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Environ Anal Health Toxicol > Volume 37:2022 > Article
Khoobdel, Dehghan, Oshaghi, Saman, Asadi, and Yusuf: The different aspects of attractive toxic baits containing fipronil for control of the German cockroach (Blattella germanica)

Abstract

The use of Attractive Toxic Baits (ATBs) is considered to be a low-risk practical method for controlling cockroaches. This study evaluates the attractiveness of a lab-made, fipronil-containing bait, and its effect on the food consumption and mortality of the German cockroach Blattella germanica, under field and laboratory conditions. Different developmental stages of the cockroach were used to determine their preferred carbohydrate/protein rich foods and examine the effectiveness of lab-made baits. The analysis of variance (ANOVA) with Tukey’s Test was determined using SAS 9.1 and GraphPad Prism software programs. The significance level was considered at p<0.05. The most-consumed foods were carbohydrate-rich foods (biscuit and banana powder) and food consumption rate was highest in non-gravid females. The most attractive bait ingredients were 20% roasted peanut butter, 50% biscuit and 30% banana powder. The highest lethality was recorded from the baits containing 0.02% fipronil under laboratory conditions, while infested houses baited with the lab-made bait showed 76.5% and 100% decline, respectively, in cockroach numbers in the first- and fourth-week post-baiting. In conclusion, palatable foods with a pleasant odour, like biscuit powder, banana powder and peanut butter were the most effective ingredients for the ATBs. The ATBs impregnated with 0.02% fipronil provide a promising approach for control of the German cockroach. However, there is a need to evaluate the potentials of the lab-made baits, under laboratory and field conditions, in the control of other health-important cockroaches.

Introduction

The German cockroach, Blattella germanica (L.), a common health pest in public dwellings, is one of the most widespread health pests, due to its adaptability to diverse habitats and its ability to mechanically transmit pathogens. B. germanica has adapted well to different types of domestic buildings in both urban and rural settings [1,2]. In addition to transmitting pathogens and inducing psychological anxiety, B. germanica saliva, feces and sloughing body parts can be picked up in the air and can trigger both asthmatic attacks and allergies [310]. Cockroaches have been reported to carry as many as 78 different bacterial species, and B. germanica is reported to carry the widest diversity of bacterial species. In addition, the cockroach infestation of human habitats, especially homes, restaurants and hospitals, is on the increase [1,11,12].
Improper application of insecticides for the control of B. germanica has led to the development of pesticide resistance and failure of control programs, resulting in food and environmental contamination. Under such circumstances, different types of Attractive Toxic Bait (ATB) formulations, such as gels, pastes, and powders, are recommended as an alternative low toxic method, and as a common part of integrated pest management (IPM) in cockroach control programs [10,1316]. In the IPM programs, utilization of ATBs in low-toxic formulation could potentially be used to manage insecticide consumption in the infested dwellings [13].
In the last two decades, the production of new insecticides as active ingredients (a.i.s) of ATBs has made B. germanica control operations safer and easier. These insecticides include Fipronil, Hydramethylnon, Indoxacarb, Imidacloprid, Dinotofuran, Abamectin, and Boric Acid [1719]. Of these, Fipronil is a popular, common and highly effective insecticide used in commercial cockroach baits. Although different types of commercial baits are available in the world markets, the standard bait formulations are not available in the Iranian markets due to the economic sanctions. Therefore, we followed the production of a lab-made ATB and evaluated its efficacy under laboratory and field conditions.
The attractiveness, palatability and toxicity of active ingredients are the main factors influencing the efficacy of ATBs [7,20]. The attractive odor of the nutritional composition of the bait ingredients could be enhanced by the addition of insect allelochemicals, such as a sexual pheromone. In addition, the use of non-repellent active ingredients and the preferred composition and texture of the bait could promote the efficacy of ATBs in cockroach control programs [2126]. We have previously evaluated the attractiveness of various food types to B. germanica under laboratory conditions [26]. However, it is necessary to determine their consumption rate and its attractiveness when combined with various ingredients to produce a highly effective ATB formulation.
The feeding behavior and food preferences of cockroaches have been studied by many researchers [3,22,2428]. The reproductive needs of B. germanica affects the food preference, resulting in a sex-difference preference. In addition, variations in the consumption of different food items were reported between the male, gravid/non-gravid female, and nymphal stages of B. germanica [3,23,26,29]. Therefore, it is important that the composition of the toxic baits attracts the cockroaches and stimulates them to consume the bait. Low bait attractiveness will lead to a decrease in its efficiency in the cockroach control program; because in the infested field, with other food sources available, the pest will usually consume the first food it finds within the active period. In contrast, highly effective ATBs could attract and assemble the cockroaches to consume the bait even during the roach resting period in the daytime. In this regards, highly effective ATBs could dissuade the cockroach from consuming any other remaining foods in the infested places [26,29].
The attractiveness of commercial or lab-made bait, in combination with other behavioral characteristics of B. germanica, could be examined in the olfactometer; while the food preference can be measured by the degree of consumption of any nutrient [3]. This study aimed to 1) test the food preferences and food consumption rates of B. germanica at different developmental stages; 2) determine the attractiveness of a lab-made bait containing various percentages of active ingredients, using a modified olfactometer; and 3) evaluate the mortality rates of the exposed cockroaches to logarithmic concentrations of Fipronil under laboratory and field conditions.

Materials and Methods

Mass rearing of B. germanica

The B. germanica colony was established in the entomology laboratory of Yazd Science and Technology Park, Central Iran. The colony was established from specimens collected from infested houses in Yazd Province and reared under laboratory conditions. The specimens were reared in transparent plastic jars (300 mm height, 175 mm diameter). The laboratory conditions were 28+/−5 ºC, 50 +/− 5% relative humidity (RH), and a photoperiod of 12:12 h (light: dark). In order to prevent the escape of the cockroaches, the upper parts of the rearing jars (inner surfaces) were coated with a petroleum jelly-mineral oil mixture (2:3), (Henan Daken Chemical Comp). We prepared the shelter and the resting sites in the rearing jars from cardboard rolls. Also, the bottom of the rearing jar was covered with wet tissue paper and cotton. In addition, the water source of the cockroach was provided by a plate (2 cm in diameter) containing two-layer wet cotton. The cockroaches were fed weekly with a lab-made diet. The composition of the lab-made diets included baguette powder, peanut butter and milk powder (70/20/10 w/w/w), prepared by mixing the powders with butter in a small mixer under laboratory conditions.

The eight-choice radial olfactometer and trap

The eight-chamber apparatus (olfactometer) was constructed based on the one designed and described by Khoobdel et al [26]. The apparatus was designed to observe cockroach behavior without using a video check system. The apparatus was made from polystyrene and Plexiglas®, and contained two types of chamber, a primary main chamber for the release of all specimens at the beginning of the experiment, and eight small test chambers.

Evaluation of the foods

The consumption of seven foods, including baguette, potato, banana, and biscuit powders, as carbohydrate-rich foods; and raw peanut butter, roasted peanut butter and chicken liver powder, as protein-rich foods, were measured to determine the food preferences of the different developmental stages of B. germanica. The detailed process of preparing the foods in the powder/butter form has been described by Khoobdel et al [26].

Food preferences

The food preferences were evaluated by exposing the cockroaches to the different foods in plastic pans. Each experiment was carried out in a plastic pan (500 mm in diameter, 270 mm in height). Each pan was covered by a glass lid with a hole (20 mm diameter) in the center. In addition, the top 5 cm of each pan was coated with a petroleum jelly: mineral oil mixture (2:3) to prevent escape. A cardboard cylinder was used as a shelter in the center of the pan. A plate containing two-layer of wet cotton was used as a water source during the experiment. Each stage of the cockroach, including the non-gravid/gravid females, male, and nymph (4–5th instar) were released into the pans separately (with each experiment containing 100 specimens). The individuals were starved for 24hr prior to the release. The seven food types-baguette, potato, banana, biscuit, chicken liver powders, raw and roasted peanut butter were added to the plates. The net weight of the plate was 6220±25 mg. Each food sample was added to the plate to a final weight of 7500 mg. Five groups of plates were prepared from each sample (including 4 test groups and one control group). The control group included a pan with all the same conditions, but without the cockroach. Each plate containing ≈1250 mg food stuff was added randomly to the pans. The attractiveness and palatability of each food to the cockroaches was assessed, based on how much of it was consumed within 72hr of the start of the test. Finally, the plates of each group were weighed and the net weight of food consumed by the cockroaches was obtained using a Corrective Formula (CF). The experimental layout was performed in a factorial arrangement and in a completely randomized design. Each experiment was carried out in three replications using a fresh group of insects. At the end of each experiment, the pans were washed twice with distilled water.
The corrective formula was CF=CG-TG, where CG=weight of food-containing plate in the Control Group after 72hr, TG=weight of the food-containing plate in the Test Group after 72hr and CF=the net weight of food consumed after 72 hr.

Ingredients of the cockroach bait

Based on the attractiveness of the bait ingredients [26] and the bait tissue palatability according to food consumption-as determined by the present study-twelve lab-made baits were prepared (code B-1 to B12), containing baguette powder, peanut butter (roasted), biscuit powder, banana powder, and potato powder at different percentages. The changes were considered in the percentage of composition used in the lab-made bait formulation to analyze the effect of each of the foods in attracting the cockroaches to the bait (Table 1).

Cockroach bait attractiveness

The attractiveness of twelve lab-made baits (without insecticide) encoded B-1 to B-12 was tested using the olfactometer apparatus. The number of cockroaches attracted to each bait in the test chambers of the olfactometer were indicators of the attractiveness of each bait. The attractiveness tests were performed in two experimental groups. Each group was offered seven baits in 8 test chambers of the olfactometer, with one chamber acting as control (chamber without bait). We first compared the attractiveness of baits B-1, B-2, B-3, B-4, B-5, B-6, B-7 and control. In the second group we compared the attractiveness of baits B-8, B-9, B-10, B-11, B-12, control, and the least and most attractive baits determined in the first group (B-1 and B-7). We compared the lab-made baits to determine the effect of bait ingredient changes on the number of cockroaches they attracted. The bait attractiveness experiments were carried out using fresh specimens in each of the replications. The experimental layout was performed in three replications, completely randomized and in a factorial arrangement. We selected 90 cockroaches (30 adult males, 30 adult non-gravid females and 30 nymphs (4–5th instar)) and released them into the main chamber of the olfactometer and starved for 24hr. Each plate including 1.5 g of the bait was randomly placed inside each test chamber and one of the chambers was randomly selected as the control group (without any bait). The experiment was started by opening the main chamber containing the starved cockroaches. The cockroaches moved to the test chambers, gradually selecting the baits based on the attractiveness of their odors. The entrance valves of the test chambers were closed after 24hrs and the number of cockroaches in each of the test chambers was recorded (differentiated by their sex and developmental stages). At the end of each experiment, the olfactometer was cleaned and washed twice with distilled water.

Preparation of the cockroach ATB

The most attractive lab-made bait (according to the results from the experiments of the cockroach bait attractiveness), containing banana powder, biscuit powder and roasted peanut butter (30/50/20 w/w/w), was selected as the basis for the ATB. The ATB ingredients were mixed with fipronil powder (technical grade, Sigma-Aldrich) as the active ingredient at four different concentrations (w/w). The bait was mixed thoroughly in a small mixer.

Bait effectiveness under laboratory conditions

The separately lab-made ATBs, containing 0.01, 0.02, 0.04 and 0.08% of fipronil, respectively, were used to determine the mortality rate of each concentration under laboratory conditions. The mortality test was carried out in the plastic pans described above. In each pan, 20 cockroaches were released: consisting of 4 gravid adult females, 4 non-gravid adult females, 4 adult males, 4 early-emerged nymphs (small nymphs), and 4 late nymphs (large nymphs). Five pans were used in each of the experiment, including 4 tests and 1 control group. The released cockroaches in each pan were starved for 24hr and then exposed to lab-made baits and normal diet simultaneously for 24hr. Water was available to the cockroaches during the experiment. Finally, the live cockroaches in the pans were transferred to holding jars and maintained with normal food diet and water for 4 days and the cockroach mortality was recorded at the end of the experiment. The mortality experiment was carried out in 4 replications, using fresh groups of insects. At the end of each experiment, the pans were washed twice with distilled water.

Bait effectiveness in field conditions

Having shown its efficacy under laboratory conditions, we then wanted to evaluate the lab-made bait for its efficacy in eliminating cockroach infestation under field conditions. The field performance of the bait containing 0.02% fipronil (the concentration selected, based on the results of the laboratory study) was evaluated in seven randomly selected infested houses within 28 days in Yazd city, central Iran. One of the infested houses was randomly selected to serve as a negative control (no baiting). Baiting was performed using 50 to 75 g of the prepared bait, depending on the intensity of the infestation. The baits were applied to the corners of cabinets and underneath them, under the ovens, refrigerators, washing machines and sinks. Six sticky traps (Mouse and rat glue plank 21×16 mm) were used to monitor the changes in the cockroach numbers in each period. The traps were placed horizontally in the places mentioned above. The attractiveness of each trap was enhanced by pouring 1 g of the prepared bait in the middle of the sticky surface. Monitoring of the cockroach population was carried out at seven different time-points: 0 (before baiting), 2, 4, 7, 14, 21 and 28 days post-baiting in the treated and un-baited houses. The numbers of cockroaches were counted and recorded at each time-point, separately based on growth stage (small nymph, large nymph, and adult).

Data Analysis

The Normality test of the data was implemented on Minitab® Version 17.1.0 (Minitab 17, 2013). The analysis of variance (ANOVA) with the Honestly Significant Difference (HSD) or Tukey’s Test was determined using SAS 9.1 and GraphPad Prism software programs. The significance level was considered at p<0.05. The graphs were made using the Microsoft Excel ver. 2016 and the GraphPad Prism ver. 7.0.

Results

Food consumption

The highest food preference, measured by the rate of its consumption, was for foods with a carbohydrate-rich composition among all the development stages and sexes of B. germanica. Among the carbohydrate-rich foods, the most-consumed were the biscuit powder and banana powder, respectively, and the least-consumed food was potato powder, while of the protein-rich materials, un-roasted peanut butter and the chicken liver powder had, respectively, the highest and the lowest preference (Figure 1). Furthermore, we found that non-gravid females (female without ootheca) showed the highest food consumption of all the different developmental stages and sexes of B. germanica. The food consumption from more to less was non-gravid females>gravid females>nymphs>males respectively (Table 2).

The attractiveness of lab-made baits

The ANOVA analysis of the lab-made baits attractiveness showed significant differences between the sexes and the developmental stages of the specimens, and there was significant difference between different baits at p=0.01. In addition, the results of the interaction between sex/stages of the cockroach and the baits indicate significant differences at p=0.01 (Tables 3 and 4).
In order to prepare a bait with high attractiveness, formulations with different percentages of the ingredients were prepared and their attractiveness was determined by the modified olfactometer. The attractiveness of twelve formulations was compared in two experiments. The results of the first experiment showed that the B-1 bait was the most attractive, although the B-2 and B-3 baits were sorted in the same group and did not show significant difference in terms of attractiveness compared to B-1 bait. In the first experiment, the B-5, B-6 and B-7 baits, respectively, were found to be the least attractive, (Figure 2). In the second experiment, the attractiveness of the B-1 and B-7 baits (from the first experiment) was compared with that of the B-8, B-9, B-10, B-11 and B-12 baits. The results showed that B-10 bait was the most attractive and was significantly more attractive than the remaining baits. In this test, B-11 was the second most attractive bait, which significantly attracted more cockroaches than other baits. The baits that attracted the lowest number of cockroaches in the second experiment were B-12, B-9, B-8, B-1 and B-7, respectively (Figure 3).
Comparing the ingredients of B-2 with those of B-5 showed that decreasing the banana powder in B-5 decreases its attractiveness in a statistically significant manner, and likewise increasing the ratios of baguette or potato powder in B-5 also decreases the bait attractiveness. Comparison of B-1 with B-10 showed that increasing the roasted peanut butter, while deleting the baguette and potato powder, significantly increased bait attractiveness. In addition, comparing B-10 with B-11 showed that decreasing the roasted peanut butter and increasing the biscuit powder significantly reduced attractiveness. Comparing B-10 with B-12 showed that decreasing roasted peanut butter and increasing banana powder significantly lowered the bait attractiveness (Table 5).
Comparison of the bait attractiveness between the sexes and developmental stages of the cockroaches in the first experiment showed the adults (male and female) were most attracted to the bait; while in the second experiment, the males were significantly more attracted to the bait than the females or nymphal stages.
Comparing the bait attractiveness for different sex/developmental stages of the cockroaches in the first experiment showed that females were most attracted to B-1, while the males preferred B-2 to B-1. In the second experiment we found that all categories of cockroach were most attracted to B-10 bait.

Cockroach mortality under laboratory conditions

The mortality of the cockroaches increased with increasing doses of fipronil. B. germanica mortality was 78.7% and 97.5% at 0.01% and 0.02% fipronil concentrations, respectively. The cockroaches mortality induced by the baits containing 0.04% and 0.08% fipronil were 93.8% and 96.2%, respectively, which are slightly lower than the mortality observed at 0.02% concentration. This may suggest that higher concentrations of the fipronil reduce the attractiveness of the bait. The developmental stage most susceptible to fipronil was the larger male nymphs, while the least susceptible stage was the non-gravid female (Table 6).

The bait efficiency in the field

The effect of the fipronil containing 0.02% w/w insecticide bait was evaluated under field conditions. The analysis of variance indicates significant differences in the trends of decreasing cockroach number in the baited houses in the days post-baiting (p<0.01), (Table 7), although the overall results show considerable effectiveness in eliminating cockroach infestation in the treated dwellings. After one week of baiting, we recorded a mortality of 76.5% in the baited houses. The number of cockroaches had declined significantly and reached zero in most of the houses by the end of the fourth week. The cockroach monitoring showed a sharp fall in the mean, from 41.5 to 9.86 per sticky trap, seven days post baiting and this number gradually decreased to 0.36 per sticky trap by the end of the fourth week (Figure 4).

Discussion

The utility of highly effective ATBs is very applicable in integrated cockroach management [10,13,15], and in this study we have determined the most effective formulation for combatting B. germanica infestations.
First, we evaluated the preferences of B. germanica for seven carbohydrate-rich or protein-rich food ingredients, by determining the consumption rate of the foods by the different developmental stages of the cockroach, in order to determine which to use as bait ingredients. Then, using this information, we formulated twelve lab-made baits with different percentages of attractive ingredients, and tasted them to determine the most attractive formulation as ATB. The results of the study showed B. germanica has a strong preference for carbohydrate-rich foods such as biscuit and banana, while protein-rich ingredients, especially unroasted peanut butter and chicken liver powder, were the least attractive.
In contrast, Jensen et al. [30] (2021) cited the male German cockroaches actively select a more protein-biased diet. They demonstrated adult male German cockroaches actively respond to a high frequency of mating opportunities by increasing protein consumption [30]. The researchers mentioned the cockroach nutritional requirements not only had been differing in cockroach life/sex stages, but also it was changed in different conditions and physiological stages [3,3032]. Generally, it is important to target all life stages of cockroach in control program; therefore, we tested the bait formulation with various protein and carbohydrate contents on different cockroach life/sex stages to determine the most attractive and the most consumed bait ingredients.
The present study has introduced a lab-made ATB containing highly attractive and palatable ingredients for the control of B. germanica. Previous work has shown that the attractiveness of the ATB is higher than that of leftover foods to feed on [26]. It is probable that carbohydrate-rich foods are considered to be the primary energy source by both sexes of cockroach because of their inability to convert lipids to monosaccharides [3,26,33].
It is clear that the cockroach population in the field must contain a combination of developmental life stages and sexes, hence it is very important to consider a mixture of different attractive ingredients to achieve the maximum efficacy. These differences are according to the dietary requirements of the developmental stage and physiological/sex status of B. germanica [34]. In a previous study, Khoobdel et al. [26] (2020) determined which materials are the most attractive for B. germanica, but it is very important that the attracted cockroaches also consume the foods in order to also ingest the active ingredient [26]. This feature has been investigated in the present study with protein and carbohydrate rich foods for males, non-gravid females, gravid females and nymphal stages of the German cockroach. We determined that both gravid and non-gravid adult females ate the most, whereas the male and the nymph cockroaches of both sexes ate much less. It is known that female fecundity, and especially egg development, depend on high ingestion of carbohydrate and protein materials whereas for the male cockroaches, a small amount of food is enough for metabolism and daily activity [33]. In addition, the size and weight of the male German cockroach is significantly different than the female [31].
In order to develop a highly effective bait, a combination of developmental stages and sexes of B. germanica were used to evaluate the food consumption rates and the attractiveness of lab-made baits. This resembled the pattern of the cockroach population in the field and we judged it more conducive to indicating which would be the most efficacious bait in the field. In this regard, the final lab-made bait formulation developed in this study could control B. germanica infestations in the field. Utilization of highly effective toxic bait in cockroach control programmes has many advantages, including the targeted use of insecticides and reduced insecticide use, leading to less environmental contamination and no irritant odour; more effective and low-risk pest control measures; greater ease of use and more time-saving, as there is no need to empty cabinets or move equipment; no contamination of the equipment or cabinets with insecticide; and, finally, more customer satisfaction in using the baiting method [10,35,36].
Interestingly, the results of our food consumption analysis showed that very little peanut butter, especially the roasted form, was eaten, although Khoobdel et al. [26] (2020) had reported that the odour of peanut butter, especially the roasted type, significantly attracted the German cockroaches [26]. Thus, the odour of roasted peanut could dramatically enhance bait attractiveness (Table 5) but did not enhance the bait consumption rate [27]. Ibrahim et al. [27] (2017), also reported that roasted peanut was highly attractive to both male and female cockroaches [27], but suggested that a mixture of roasted peanut, fresh coriander leaves, zucchini fruit and coriander oil attracted even more cockroaches than peanut butter [27]. Thus, bait attractiveness could potentially be further enhanced by including these odours.
In contrast to the peanut butter, the banana and biscuit powders were found to be the most preferred food for B. germanicus, and the biscuit powder used in the present research also has an attractive odor. We found the B-10 formulation (20% roasted peanut butter, 50% biscuit and 30% banana powder) to be the most attractive of the lab-made bait formulations. We also concluded that it is necessary to use at least 20% of roasted peanut butter, as an attractant rather than as food, to produce a highly attractive bait. When we reduced the roasted peanut butter from 20% to 5% in B-11, the attractiveness was significantly reduced in comparison with B-10. Khoobdel et al. [26] (2020) found that increasing the concentration of fipronil from 0.01% to 0.08% fipronil caused a significant repellent effect. In the present study, the baits containing 0.2%, 0.04% and 0.08% fipronil showed the same lethality rate in the laboratory. Hence, 0.02% is recommended as an ideal concentration for an active ingredient in evaluating bait efficacy in the field.
Fipronil can kill cockroaches in milligram concentrations, but the time taken to eradicate the cockroaches in a control program is very important, and this affects the efficiency requirements of a bait formulation. It is essential that cockroaches receive a lethal dose of insecticide from the first bait consumption to minimize the development of resistance, which is a problem arising with insecticides used by residual spray [37,38]. The second advantage of ATBs is that the cockroaches are stimulated to emerge from their shelters by the attractive odour of the bait, which then stimulates cockroaches to consume it; while it is not always possible to access the cockroach shelters to apply the insecticide using the residual spraying methods [39].
Different bait formulations have been produced by reputable companies worldwide, and their effectiveness have been proven in cockroach control programs. Among them, gel formulations are the most popular. Powder formulation, with its loose and acceptable texture and pleasant odour is very effective. However, in infested environments that are washed daily, the use of this type of bait is associated with limitations [37]. The present study showed the lab-made powder bait is highly efficient in both lab and field conditions.
Different baits, depending on the active ingredients, attractive ingredients, and the type of formulation, have shown a variety of efficiencies under field conditions [40]. Savoldelli et al. [40] (2005), reported 67.5%, 82.5%, 37.5%, 47.5%, and 72.5% mortality of the brown banded cockroach exposed to hydramethylnon 1.8%, hydramethylnon 2%, imidacloprid 2.15%, fipronil 0.03% and fipronil 0.05% gel baits respectively [37]. The gel bait containing 2% hydramethylnon (Infiniti ®) reduced German cockroach numbers by more than 95% in less than one week in Thailand [17]. In another study, a gel containing 2.15% imidacloprid (Bayer, Shawnee Mission, KS) reduced the number of cockroaches trapped in a sticky trap by 50% and 80% in the first and fourth week, respectively [18]. The control of B. germanica by fipronil gel 0.05% and imidacloprid gel 2.15% reduced the pest number to zero in less than nine weeks in three infested dwellings in Tehran [36]. In another study, the lethality of novaflumerone-containing gel (which has an inhibitory effect on chitin synthesis in B. germanica nymphs) was more than 90% on the eleventh and nineteenth days after exposure, respectively. The lab-made baits containing 0.02% fipronil that we examined in the present study showed 97.5% mortality, which compares well with the commercial formulations in both lab and field conditions, with the cockroach number decreasing to 76.5% at the end of the first week and reaching zero in most of the infested houses at the end of the fourth week.
It is worth mentioning that the known commercial ATB formulations for cockroach control, such as Goliath®, Maxforce®, and Siege®, are not available in Iran because of the economic sanctions. Therefore, the ATBs used could not be compared with the standard ones. Moreover, results of this study will help in the production and utilization of highly effective domestic ATBs in Iran.
Cockroaches consume the bait as a food source, so removing other cockroach food sources could help to achieve the pest control faster. Also, the use of insecticides or repellent materials in the same place could affect the bait efficiency. It is recommended that the maximum amount of bait should be used in the hidden gathering places of cockroaches, where the sticky traps have trapped most cockroaches, or the cast-off skins or excreta of cockroaches and egg ootheca have been dumped. The bait should be utilized mostly near cracks in walls; in cabinet corners; underneath and behind refrigerators, stoves, washing machines, and other kitchen equipment; near wooden furnishings, such as tables, door frames, and the hinges of wooden doors; inside aluminum dish stores; and inside power cable ducts [10,14,15,41].

Conclusions

In conclusion, the inclusion of ingredients with strong and pleasant odor, as well as a palatable texture, such as banana, biscuits and roasted peanut butter, are appropriate for use as attractants in the formulation of 0.02% fipronil-containing ATBs against different developmental stages and sexes of the German cockroach.

Acknowledgement

We would like to thank the Biotechnology Development Center in Yazd Science and the staff of Technology Park for the help of their private entomology laboratory, especially Eng. Abbas Baghi. This research was supported by the Health Research Center, Baqiyatallah University of Medical Sciences (code no: 95-09-001020). We are grateful to Dr. Farhad Saravani for editing of the manuscript. Also, we are grateful to Dr. Miranda Thomas from ICGEB for her insightful suggestions and careful editing of the manuscript.

Conflict of interest

Conflict of interest
There are no conflicts of interest in the manuscript and the manuscript is approved by all authors for publication.

Notes

CRediT author statement
MK: Supervision; HD: Conceptualization, Methodology, Investigation, Writing-Original draft Preparation; MAO: Writing-Reviewing & Editing; EAGS: Visualization, Investigation; AA: Software; MAY: Writing-Reviewing & Editing.

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Figure 1
The mean food consumption (g) by the German cockroaches. The error bars indicate S.E.
eaht-37-4-e2022032f1.jpg
Figure 2
The mean frequency of the attracted German cockroach to different formulation of the lab-made baits using modified olfactometer (experiment 1). The error bars indicate the S.E. (Tukey’ HSD; p≤ 0.05).
eaht-37-4-e2022032f2.jpg
Figure 3
The mean frequency of the attracted German cockroach to different formulation of the lab-made baits using the modified olfactometer (experiment 2). The error bars indicate S.E. (Tukey’ HSD; p≤ 0.05).
eaht-37-4-e2022032f3.jpg
Figure 4
The effect of the lab-made attractive toxic baits (0.02% Fipronil, 30% banana powder, 50% biscuit powder and 20% roasted peanut) on German cockroach population throughout four weeks in the infested houses in Yazd County, central Iran. The vertical axis indicates the number of the trapped cockroaches/infested house/six sticky traps.
eaht-37-4-e2022032f4.jpg
Table 1
Percentage composition of the different ingredients used in the man-made bait formulations against the German cockroaches.
Bait ingredient B-1 B-2 B-3 B-4 B-5 B-6 B-7 B-8 B-9 B-10 B-11 B-12
Baguette Powder 5 5 5 5 15 20 20 10 0 0 0 0
Peanut butter (roasted) 10 10 20 20 10 10 10 10 10 20 5 5
Biscuit powder 50 30 25 45 30 25 35 50 50 50 65 50
Banana powder 30 50 45 25 30 25 15 30 30 30 30 45
Potato powder 5 5 5 5 15 20 20 0 10 0 0 0
Total 100 100 100 100 100 100 100 100 100 100 100 100
Table 2
The German cockroach food consumption at different developmental stages and sexes.
N.G. female* G. female** Male Nymph
Mean 0.123 0.118 0.064 0.073
S.D of mean 0.0796 0.116 0.037 0.062
Minimum 0.016 0.027 0 0.013
Maximum 0.245 0.359 0.111 0.162
Sum 0.858 0.828 0.448 0.513

* Non-Gravid adult females.

** Gravid adult females.

Table 3
The variance analysis of the attracted non-gravid female, male and nymph of the German cockroaches to man-made baits encoded as B-1, B-2, B-3, B-4, B-5, B-6, and B-7 containing various percentage of the ingredients (baguette powder, potato puree, banana powder, biscuit powder and roasted Peanut butter) using 8-choice radial olfactometer.
SOV DF MS
Sex/Stages 2 9.39**
baits 7 48.73**
Sex/Stages×baits 14 5.04**
Error 48 1.05
CV 30.32

** p value<0.01,

CV: coefficient of variation, SOV: source of variations, MS: Mean of the squares, DF: degrees of freedom.

Table 4
The variance analysis of the attracted non-gravid female, male and nymph of the German cockroaches to man-made baits encoded as B-1, B-7, B-8, B-9, B-10, B-11, and B-12 containing different percentage of ingredient (baguette powder, potato puree, banana powder, biscuit powder and roasted Peanut butter) using 8-choice radial olfactometer.
SOV DF MS
Sex/Stages 2 11.76**
baits 7 104.18**
Sex/Stages× baits 14 4.75**
Error 48 1.04
CV 31.95

** p value<0.01,

CV: coefficient of variation; SOV: source of variations; MS: Mean of the squares; DF: degrees of freedom.

Table 5
The comparison of man-made baits and interpretation of ingredient changes in two experiments using 8-choice radial olfactometer.
Experiments The baits comparation Objectives The baits attractiveness Interpretation

Reduce Increase
Experiment I B-1 with B-2 Reducing biscuit powder and increasing banana powder × -
B-2 with B-3 Reducing biscuit and banana powders and increasing roasted peanut butter × -
B-2 with B-5 Reducing banana powder and increasing baguette and potato powder * × Reducing the banana powder decreases attractiveness statistically significant while increasing the baguette and potato powder could decrease the bait attractiveness.
B-3 with B-4 Reducing banana powder and increasing biscuit powder × -
B-5 with B-6 Reducing biscuit and banana powder and increasing baguette and potato powder × -
B-6 with B-7 Reducing biscuit powder and increasing banana powder × -
Experiment II B-1 with B-8 increasing baguette powder and deleting potato powder × -
B-1 with B-9 Increasing potato powder and deleting baguette powder × -
B-1 with B-10 increasing roasted peanut butter and deleting baguette and potato powder × * Increasing the roasted peanut butter and at the same time deleting the baguette and potato powder statistically significant raised the bait attractiveness.
B-10 with B-11 Reducing roasted peanut butter and increasing biscuit powder * × Decreasing the roasted peanut butter and at the same time increasing the biscuit powder statistically significant decline the bait attractiveness.
B-10 with B-12 Reducing roasted peanut butter and increasing banana powder * × Decreasing the roasted peanut butter and at the same time increasing the banana powder statistically significant decline the bait attractiveness.

* statistically significant difference p≤ 0.05.

1 Tables may have a footnote.

Table 6
The German cockroach mortality rates (Mean±SE) exposed to baits containing four different fipronil concentrations at different developmental stages under laboratory condition (based on Tukey’s test p<0.05).
Treatments in logarithmic concentrations Mean (±S.D)*

Adult female Adult male Nymphal stages Sum


Gravid non-gravid Large nymph Small nymph
T 0.01 81.2(±23.93) a 62.5(±14.43) a 81.2(±12.5) b 75(±20.41) a 93.7(±12.5) a 78.7(±11.33) b
T 0.02 100(±0.00) a 87.5(±14.43) a 100(±0.00) a 100(±0.00) a 100(±0.00) a 97.5(±5.59) a
T 0.04 93.7(±12.50) a 81.2(±12.5) a 100(±0.00) a 93.7(±12.5) a 100(±0.00) a 93.8(±7.67) a
T 0.08 100(±0.00) a 87.5(±14.43) a 100(±0.00) a 93.7(±12.5) a 100(±0.00) a 96.2(±5.59) a
CONT 0 b 0 b 0 c 0 b 0 b 0 c

* Means followed by the same letters are not significantly different.

Table 7
The variance analysis of the German cockroach number (small nymph, large nymph and Adult) in infested houses after baiting with attractive toxic baits (0.02% Fipronil, 30% banana powder, 50% biscuit powder and 20% roasted peanut) for four weeks (0th, 2th, 4th, 7th, 14th, 2th, 28th).
SOV DF MS
Stages 2 262.2**
Days 7 466.9**
Stages× days 14 12N.S
Error 123 31.45
CV 89.6

N.S: non-significant,

** p value<0.05,

CV: coefficient of variation, SOV: source of variations, MS: Mean of the squares, DF: degrees of freedom

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