to insect growth regulators and age-stage, two-sex life table in Musca domestica from different dairy facilities

Naeem Abbas; Abdulwahab M. Hafez

doi:10.1371/journal.pone.0248693

Abstract

Among the vectorial insect pests, the domestic house fly (Musca domestica L., Diptera: Muscidae) is a ubiquitous livestock pest with the ability to develop resistance and adapt to diverse climates. Successful management of the house fly in various locations requires information about its resistance development and life table features. The status of insect growth regulators resistance and life table features on the basis of age, stage, and two sexes of the house fly from five different geographical locations of Riyadh, Saudi Arabia: Dirab, Al-Masanie, Al-Washlah, Al-Uraija and Al-Muzahmiya were therefore investigated. The range of resistance levels were 3.77–8.03-fold for methoxyfenozide, 5.50–29.75 for pyriproxyfen, 0.59–2.91-fold for cyromazine, 9.33–28.67-fold for diflubenzuron, and 1.63–8.25-fold for triflumuron in five populations of house fly compared with the susceptible strain. Analysis of life history parameters—such as survival rate, larval duration, pupal duration, pre-female duration, pre-male duration, adult and total pre-oviposition periods, longevity of male, oviposition period, female ratio, and fecundity female^-1—revealed significant variations among the field populations. Additionally, demographic features—including the generation time, the finite and intrinsic rates of increase, doubling time, and net reproductive rate—varied significantly among the field populations. These results will be helpful in planning the management of the house fly in geographically isolated dairies in Saudi Arabia.

Citation: Abbas N, Hafez AM (2021) Resistance to insect growth regulators and age-stage, two-sex life table in Musca domestica from different dairy facilities. PLoS ONE 16(4): e0248693. https://doi.org/10.1371/journal.pone.0248693

Editor: Ahmed Ibrahim Hasaballah, Al-Azhar University, EGYPT

Received: October 6, 2020; Accepted: March 3, 2021; Published: April 8, 2021

Copyright: © 2021 Abbas, Hafez. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The authors extend their appreciation to the Deputyship for Research & Innovation, “Ministry of Education” in Saudi Arabia for funding this research work through the project number IFKSURG-1442-480. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Musca domestica L. (Diptera: Muscidae) is a ubiquitous insect pest of livestock and humans [1, 2] capable of adapting to a wide range of climates. This insect is commonly known as the house fly and serves as a carrier for many pathogens of public health and veterinary importance [3, 4]. Attempts to control the house fly with a wide range of insecticides have failed because this insect rapidly develops resistance to these chemicals [5–11]. This widespread development of insecticide resistance has necessitated the employment of integrated vector management strategies.

Various control measures are available to manage the house fly, for example, cultural practices, chemicals, and biological agents including fungal/bacterial pathogens and parasitoids/predators or combination of these measures [12, 13]. Insect growth regulators (IGR) comprise an effective chemical tool for integrated pest management due to their properties of high selectivity, killing immature stages, comparative environmentally safe, and reduced risk to the safety of mammals [14–16]. The juvenile hormone mimic pyriproxyfen inhibits the emergence of adults, cyromazine is a molting disrupter, diflubenzuron and triflumuron are inhibitors of chitin biosynthesis affecting chitin synthase 1, and methoxyfenozide is an ecdysone agonist [17]. These insecticides are effectively recommended to manage medical pests, including M. domestica, and are strong candidates for integrated pest management due to their different novel mode of actions and less environmental hazards [16, 18–20]. However, resistance to IGRs has been reported previously in house fly [20–25].

The study of life tables involves summarizing age or stage specific birth, death, and reproductive data. Classic models typically focus on females, but we will use both males and females. This methodology is a basic tool in pest management [26–28]. Comparison of the life tables of geographically separated pest populations aids in the design of effective pest management strategies. Geographic influences such as latitude and longitude and environmental influences such as humidity, photoperiod, and temperature often account for variations in the life tables of insect pests [29, 30]. Geographically and environmentally isolated pest populations have previously been reported to show variations in life tables, for instance, the house fly from urban localities in Pakistan [31]; Parapoynx crisonalis (Walker) (Lepidoptera: Pyralidae) [29]; Plutella xylostella (L.) (Lepidoptera: Plutellidae) from China [32]; and Melanoplus femurrubrum (De Geer) (Orthoptera: Acrididae) from USA [33]. Variations have also emerged in pesticide resistance in the house fly, Anopheles stephensi Liston (Diptera: Culicidae); Oxycarenus hyalinipennis Costa (Hemiptera: Lygaidae); Amrasca devastans (Distant) (Hemiptera: Cicadellidae); and Dysdercus koenigii (F.) (Hemiptera: Pyrrhocoridae) [5, 7, 20, 34–39].

Development of resistance in spatial dispersed pests is important to consider in resistant management strategies. For example, the populations of house fly from Punjab, Pakistan showed significant variations in resistant levels to various insecticides under different environments such as dairy (open) and poultry farms (enclosed) [5, 40]. The knowledge of insecticide resistance and life table features in the house fly from different separated dairies is very important in the design of effective management plans in different regions. Resistance to insect growth regulator insecticides and variations in the life history features of house fly from different originated dairies in Saudi Arabia are currently unexplored. Therefore, the present experiments were conducted to obtain an understanding of the resistance status and life table on the basis of age, stage and two sexes of the house fly collected from different dairies in Saudi Arabia.

Materials and methods

Ethics approval

No specific permit was required to collect house fly samples from the dairy farms, as these farms were privately owned and collections were made merely by personal communication with the owners.

Collections of house fly populations

Approximately 150–200 adult house flies (of mixed sexes) were trapped in plastic jars (33 cm ×19 cm) from five dairy farms located in Riyadh, Saudi Arabia: Dirab (latitude 24.49° N, 46.62° E; elevation 576 m), Al-Masanie (latitude 24.58° N, 46.73° E; elevation 581 m), Al-Uraija (latitude 24.63° N, 46.66° E; elevation 612 m), Al-Washlah (latitude 24.54° N, 46.72° E; elevation 643 m), and Al-Muzahmiya (latitude 24.47° N, 46.27° E; elevation 764 m). These dairies were located averagely more than 30 kilometer apart to each other. At these dairies, cultural practices (sanitation) and about 8–10 number of insecticide sprays from pyrethroids and organophosphates classes per season are being used for the control of dairy pests (Personal communication).

Laboratory rearing of house fly populations

The rearing protocol of the house fly was adopted according to Abbas et al. [41] with some modifications. After collection, each population was shifted in a separate transparent cage (40×40 cm) in the laboratory and reared for one generation to get uniform insects. An adult diet (sugar + powdered milk at a 1:1 ratio, weighed in g) and water-soaked cotton wicks placed in 9 cm plastic petri dishes were provided for adult food. Adults were provided with fresh food every two days. Cotton wicks were moistened daily and replaced at two days interval. A paste of wheat bran, yeast, sugar and milk at a ratio of 20:5:1.5:1.5 (g), respectively, mixed with 120 mL water, was prepared in plastic cups (500 mL) and placed in adult cages for fecundity after two days rearing in the laboratory. Plastic cups with eggs were removed from adult cages daily and covered with a muslin cloth to avoid larval escape. When larvae had consumed the diet in the plastic cups, they were shifted into glass beakers with larval medium, where they became pupae. The emerged adults were shifted to cages to proceed to the next generation. All populations were maintained at 27±2°C, 65±5% humidity and a 12:12 h (L:D) photoperiod in the laboratory.

Insecticides

Commercial-grade formulated IGR groups including pyriproxyfen (IRAC # 7C, Admiral 10EC, Sumitomo Chemicals, Japan), diflubenzuron (IRAC # 15, Diflon 250WP, Saudi Delta Company, SA), triflumuron (IRAC # 15, Starycide 480SC, Bayer Crop Sciences, Germany), cyromazine (IRAC # 17, Novasat 75WP, Astranova Chemicals, SA), and methoxyfenozide (IRAC # 18, Runner 24SC, Dow Agro-sciences, UK).

Larval bioassays

The toxicity of IGR insecticides to the larvae of different dairy populations of M. domestica was determined through a diet incorporation bioassay following the method of Abbas et al. [20]. Different concentrations of each of the tested IGRs were incorporated into the larval medium (consisting of wheat bran, yeast, milk powder, and sugar at a ratio of 20:5:5:1.5:1.5 g, respectively). Five concentrations (causing mortality from >0% to <100%) of each IGR with four replicates of each were used in each bioassay. In total, 10 second instar larvae in each replicate, 40 larvae in each concentration, and 200 larvae were used in each bioassay. In the control treatment, 40 larvae with four replicates (10 larvae per replicate) were provided with larval medium without any IGR insecticide concentrations. All bioassays were conducted under the above mentioned constant conditions. Data were recorded at the emergence of adults after 3 weeks of the bioassay. Larvae that failed to transform into adults were considered as dead.

Life table construction

To construct the life table of house fly, 100 newly (≤24 h) laid eggs were randomly collected from different egg batches at one day of each mass population and were placed in plastic cups (500 ml) supplied with artificial larval diet aforementioned above. Single egg was considered as a replicate for each population [42]. The cups were enclosed with muslin cloth to prevent larval escape. Each population was reared separately. Hatched larvae were reared in cups on provided diet until pupation, and their developmental periods were recorded. Freshly emerged adults within 24 h were sexed and one male and one female placed into plastic jars (15 cm x 11 cm). Larval medium was provided daily in 9 cm petri dishes for oviposition. Eggs were counted daily till the death of females and egg hatchability was recorded. The female ratio, adult longevity, and oviposition period were also recorded. The experiment was conducted under the aforesaid laboratory conditions.

For each strain, the following parameters were calculated according to Chi and Su [43] and Tuan et al. [27]. Briefly, the age-specific survivorship (l_x) was determined as follows:

The age-stage-specific fecundity (m_x) was determined as follows:

The net reproductive rate (R0) was calculated as follows:

The intrinsic rate of increase (r) was assessed by the Lotka–Euler equation with the age indexing zero as follows:

The finite rate of increase (λ) was determined as:

The generation time (T) was determined as follows:

The life expectancy (e_xj) was calculated as follows:

The reproductive value (v_xj) was detected as follows:

The gross reproductive rate (GRR) was calculated as:

Where, x = alpha to beta

Data analyses

The bioassay data were analyzed using the POLO Plus software [44] to determine the values of median lethal concentration (LC₅₀). In each bioassay, the mortality rates were corrected by the mortality rate obtained in the control treatment using the formula of Abbott [45], if required. Resistance ratios (RRs) were calculated as: LC₅₀ of field population/LC₅₀ of susceptible strain. The resistance levels were scaled as mention by Ahmad et al. [46]; RR = 1 (susceptibility), RR = 2–10 (low resistance), RR = 11–30 (moderate resistance), RR = 31–100 (high resistance), and RR > 100 (very high resistance).

The life table data were analyzed with the TWO-SEX-MS Chart program [47] established on the basis of two sex life table principle [28, 48]. The variances and standard errors (SE) of life history features were determined by paired bootstrap test with 100,000 replicates at P ≤ 0.05 using the TWOSEX-MS Chart [47]. The parameters l_x, s_xj, f_x, m_x, l_xm_x, v_xj, and e_xj were graphed with Sigma Plot 11.0.

Results

Resistance of M. domestica larvae to IGRs

The toxicity of tested IGRs was not significantly different (overlapped 95% FL) among the field populations. Low resistance against methoxyfenozide (3.77–8.03-fold) and triflumuron (1.63–8.25-fold) was detected in all the five populations of M. domestica in comparison to the susceptible strain. Populations collected from the Dirab, Al-Masanie, and Al-Uraija had moderate resistance (10.75–29.75-fold) to pyriproxyfen, while the Al-Washlah and Al-Muzahmiya populations had low resistance levels (5.50–8.25-fold), compared with the susceptible strain. Susceptibility to cyromazine was found in all the tested populations (0.59–1.32-fold), except the Al-Masanie population which had low resistance (2.91-fold). Populations collected from the Dirab, Al-Washlah, Al-Masanie, and Al-Muzahmiya had moderate resistance (13.67–28.67-fold) to diflubenzuron, while the Al-Uraija population had low resistance level (9.33-fold), compared with the susceptible strain (Table 1).

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Table 1. Resistance to insect growth regulators in the larvae of different dairy farms M. domestica populations.

https://doi.org/10.1371/journal.pone.0248693.t001

Life history parameters of house flies from dairies

The larval durations of all the tested populations were significantly different from each other (P < 0.05). The pupal duration of the Al-Uraija population was significantly longer than that of the Dirab, Al-Masanie, Al-Washlah and Al-Muzahmiya populations (P < 0.05). The egg to adult duration for male flies from the Al-Masanie population was significantly longer than for flies from all other areas except Dirab (P < 0.05). Similarly, the egg to adult duration for female flies from the Al-Masanie population was significantly longer than for flies from all other areas (P < 0.05). The male total longevity in the Al-Uraija and Al-Muzahmiya populations was significantly shorter than those of the Dirab, Al-Masanie, and Al-Washlah populations (P < 0.05). The female total longevity in the Al-Washlah, Al-Uraija, and Al-Muzahmiya populations was significantly shorter (P < 0.05) than that of the Al-Masanie population (Table 2).

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Table 2. Development duration and life history parameters of five house fly populations collected from dairies in Riyadh, Saudi Arabia.

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The total-pre-oviposition period (TPOP) and adult-pre-oviposition period (APOP) of the Al-Masanie and Al-Washlah populations were significantly longer than those of the Dirab, Al-Uraija, and Al-Muzahmiya populations (P < 0.05). The oviposition period were significantly reduced in the Al-Washlah population compared with that of the Al-Muzahmiya population (P < 0.05), but similar with the other tested populations. The female ratio in the Al-Uraija population was significantly lower compared with the Dirab and Al-Washlah populations (P < 0.05). Whereas the reproductive female ratio was significantly lower in the Al-Washlah population compared with the other populations (P < 0.05). The fecundity/female was significantly lower in the Al-Washlah population than that of the Al-Masanie and Al-Muzahmiya populations (P < 0.05), but did not differ from that of the Dirab and Al-Uraija populations (Table 2).

Demographic life table features of house flies from dairies

The intrinsic rates of increase (r) in the Al-Masanie (0.013) and Al-Washlah (0.12) populations were significantly lower (P < 0.05) than that of the Dirab (0.17), Al-Uraija (0.18), and Al-Muzahmiya (0.19) populations. The finite rates of increase (λ) of the Al-Masanie and Al-Washlah (1.13) populations were significantly lower than that of the Dirab (1.18), Al-Uraija (1.19), and Al-Muzahmiya (1.21) populations (P < 0.05). The net reproductive rate (R₀) in the Al-Muzahmiya population (89.32) was significantly higher than that of the Al-Masanie (39.52) and Al-Washlah (33.04) populations (P < 0.05), and similar to that of the Dirab (74.50) and Al-Uraija (64.35) populations. The generation time (T) in the Al-Masanie (29.43) and Al-Washlah (29.80) populations was significantly longer than that of the Dirab (26.05), Al-Uraija (23.54), and Al-Muzahmiya (24.08) populations (P < 0.05). The doubling time (DT) was shorter in the Al-Uraija (3.92) and Al-Muzahmiya (3.72) populations (P < 0.05) than that of the Al-Washlah population (5.91), but similar to that of the Dirab (4.19) and Al-Masanie (5.55) populations. Among all the tested populations, the GRR (gross reproduction rate) was similar (P > 0.05, Table 3).

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Table 3. Demographic life table features of five house fly populations collected from dairies in Riyadh, Saudi Arabia.

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Age-stage-specific survival rates (s_xj) of house flies from dairies

The parameter s_xj refers to the possible survival of newly born eggs to age x and development to stage j (Fig 1). In all the populations the peak value of s_xj for larvae was similar. However, the highest peak values of s_xj for pupae in the Dirab (0.80) and Al-Washlah (0.70) populations were lower than those of the Al-Masanie (0.89), Ai-Uraija (0.99), and Al-Muzahmiya (0.97) populations. Similarly, the highest peak values of s_xj for females and males in the Dirab (0.25 and 0.24, respectively), Al-Uraija (0.21 and 0.49, respectively), and Al-Muzahmiya (0.29 and 0.36, respectively) populations were higher than those for the Al-Masanie (0.11 and 0.14, respectively) and Al-Washlah (0.19 and 0.13, respectively) populations.

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Fig 1. Age-stage-specific survival rate (s_xj) for the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations of house fly.

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Age-specific survivorship (l_x), fecundities (m_x, f_x), and maternity (l_xm_x) of house flies from dairies

The parameters l_x, f_x, m_x and l_xm_x were determined for all populations (Fig 2). Among all populations, non-significant differences were found in the highest peak values for l_x. The highest peaks of f_x in the Dirab (40.67 eggs female^-1day^-1) and Al-Muzahmiya (40.06 eggs female^-1day^-1) populations were lower than those in the Al-Masanie (44.33 eggs female^-1day^-1), Al-Washlah (43.75 eggs female^-1day^-1), and Al-Uraija (55.67 eggs female^-1day^-1) populations, while the highest peaks of m_x in the Dirab (19 eggs individual^-1day^-1), Al-Masanie (20.71 eggs individual^-1day^-1), and Al-Uraija (21.97 eggs individual^-1day^-1) populations were lower than those in the Al-Washlah (25 eggs individual^-1day^-1) and Al-Muzahmiya (34.43 eggs individual^-1day^-1) populations. Additionally, the peak times of l_x, f_x and m_x for the Dirab (45^th day), Al-Masanie (29^th day), Al-Washlah (43^th day), Al-Uraija (20^th day), and Al-Muzahmiya (31^th day) populations varied significantly among populations. Similarly, the highest peak values for l_xm_x in the Al-Masanie (4.35 at 24^th day) and Al-Washlah (2.68 at 25^th day) populations were lower than those in the Dirab (6.08 at 21^th day), Al-Uraija (8.35 at 20^th day), and Al-Muzahmiya (7.12 at 21^th day) populations.

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Fig 2. Age-specific survivorship (l_x), age-specific female fecundity (f_x), age-specific fecundity of the total population (m_x), and age-specific maternity (l_xm_x) for the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations of house fly.

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Age-stage-specific reproductive values (v_xj) of house flies from dairies

The v_xj reveals the reproductive value of insects at the age x and stage j in terms of future progeny (Fig 3). The peak v_xj values for larvae were 6.54, 3.91, 4.11, 3.44, and 5.52 day^-1 in the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations, respectively. The peak v_xj values for pupae in the Dirab (12.35 day^-1) Al-Masanie (7.49 day^-1), Al-Uraija (11.41 day^-1), and Al-Muzahmiya (11.56 day^-1) populations were lower than those in the Al-Washlah population (18.00 day^-1). The peak v_xj values for females in the Al-Masanie (166.7 day^-1), Al-Washlah (160.92 day^-1) and Al-Uraija (169.90 day^-1) populations were significantly higher than those in the Dirab (126.12 day^-1) and Al-Muzahmiya (132.47 day^-1) populations. The duration was shorter in the Al-Uraija and Al-Muzahmiya populations than that in the Dirab, Al-Masanie, and Al-Washlah populations.

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Fig 3. Age-stage-specific reproductive values (v_xj) for the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations of house fly.

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Age-stage-specific life expectancy (e_xj) of house flies from dairies

The e_xj refers to the expected days over which an insect at age x and stage j will survive after age x shown in Fig 4. The e_xj values for eggs were 22.13, 21.33, 16.48, 21.10, and 24.61 days in the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations, respectively. In the Al-Uraija and Al-Washlah populations, the peak e_xj values for larvae were 20.1 and 20.69 days, respectively, which were shorter than those in the Dirab (25.16 days), Al-Masanie (21.72), and Al-Muzahmiya (23.61 days) populations. The peak e_xj values for pupae were 19.16, 14.72, 17.69, 16.1, and 18.76 days in the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations, and each of these values differed significantly. The peak e_xj values for the female and male house fly differed significantly in the tested populations—Al-Masanie (26.1 days and 24.73 days, respectively), Al-Washlah (24.88 days and 29.46 days, respectively), Al-Muzahmiya (21.60 days and 16.13 days, respectively), Dirab (19.80 days and 19.81 days, respectively), and Al-Uraija (18.80 days and 18.30 days, respectively).

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Fig 4. Age-specific life expectancy (e_xj) for the Dirab, Al-Masanie, Al-Washlah, Al-Uraija, and Al-Muzahmiya populations of house fly.

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Correlation between IGR resistance ratios and life history features

There were nonsignificant correlations among the resistance ratios of tested IGRs in different house fly populations (Table 4). All the tested IGRs had nonsignificant positive and negative correlations with most of the life history features (P > 0.05). However, triflumuron had a significant positive correlation with the pupal duration (P = 0.04). The methoxyfenozide had significant positive correlation with pre-adult male duration (P = 0.03) and female longevity (P = 0.04; Table 5).

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Table 4. Correlation of resistance ratios of insect growth regulators to the house fly populations.

https://doi.org/10.1371/journal.pone.0248693.t004

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Table 5. Correlation between resistance ratios and life table features of the house fly populations.

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Discussion

In the current study, the five populations of house fly collected from dairy facilities showed susceptibility to cyromazine, low resistance to methoxyfenozide and triflumuron, low–moderate resistance to pyriproxyfen and diflubenzuron in comparison to the susceptible strain. However, the toxicity of these tested IGRs was not significantly different among the field populations. The insect populations that showed more than tenfold resistance to insecticides are known to be resistant [5, 49]. In this study, less than tenfold resistance to methoxyfenozide, cyromazine and triflumuron in all tested populations, pyriproxyfen in two populations, and diflubenzuron in one population were detected. These populations were considered tolerant rather than resistant. Previously, resistance to these insecticides has been found in house fly [20–22], Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) [50], Spodoptera litura (F.) (Lepidoptera: Noctuidae) [51], and Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) [52]. The development of resistance depends upon the use of particular insecticides at a facility [5, 53]. In Saudi Arabia, spray applications of different insecticides are more common relative to IGRs. Therefore, similar toxicities of IGRs against house fly populations may be due to no and/or very low use of these insecticides at these dairy facilities. However, this is the first susceptibility report of house fly populations to IGRs from dairy facilities in Riyadh, Saudi Arabia. Among the five tested IGRs, methoxyfenozide, cyromazine, and triflumuron were found to be the most toxic larvicides against house fly larvae. Therefore, these larvicides could be the most promising agents for the integrated vector management system in Saudi Arabia. However, the potential cross-resistance from other chemical classes [17] should be considered when aiming to design a successful IGRs rotation pattern which requires further studies to prolong the effectiveness of these larvicides. Additionally, use of cultural practices (sanitation) and biological control agents with inclusion of insecticides for the control of house fly should be considered as an integrated pest management tool [12, 13].

The adaptation of an insect pest to an altered environment and insecticide applications depends on its life table parameters, and evidence defining its population dynamics is crucial in formulating an effective pest management plan. The present study was conducted on the five house fly populations from different dairy farms in Riyadh, Saudi Arabia, to explore their life table dynamics. Results revealed prominent variations in the larval duration, pupal duration, pre-adult male and female duration, oviposition period, longevity of males and females, APOP, TPOP, female ratio, and fecundity female^-1. The reason for the differences in life history features could be attributed to altered elevations, latitudes, and environmental factors—for instance, temperature and humidity—favoring the adaptation of the house flies. Similar to those in the current results, significant variations in life history parameters have been reported in several differing isolated pest populations [29–31, 54, 55]. For example, the developmental time of P. xylostella populations from higher latitudes was longer than that from lower latitudes [32]. In contrast, Shirai [55] reported no difference in the immature developmental time among nine geographically separate P. xylostella populations. The larval duration in Colaphellus bowringi Baly (Coleoptera: Chrysomelidae) was increased with increasing latitudes [30], but decreased in geometrid moths; Cabera exanthemata (Scopoli), Lomaspilis marginata (L.), Chiasmia clathrata (L.), and Cabera pusaria (L.) (Lepidoptera: Geometridae) [54]. Chen et al. [29] reported a higher net reproductive rate at 24 ˚C than at other tested temperatures in P. crisonalis. In house fly populations from Pakistan, the immature developmental time was shorter and pupal weights were heavier in those from lower latitudes with hot climates [31]. The aforementioned variations among different insect pests could be due to the varied latitudes and favorable environments responsible for the flexibility of insect pests in their particular facilities [30, 56].

The present results exhibited variations in the demographic parameters (r, λ, R_O, T, and DT) among the five house fly populations. The r and λ of the Al-Masanie and Al-Washlah populations were significantly lower than those in other tested field populations. The Al-Muzahmiya population exhibited the highest Ro among all of the field populations. The mean generation time of the Al-Uraija and Al-Muzahmiya populations was significantly shorter than that of other tested populations, while the doubling time of the Al-Washlah population was higher than those of the Al-Uraija and Al-Muzahmiya populations. The parameters r, λ, and R_O provide the growth potential estimation of pests—a wider insight than that provided by individual life history features [2]. Because the parameters r and λ depend upon the fecundity and growth of individuals, therefore differences in these parameters might affect the expansion rates of populations [2, 57, 58]. The lower rates of increase in the populations in this study could be attributable to lower fecundity female^-1. In agreement with present results, significant variations in demographic life table parameters of pests have previously been reported in P. crisonalis [29], M. femurrubrum [33], and P. xylostella [32].

The parameters s_xj, l_x, f_x, m_x, l_xm_x, v_xj, and e_xj are important indicators for evaluating the biological fitness of insect pest populations. Similar insect pests under altered environments have different survival rates, reproduction abilities, and life spans, all of which reflect specific environmental effects and species-specific parameters [59, 60]. The present results for s_xj, l_x, f_x, m_x, l_xm_x, v_xj, and e_xj revealed significant variations in house fly populations from five different dairy farms. Because of differing environmental factors—for instance, temperature—and extents of insecticide exposure, significant variations in these parameters have previously been documented in a range of pests, including P. crisonalis [29], Sogatella furcifera (Horvath) (Hemiptera: Delphacidae) [60], Bradysia odoriphaga Yang and Zhang (Diptera: Sciaridae) [42], Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae) [61], S. litura [27], and Tetranychus urticae Koch (Acari: Tetranychidae) [62]. The house fly has 5–7 kilometer flight range and dispersal [63], whereas in the present study, the house fly populations were collected from averagely more than 30 kilometer apart located dairies. The differences in life history features may be due to different populations and differences in extent of management activities for house fly in specific dairy facilities by the dairy owners.

Effectiveness and implementation of control measures against insect pests depend on knowledge of the life table attributes of any pest in its respective environment [31, 32]. In the present study, M. domestica populations collected from Dirab, Al-Uraija, and Al-Muzahmiya facilities showed faster development and better life table parameters than those from the Al-Masanie and Al-Washlah facilities. Rapid growth of house fly in these dairy facilities may enhance the insecticidal usage, which ultimately may lead to resistance problem in the future. Therefore, the management of house fly should be focused on specific dairy facility. Moreover, nonsignificant correlations between life history features and IGRs suggest that the integration of IGRs with cultural practices in these dairy facilities may suppress the house fly growth and resistance problem. Our results provide useful insights about the age, stage, and two sexes based life table variations in house fly populations from Riyadh, Saudi Arabia for the better management in specific dairy facilities.

Supporting information

S1 File. Life table of Musca domestica population collected from Dirab, Saudi Arabia.

https://doi.org/10.1371/journal.pone.0248693.s001

(XLSX)

S2 File. Life table of Musca domestica population collected from Al-Masanie, Saudi Arabia.

https://doi.org/10.1371/journal.pone.0248693.s002

(XLSX)

S3 File. Life table of Musca domestica population collected from Al-Washlah, Saudi Arabia.

https://doi.org/10.1371/journal.pone.0248693.s003

(XLSX)

S4 File. Life table of Musca domestica population collected from Al-Uraija, Saudi Arabia.

https://doi.org/10.1371/journal.pone.0248693.s004

(XLSX)

S5 File. Life table of Musca domestica population collected from Al-Muzahmiya, Saudi Arabia.

https://doi.org/10.1371/journal.pone.0248693.s005

(XLSX)

Acknowledgments

The authors thank the Deanship of Scientific Research and Researchers Support and Services Unit (RSSU) at King Saud University for their technical support. Authors would like also to thank the researchers and technicians from Pesticides and Environmental Toxicology Laboratory: Ahmed Mohammed Dabo and Safwat Gamal Sabra for their help in collecting and maintaining the house fly field populations in the laboratory and for other laboratory work.

References

1. Abbas N, Shah RM, Shad SA, Azher F. Dominant fitness costs of resistance to fipronil in Musca domestica Linnaeus (Diptera: Muscidae). Vet Parasitol. 2016;226:78–82. pmid:27514889
- View Article
- PubMed/NCBI
- Google Scholar
2. Shah RM, Shad SA, Abbas N. Methoxyfenozide resistance of the housefly, Musca domestica L. (Diptera: Muscidae): cross-resistance patterns, stability and associated fitness costs. Pest Manage Sci. 2017;73(1):254–61. pmid:27098995
- View Article
- PubMed/NCBI
- Google Scholar
3. Fasanella A, Scasciamacchia S, Garofolo G, Giangaspero A, Tarsitano E, Adone R. Evaluation of the house fly Musca domestica as a mechanical vector for an anthrax. PloS One. 2010;5(8):e12219. pmid:20808920
- View Article
- PubMed/NCBI
- Google Scholar
4. Förster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K. Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res. 2007;101(1):243–6. pmid:17370089
- View Article
- PubMed/NCBI
- Google Scholar
5. Abbas N, Shad SA, Ismail M. Resistance to conventional and new insecticides in house flies (Diptera: Muscidae) from poultry facilities in Punjab, Pakistan. J Econ Entomol. 2015;108(2):826–33. pmid:26470195
- View Article
- PubMed/NCBI
- Google Scholar
6. Abbas N, Ijaz M, Shad SA, Binyameen M. Assessment of resistance risk to fipronil and cross resistance to other insecticides in the Musca domestica L. (Diptera: Muscidae). Vet Parasitol. 2016;223:71–6. pmid:27198780
- View Article
- PubMed/NCBI
- Google Scholar
7. Khan HAA, Akram W, Fatima A. Resistance to pyrethroid insecticides in house flies, Musca domestica L., (Diptera: Muscidae) collected from urban areas in Punjab, Pakistan. Parasitol Res. 2017;116(12):3381–5. pmid:29075926
- View Article
- PubMed/NCBI
- Google Scholar
8. Freeman JC, Ross DH, Scott JG. Insecticide resistance monitoring of house fly populations from the United States. Pestic Biochem Physiol. 2019;158:61–8. pmid:31378362
- View Article
- PubMed/NCBI
- Google Scholar
9. Li Q, Huang J, Yuan J. Status and preliminary mechanism of resistance to insecticides in a field strain of house fly (Musca domestica, L). Rev Bras Entomol. 2018;62(4):311–4.
- View Article
- Google Scholar
10. Shah RM, Shad SA. House fly resistance to chlorantraniliprole: cross resistance patterns, stability and associated fitness costs. Pest Manage Sci. 2020;76(5):1866–73. pmid:31840405
- View Article
- PubMed/NCBI
- Google Scholar
11. Abbas N, Khan HAA, Shad SA. Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin: mode of inheritance, realized heritability, and cross-resistance to other insecticides. Ecotoxicology. 2014;23(5):791–801. pmid:24609299
- View Article
- PubMed/NCBI
- Google Scholar
12. Malik A, Singh N, Satya S. House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health. 2007;42(4):453–69. pmid:17474025
- View Article
- PubMed/NCBI
- Google Scholar
13. Farooq M, Freed S. Infectivity of housefly, Musca domestica (Diptera: Muscidae) to different entomopathogenic fungi. Braz J Microbiol. 2016;47(4):807–16. pmid:27522925
- View Article
- PubMed/NCBI
- Google Scholar
14. Tunaz H, Uygun N. Insect growth regulators for insect pest control. Turk J Agric For. 2004;28(6):377–87.
- View Article
- Google Scholar
15. Mian LS, Mulla MS. Biological and environmental dynamics of insect growth regulators (IGRs) as used against Diptera of public health importance. Resid Rev. 1982. p. 27–112. pmid:6760307
- View Article
- PubMed/NCBI
- Google Scholar
16. Kočišová A, Petrovský M, Toporčák J, Novák P. The potential of some insect growth regulators in housefly (Musca domestica) control. Biol Bratisl. 2004;59(5):661–8.
- View Article
- Google Scholar
17. IRAC. IRAC: Mode of action classification scheme, Version 9.4,. www.irac-online.org › documents › moa-classification. 2020:pp, 1–26.
18. Shah RM, Abbas N, Shad SA, Sial AA. Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitol Res. 2015;114(2):487–94. pmid:25363707
- View Article
- PubMed/NCBI
- Google Scholar
19. Matsumura F. Studies on the action mechanism of benzoylurea insecticides to inhibit the process of chitin synthesis in insects: A review on the status of research activities in the past, the present and the future prospects. Pestic Biochem Physiol. 2010;97(2):133–9.
- View Article
- Google Scholar
20. Abbas N, Shad SA, Shah RM. Resistance status of Musca domestica L. populations to neonicotinoids and insect growth regulators in Pakistan poultry facilities. Pak J Zool. 2015;47(6):1663–71.
- View Article
- Google Scholar
21. Khan HAA, Akram W, Arshad M, Hafeez F. Toxicity and resistance of field collected Musca domestica (Diptera: Muscidae) against insect growth regulator insecticides. Parasitol Res. 2016;115(4):1385–90. pmid:26711449
- View Article
- PubMed/NCBI
- Google Scholar
22. Bell HA, Robinson KA, Weaver RJ. First report of cyromazine resistance in a population of UK house fly (Musca domestica) associated with intensive livestock production. Pest Manage Sci. 2010;66(7):693–5.
- View Article
- Google Scholar
23. Tang JD, Caprio MA, Sheppard DC, Gaydon DM. Genetics and fitness costs of cyromazine resistance in the house fly (Diptera: Muscidae). J Econ Entomol. 2002;95(6):1251–60. pmid:12539839
- View Article
- PubMed/NCBI
- Google Scholar
24. Shah RM, Shad SA, Abbas N. Mechanism, stability and fitness cost of resistance to pyriproxyfen in the house fly, Musca domestica L. (Diptera: Muscidae). Pestic Biochem Physiol. 2015;119:67–73. pmid:25868819
- View Article
- PubMed/NCBI
- Google Scholar
25. Shah RM, Abbas N, Shad SA, Binyameen M. Determination of the genetic and synergistic suppression of a methoxyfenozide-resistant strain of the house fly Musca domestica L. (Diptera: Muscidae). Neotrop Entomol. 2018;47(5):709–15. pmid:29654414
- View Article
- PubMed/NCBI
- Google Scholar
26. Chi H, You M, Atlıhan R, Smith CL, Kavousi A, Özgökçe MS, et al. Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen. 2020;40(2):102–23.
- View Article
- Google Scholar
27. Tuan SJ, Lee CC, Chi H. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manage Sci. 2014;70(5):805–13. pmid:23893943
- View Article
- PubMed/NCBI
- Google Scholar
28. Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988;17(1):26–34.
- View Article
- Google Scholar
29. Chen Q, Li N, Wang X, Ma L, Huang J-B, Huang G-H. Age-stage, two-sex life table of Parapoynx crisonalis (Lepidoptera: Pyralidae) at different temperatures. PloS One. 2017;12(3):e0173380. pmid:28264022
- View Article
- PubMed/NCBI
- Google Scholar
30. Tang J, He H, Chen C, Fu S, Xue F. Latitudinal cogradient variation of development time and growth rate and a negative latitudinal body weight cline in a widely distributed cabbage beetle. PloS One. 2017;12(7):e0181030. pmid:28704496
- View Article
- PubMed/NCBI
- Google Scholar
31. Khan HAA, Khan MU, Nasiba A, Riaz S, Altaf M. Geographical variations in life histories of house flies, Musca domestica (Diptera: Muscidae), in Punjab, Pakistan. J Med Entomol. 2019;56(5):1225–30. pmid:31081906
- View Article
- PubMed/NCBI
- Google Scholar
32. Pan Q-J, Chen L, Lin X-L, Ridsdill-Smith TJ, Liu T-X. Geographical variations in life histories of Plutella xylostella in China. J Pest Sci. 2014;87(4):659–70.
- View Article
- Google Scholar
33. Parsons SMA, Joern A. Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia. 2014;174(2):379–91. pmid:24065558
- View Article
- PubMed/NCBI
- Google Scholar
34. Saeed R, Abbas N, Razaq M, Mahmood Z, Naveed M, Rehman HMU. Field evolved resistance to pyrethroids, neonicotinoids and biopesticides in Dysdercus koenigii (Hemiptera: Pyrrhocoridae) from Punjab, Pakistan. Chemosphere. 2018;213:149–55. pmid:30216815
- View Article
- PubMed/NCBI
- Google Scholar
35. Saeed R, Razaq M, Abbas N, Jan MT, Naveed M. Toxicity and resistance of the cotton leaf hopper, Amrasca devastans (Distant) to neonicotinoid insecticides in Punjab, Pakistan. Crop Prot. 2017;93:143–7.
- View Article
- Google Scholar
36. Ullah S, Shad SA, Abbas N. Resistance of dusky Cotton bug, Oxycarenus hyalinipennis Costa (Lygaidae: Hemiptera), to conventional and novel chemistry insecticides. J Econ Entomol. 2016;109(1):345–51. pmid:26546488
- View Article
- PubMed/NCBI
- Google Scholar
37. Khan HAA, Akram W, Lee S. Resistance to selected pyrethroid insecticides in the malaria mosquito, Anopheles stephensi (Diptera: Culicidae), from Punjab, Pakistan. J Med Entomol. 2018;55(3):735–8. pmid:29346647
- View Article
- PubMed/NCBI
- Google Scholar
38. Kaufman PE, Nunez SC, Mann RS, Geden CJ, Scharf ME. Nicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Manage Sci. 2010;66(3):290–4. pmid:19904713
- View Article
- PubMed/NCBI
- Google Scholar
39. Wang J-N, Hou J, Wu Y-Y, Guo S, Liu Q-M, Li T-Q, et al. Resistance of house fly, Musca domestica L. (Diptera: Muscidae), to five insecticides in Zhejiang Province, China: The situation in 2017. Can J Infect Dis Med Microbiol. 2019;2019:1–10. pmid:31341522
- View Article
- PubMed/NCBI
- Google Scholar
40. Khan HAA, Akram W, Shad SA. Resistance to conventional insecticides in Pakistani populations of Musca domestica L. (Diptera: Muscidae): a potential ectoparasite of dairy animals. Ecotoxicology. 2013;22:522–7. pmid:23371032
- View Article
- PubMed/NCBI
- Google Scholar
41. Abbas N, Khan HAA, Shad SA. Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission. Parasitol Res. 2014;113(4):1343–52. pmid:24481906
- View Article
- PubMed/NCBI
- Google Scholar
42. Gul H, Ullah F, Biondi A, Desneux N, Qian D, Gao X, et al. Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia odoriphaga. Entomol Gen. 2019;39(2):81–92.
- View Article
- Google Scholar
43. Chi H, Su H-Y. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol. 2006;35(1):10–21.
- View Article
- Google Scholar
44. LeOra S. Poloplus, a user’s guide to probit or logit analysis. LeOra Software, Berkeley, CA. 2003.
45. Abbott W. A method of computing the effectiveness of an insecticide. J Econ Entomol. 1925;18(2):265–7.
- View Article
- Google Scholar
46. Ahmad M, Iqbal Arif M, Ahmad M. Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Prot. 2007;26(6):809–17.
- View Article
- Google Scholar
47. Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140120197173/Ecology/prod02htm. 2019.
- View Article
- Google Scholar
48. Chi H, Yang T-C. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ Entomol. 2003;32(2):327–33.
- View Article
- Google Scholar
49. Valles SM, Koehler PG, Brenner RJ. Antagonism of fipronil toxicity by piperonyl butoxide and S, S, S-tributyl phosphorotrithioate in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol. 1997;90(5):1254–8.
- View Article
- Google Scholar
50. Saddiq B, Shad SA, Aslam M, Ijaz M, Abbas N. Monitoring resistance of Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) to new chemical insecticides in Punjab, Pakistan. Crop Prot. 2015;74:24–9.
- View Article
- Google Scholar
51. Ahmad M, Gull S. Susceptibility of armyworm Spodoptera litura (Lepidoptera: Noctuidae) to novel insecticides in Pakistan. Can Entomol. 2017;149(5):649–61.
- View Article
- Google Scholar
52. Gutiérrez-Moreno R, Mota-Sanchez D, Blanco CA, Whalon ME, Terán-Santofimio H, Rodriguez-Maciel JC, et al. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol. 2019;112(2):792–802. pmid:30535077
- View Article
- PubMed/NCBI
- Google Scholar
53. Scott JG, Alefantis TG, Kaufman PE, Rutz DA. Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manage Sci. 2000;56(2):147–53.
- View Article
- Google Scholar
54. Kivelä SM, Välimäki P, Carrasco D, Mäenpää MI, Oksanen J. Latitudinal insect body size clines revisited: a critical evaluation of the saw-tooth model. J Anim Ecol. 2011;80(6):1184–95. pmid:21605117
- View Article
- PubMed/NCBI
- Google Scholar
55. Shirai Y. Temperature tolerance of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae) in tropical and temperate regions of Asia. Bull Entomol Res. 2000;90(4):357–64. pmid:11020794
- View Article
- PubMed/NCBI
- Google Scholar
56. Honek A. Geographical variation in thermal requirements for insect development. Eur J Entomol. 2013;93(3):303–12.
- View Article
- Google Scholar
57. Abbas N, Khan H, Shad SA. Cross-resistance, stability, and fitness cost of resistance to imidacloprid in Musca domestica L., (Diptera: Muscidae). Parasitol Res. 2015;114(1):247–55. Epub 2014/10/25. pmid:25342464.
- View Article
- PubMed/NCBI
- Google Scholar
58. Abbas N, Shad SA, Razaq M. Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: Noctuidae). Pestic Biochem Physiol. 2012;103(3):181–8.
- View Article
- Google Scholar
59. Zhang P, Zhao Y-H, Wang Q-H, Mu W, Liu F. Lethal and sublethal effects of the chitin synthesis inhibitor chlorfluazuron on Bradysia odoriphaga Yang and Zhang (Diptera: Sciaridae). Pestic Biochem Physiol. 2017;136:80–8. pmid:28187835
- View Article
- PubMed/NCBI
- Google Scholar
60. Xiang X, Liu S, Wang X, Zhang Y, Gong C, Chen L, et al. Sublethal effects of sulfoxaflor on population projection and development of the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Crop Prot. 2019;120:97–102.
- View Article
- Google Scholar
61. Yuan H-g, Wu S-y, Lei Z-r, Rondon SI, Gao Y-l. Sub-lethal effects of Beauveria bassiana (Balsamo) on field populations of the potato tuberworm Phthorimaea operculella Zeller in China. J Integr Agric. 2018;17(4):911–8.
- View Article
- Google Scholar
62. Wang L, Zhang Y, Xie W, Wu Q, Wang S. Sublethal effects of spinetoram on the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Pestic Biochem Physiol. 2016;132:102–7. pmid:27521920
- View Article
- PubMed/NCBI
- Google Scholar
63. Nazni WA, Luke H, Rozita WMW, Abdullah AG, Sa’diyah I, Azahari AH, et al. Determination of the flight range and dispersal of the house fly, Musca domestica (L.) using mark release recapture technique. Trop Biomed. 2005;22(1):53–61. pmid:16880754
- View Article
- PubMed/NCBI
- Google Scholar

[ref1] 1. Abbas N, Shah RM, Shad SA, Azher F. Dominant fitness costs of resistance to fipronil in Musca domestica Linnaeus (Diptera: Muscidae). Vet Parasitol. 2016;226:78–82. pmid:27514889
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. Shah RM, Shad SA, Abbas N. Methoxyfenozide resistance of the housefly, Musca domestica L. (Diptera: Muscidae): cross-resistance patterns, stability and associated fitness costs. Pest Manage Sci. 2017;73(1):254–61. pmid:27098995
View Article
PubMed/NCBI
Google Scholar

[6] View Article

[7] PubMed/NCBI

[8] Google Scholar

[ref3] 3. Fasanella A, Scasciamacchia S, Garofolo G, Giangaspero A, Tarsitano E, Adone R. Evaluation of the house fly Musca domestica as a mechanical vector for an anthrax. PloS One. 2010;5(8):e12219. pmid:20808920
View Article
PubMed/NCBI
Google Scholar

[10] View Article

[11] PubMed/NCBI

[12] Google Scholar

[ref4] 4. Förster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K. Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res. 2007;101(1):243–6. pmid:17370089
View Article
PubMed/NCBI
Google Scholar

[14] View Article

[15] PubMed/NCBI

[16] Google Scholar

[ref5] 5. Abbas N, Shad SA, Ismail M. Resistance to conventional and new insecticides in house flies (Diptera: Muscidae) from poultry facilities in Punjab, Pakistan. J Econ Entomol. 2015;108(2):826–33. pmid:26470195
View Article
PubMed/NCBI
Google Scholar

[18] View Article

[19] PubMed/NCBI

[20] Google Scholar

[ref6] 6. Abbas N, Ijaz M, Shad SA, Binyameen M. Assessment of resistance risk to fipronil and cross resistance to other insecticides in the Musca domestica L. (Diptera: Muscidae). Vet Parasitol. 2016;223:71–6. pmid:27198780
View Article
PubMed/NCBI
Google Scholar

[22] View Article

[23] PubMed/NCBI

[24] Google Scholar

[ref7] 7. Khan HAA, Akram W, Fatima A. Resistance to pyrethroid insecticides in house flies, Musca domestica L., (Diptera: Muscidae) collected from urban areas in Punjab, Pakistan. Parasitol Res. 2017;116(12):3381–5. pmid:29075926
View Article
PubMed/NCBI
Google Scholar

[26] View Article

[27] PubMed/NCBI

[28] Google Scholar

[ref8] 8. Freeman JC, Ross DH, Scott JG. Insecticide resistance monitoring of house fly populations from the United States. Pestic Biochem Physiol. 2019;158:61–8. pmid:31378362
View Article
PubMed/NCBI
Google Scholar

[30] View Article

[31] PubMed/NCBI

[32] Google Scholar

[ref9] 9. Li Q, Huang J, Yuan J. Status and preliminary mechanism of resistance to insecticides in a field strain of house fly (Musca domestica, L). Rev Bras Entomol. 2018;62(4):311–4.
View Article
Google Scholar

[34] View Article

[35] Google Scholar

[ref10] 10. Shah RM, Shad SA. House fly resistance to chlorantraniliprole: cross resistance patterns, stability and associated fitness costs. Pest Manage Sci. 2020;76(5):1866–73. pmid:31840405
View Article
PubMed/NCBI
Google Scholar

[37] View Article

[38] PubMed/NCBI

[39] Google Scholar

[ref11] 11. Abbas N, Khan HAA, Shad SA. Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin: mode of inheritance, realized heritability, and cross-resistance to other insecticides. Ecotoxicology. 2014;23(5):791–801. pmid:24609299
View Article
PubMed/NCBI
Google Scholar

[41] View Article

[42] PubMed/NCBI

[43] Google Scholar

[ref12] 12. Malik A, Singh N, Satya S. House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health. 2007;42(4):453–69. pmid:17474025
View Article
PubMed/NCBI
Google Scholar

[45] View Article

[46] PubMed/NCBI

[47] Google Scholar

[ref13] 13. Farooq M, Freed S. Infectivity of housefly, Musca domestica (Diptera: Muscidae) to different entomopathogenic fungi. Braz J Microbiol. 2016;47(4):807–16. pmid:27522925
View Article
PubMed/NCBI
Google Scholar

[49] View Article

[50] PubMed/NCBI

[51] Google Scholar

[ref14] 14. Tunaz H, Uygun N. Insect growth regulators for insect pest control. Turk J Agric For. 2004;28(6):377–87.
View Article
Google Scholar

[53] View Article

[54] Google Scholar

[ref15] 15. Mian LS, Mulla MS. Biological and environmental dynamics of insect growth regulators (IGRs) as used against Diptera of public health importance. Resid Rev. 1982. p. 27–112. pmid:6760307
View Article
PubMed/NCBI
Google Scholar

[56] View Article

[57] PubMed/NCBI

[58] Google Scholar

[ref16] 16. Kočišová A, Petrovský M, Toporčák J, Novák P. The potential of some insect growth regulators in housefly (Musca domestica) control. Biol Bratisl. 2004;59(5):661–8.
View Article
Google Scholar

[60] View Article

[61] Google Scholar

[ref17] 17. IRAC. IRAC: Mode of action classification scheme, Version 9.4,. www.irac-online.org › documents › moa-classification. 2020:pp, 1–26.

[ref18] 18. Shah RM, Abbas N, Shad SA, Sial AA. Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitol Res. 2015;114(2):487–94. pmid:25363707
View Article
PubMed/NCBI
Google Scholar

[64] View Article

[65] PubMed/NCBI

[66] Google Scholar

[ref19] 19. Matsumura F. Studies on the action mechanism of benzoylurea insecticides to inhibit the process of chitin synthesis in insects: A review on the status of research activities in the past, the present and the future prospects. Pestic Biochem Physiol. 2010;97(2):133–9.
View Article
Google Scholar

[68] View Article

[69] Google Scholar

[ref20] 20. Abbas N, Shad SA, Shah RM. Resistance status of Musca domestica L. populations to neonicotinoids and insect growth regulators in Pakistan poultry facilities. Pak J Zool. 2015;47(6):1663–71.
View Article
Google Scholar

[71] View Article

[72] Google Scholar

[ref21] 21. Khan HAA, Akram W, Arshad M, Hafeez F. Toxicity and resistance of field collected Musca domestica (Diptera: Muscidae) against insect growth regulator insecticides. Parasitol Res. 2016;115(4):1385–90. pmid:26711449
View Article
PubMed/NCBI
Google Scholar

[74] View Article

[75] PubMed/NCBI

[76] Google Scholar

[ref22] 22. Bell HA, Robinson KA, Weaver RJ. First report of cyromazine resistance in a population of UK house fly (Musca domestica) associated with intensive livestock production. Pest Manage Sci. 2010;66(7):693–5.
View Article
Google Scholar

[78] View Article

[79] Google Scholar

[ref23] 23. Tang JD, Caprio MA, Sheppard DC, Gaydon DM. Genetics and fitness costs of cyromazine resistance in the house fly (Diptera: Muscidae). J Econ Entomol. 2002;95(6):1251–60. pmid:12539839
View Article
PubMed/NCBI
Google Scholar

[81] View Article

[82] PubMed/NCBI

[83] Google Scholar

[ref24] 24. Shah RM, Shad SA, Abbas N. Mechanism, stability and fitness cost of resistance to pyriproxyfen in the house fly, Musca domestica L. (Diptera: Muscidae). Pestic Biochem Physiol. 2015;119:67–73. pmid:25868819
View Article
PubMed/NCBI
Google Scholar

[85] View Article

[86] PubMed/NCBI

[87] Google Scholar

[ref25] 25. Shah RM, Abbas N, Shad SA, Binyameen M. Determination of the genetic and synergistic suppression of a methoxyfenozide-resistant strain of the house fly Musca domestica L. (Diptera: Muscidae). Neotrop Entomol. 2018;47(5):709–15. pmid:29654414
View Article
PubMed/NCBI
Google Scholar

[89] View Article

[90] PubMed/NCBI

[91] Google Scholar

[ref26] 26. Chi H, You M, Atlıhan R, Smith CL, Kavousi A, Özgökçe MS, et al. Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen. 2020;40(2):102–23.
View Article
Google Scholar

[93] View Article

[94] Google Scholar

[ref27] 27. Tuan SJ, Lee CC, Chi H. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manage Sci. 2014;70(5):805–13. pmid:23893943
View Article
PubMed/NCBI
Google Scholar

[96] View Article

[97] PubMed/NCBI

[98] Google Scholar

[ref28] 28. Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988;17(1):26–34.
View Article
Google Scholar

[100] View Article

[101] Google Scholar

[ref29] 29. Chen Q, Li N, Wang X, Ma L, Huang J-B, Huang G-H. Age-stage, two-sex life table of Parapoynx crisonalis (Lepidoptera: Pyralidae) at different temperatures. PloS One. 2017;12(3):e0173380. pmid:28264022
View Article
PubMed/NCBI
Google Scholar

[103] View Article

[104] PubMed/NCBI

[105] Google Scholar

[ref30] 30. Tang J, He H, Chen C, Fu S, Xue F. Latitudinal cogradient variation of development time and growth rate and a negative latitudinal body weight cline in a widely distributed cabbage beetle. PloS One. 2017;12(7):e0181030. pmid:28704496
View Article
PubMed/NCBI
Google Scholar

[107] View Article

[108] PubMed/NCBI

[109] Google Scholar

[ref31] 31. Khan HAA, Khan MU, Nasiba A, Riaz S, Altaf M. Geographical variations in life histories of house flies, Musca domestica (Diptera: Muscidae), in Punjab, Pakistan. J Med Entomol. 2019;56(5):1225–30. pmid:31081906
View Article
PubMed/NCBI
Google Scholar

[111] View Article

[112] PubMed/NCBI

[113] Google Scholar

[ref32] 32. Pan Q-J, Chen L, Lin X-L, Ridsdill-Smith TJ, Liu T-X. Geographical variations in life histories of Plutella xylostella in China. J Pest Sci. 2014;87(4):659–70.
View Article
Google Scholar

[115] View Article

[116] Google Scholar

[ref33] 33. Parsons SMA, Joern A. Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia. 2014;174(2):379–91. pmid:24065558
View Article
PubMed/NCBI
Google Scholar

[118] View Article

[119] PubMed/NCBI

[120] Google Scholar

[ref34] 34. Saeed R, Abbas N, Razaq M, Mahmood Z, Naveed M, Rehman HMU. Field evolved resistance to pyrethroids, neonicotinoids and biopesticides in Dysdercus koenigii (Hemiptera: Pyrrhocoridae) from Punjab, Pakistan. Chemosphere. 2018;213:149–55. pmid:30216815
View Article
PubMed/NCBI
Google Scholar

[122] View Article

[123] PubMed/NCBI

[124] Google Scholar

[ref35] 35. Saeed R, Razaq M, Abbas N, Jan MT, Naveed M. Toxicity and resistance of the cotton leaf hopper, Amrasca devastans (Distant) to neonicotinoid insecticides in Punjab, Pakistan. Crop Prot. 2017;93:143–7.
View Article
Google Scholar

[126] View Article

[127] Google Scholar

[ref36] 36. Ullah S, Shad SA, Abbas N. Resistance of dusky Cotton bug, Oxycarenus hyalinipennis Costa (Lygaidae: Hemiptera), to conventional and novel chemistry insecticides. J Econ Entomol. 2016;109(1):345–51. pmid:26546488
View Article
PubMed/NCBI
Google Scholar

[129] View Article

[130] PubMed/NCBI

[131] Google Scholar

[ref37] 37. Khan HAA, Akram W, Lee S. Resistance to selected pyrethroid insecticides in the malaria mosquito, Anopheles stephensi (Diptera: Culicidae), from Punjab, Pakistan. J Med Entomol. 2018;55(3):735–8. pmid:29346647
View Article
PubMed/NCBI
Google Scholar

[133] View Article

[134] PubMed/NCBI

[135] Google Scholar

[ref38] 38. Kaufman PE, Nunez SC, Mann RS, Geden CJ, Scharf ME. Nicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Manage Sci. 2010;66(3):290–4. pmid:19904713
View Article
PubMed/NCBI
Google Scholar

[137] View Article

[138] PubMed/NCBI

[139] Google Scholar

[ref39] 39. Wang J-N, Hou J, Wu Y-Y, Guo S, Liu Q-M, Li T-Q, et al. Resistance of house fly, Musca domestica L. (Diptera: Muscidae), to five insecticides in Zhejiang Province, China: The situation in 2017. Can J Infect Dis Med Microbiol. 2019;2019:1–10. pmid:31341522
View Article
PubMed/NCBI
Google Scholar

[141] View Article

[142] PubMed/NCBI

[143] Google Scholar

[ref40] 40. Khan HAA, Akram W, Shad SA. Resistance to conventional insecticides in Pakistani populations of Musca domestica L. (Diptera: Muscidae): a potential ectoparasite of dairy animals. Ecotoxicology. 2013;22:522–7. pmid:23371032
View Article
PubMed/NCBI
Google Scholar

[145] View Article

[146] PubMed/NCBI

[147] Google Scholar

[ref41] 41. Abbas N, Khan HAA, Shad SA. Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission. Parasitol Res. 2014;113(4):1343–52. pmid:24481906
View Article
PubMed/NCBI
Google Scholar

[149] View Article

[150] PubMed/NCBI

[151] Google Scholar

[ref42] 42. Gul H, Ullah F, Biondi A, Desneux N, Qian D, Gao X, et al. Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia odoriphaga. Entomol Gen. 2019;39(2):81–92.
View Article
Google Scholar

[153] View Article

[154] Google Scholar

[ref43] 43. Chi H, Su H-Y. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol. 2006;35(1):10–21.
View Article
Google Scholar

[156] View Article

[157] Google Scholar

[ref44] 44. LeOra S. Poloplus, a user’s guide to probit or logit analysis. LeOra Software, Berkeley, CA. 2003.

[ref45] 45. Abbott W. A method of computing the effectiveness of an insecticide. J Econ Entomol. 1925;18(2):265–7.
View Article
Google Scholar

[160] View Article

[161] Google Scholar

[ref46] 46. Ahmad M, Iqbal Arif M, Ahmad M. Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Prot. 2007;26(6):809–17.
View Article
Google Scholar

[163] View Article

[164] Google Scholar

[ref47] 47. Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140120197173/Ecology/prod02htm. 2019.
View Article
Google Scholar

[166] View Article

[167] Google Scholar

[ref48] 48. Chi H, Yang T-C. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ Entomol. 2003;32(2):327–33.
View Article
Google Scholar

[169] View Article

[170] Google Scholar

[ref49] 49. Valles SM, Koehler PG, Brenner RJ. Antagonism of fipronil toxicity by piperonyl butoxide and S, S, S-tributyl phosphorotrithioate in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol. 1997;90(5):1254–8.
View Article
Google Scholar

[172] View Article

[173] Google Scholar

[ref50] 50. Saddiq B, Shad SA, Aslam M, Ijaz M, Abbas N. Monitoring resistance of Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) to new chemical insecticides in Punjab, Pakistan. Crop Prot. 2015;74:24–9.
View Article
Google Scholar

[175] View Article

[176] Google Scholar

[ref51] 51. Ahmad M, Gull S. Susceptibility of armyworm Spodoptera litura (Lepidoptera: Noctuidae) to novel insecticides in Pakistan. Can Entomol. 2017;149(5):649–61.
View Article
Google Scholar

[178] View Article

[179] Google Scholar

[ref52] 52. Gutiérrez-Moreno R, Mota-Sanchez D, Blanco CA, Whalon ME, Terán-Santofimio H, Rodriguez-Maciel JC, et al. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol. 2019;112(2):792–802. pmid:30535077
View Article
PubMed/NCBI
Google Scholar

[181] View Article

[182] PubMed/NCBI

[183] Google Scholar

[ref53] 53. Scott JG, Alefantis TG, Kaufman PE, Rutz DA. Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manage Sci. 2000;56(2):147–53.
View Article
Google Scholar

[185] View Article

[186] Google Scholar

[ref54] 54. Kivelä SM, Välimäki P, Carrasco D, Mäenpää MI, Oksanen J. Latitudinal insect body size clines revisited: a critical evaluation of the saw-tooth model. J Anim Ecol. 2011;80(6):1184–95. pmid:21605117
View Article
PubMed/NCBI
Google Scholar

[188] View Article

[189] PubMed/NCBI

[190] Google Scholar

[ref55] 55. Shirai Y. Temperature tolerance of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae) in tropical and temperate regions of Asia. Bull Entomol Res. 2000;90(4):357–64. pmid:11020794
View Article
PubMed/NCBI
Google Scholar

[192] View Article

[193] PubMed/NCBI

[194] Google Scholar

[ref56] 56. Honek A. Geographical variation in thermal requirements for insect development. Eur J Entomol. 2013;93(3):303–12.
View Article
Google Scholar

[196] View Article

[197] Google Scholar

[ref57] 57. Abbas N, Khan H, Shad SA. Cross-resistance, stability, and fitness cost of resistance to imidacloprid in Musca domestica L., (Diptera: Muscidae). Parasitol Res. 2015;114(1):247–55. Epub 2014/10/25. pmid:25342464.
View Article
PubMed/NCBI
Google Scholar

[199] View Article

[200] PubMed/NCBI

[201] Google Scholar

[ref58] 58. Abbas N, Shad SA, Razaq M. Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: Noctuidae). Pestic Biochem Physiol. 2012;103(3):181–8.
View Article
Google Scholar

[203] View Article

[204] Google Scholar

[ref59] 59. Zhang P, Zhao Y-H, Wang Q-H, Mu W, Liu F. Lethal and sublethal effects of the chitin synthesis inhibitor chlorfluazuron on Bradysia odoriphaga Yang and Zhang (Diptera: Sciaridae). Pestic Biochem Physiol. 2017;136:80–8. pmid:28187835
View Article
PubMed/NCBI
Google Scholar

[206] View Article

[207] PubMed/NCBI

[208] Google Scholar

[ref60] 60. Xiang X, Liu S, Wang X, Zhang Y, Gong C, Chen L, et al. Sublethal effects of sulfoxaflor on population projection and development of the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Crop Prot. 2019;120:97–102.
View Article
Google Scholar

[210] View Article

[211] Google Scholar

[ref61] 61. Yuan H-g, Wu S-y, Lei Z-r, Rondon SI, Gao Y-l. Sub-lethal effects of Beauveria bassiana (Balsamo) on field populations of the potato tuberworm Phthorimaea operculella Zeller in China. J Integr Agric. 2018;17(4):911–8.
View Article
Google Scholar

[213] View Article

[214] Google Scholar

[ref62] 62. Wang L, Zhang Y, Xie W, Wu Q, Wang S. Sublethal effects of spinetoram on the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Pestic Biochem Physiol. 2016;132:102–7. pmid:27521920
View Article
PubMed/NCBI
Google Scholar

[216] View Article

[217] PubMed/NCBI

[218] Google Scholar

[ref63] 63. Nazni WA, Luke H, Rozita WMW, Abdullah AG, Sa’diyah I, Azahari AH, et al. Determination of the flight range and dispersal of the house fly, Musca domestica (L.) using mark release recapture technique. Trop Biomed. 2005;22(1):53–61. pmid:16880754
View Article
PubMed/NCBI
Google Scholar

[220] View Article

[221] PubMed/NCBI

[222] Google Scholar

Figures

Abstract

Introduction

Materials and methods

Ethics approval

Collections of house fly populations

Laboratory rearing of house fly populations

Insecticides

Larval bioassays

Life table construction

Data analyses

Results

Resistance of M. domestica larvae to IGRs

Life history parameters of house flies from dairies

Demographic life table features of house flies from dairies

Age-stage-specific survival rates (sxj) of house flies from dairies

Age-specific survivorship (lx), fecundities (mx, fx), and maternity (lxmx) of house flies from dairies

Age-stage-specific reproductive values (vxj) of house flies from dairies

Age-stage-specific life expectancy (exj) of house flies from dairies

Correlation between IGR resistance ratios and life history features

Discussion

Supporting information

S1 File. Life table of Musca domestica population collected from Dirab, Saudi Arabia.

S2 File. Life table of Musca domestica population collected from Al-Masanie, Saudi Arabia.

S3 File. Life table of Musca domestica population collected from Al-Washlah, Saudi Arabia.

S4 File. Life table of Musca domestica population collected from Al-Uraija, Saudi Arabia.

S5 File. Life table of Musca domestica population collected from Al-Muzahmiya, Saudi Arabia.

Acknowledgments

References

Age-stage-specific survival rates (s_xj) of house flies from dairies

Age-specific survivorship (l_x), fecundities (m_x, f_x), and maternity (l_xm_x) of house flies from dairies

Age-stage-specific reproductive values (v_xj) of house flies from dairies

Age-stage-specific life expectancy (e_xj) of house flies from dairies