Next Article in Journal
Navigational Signals for Insect and Slug Parasitic Nematodes: The Role of Ascorbate–Glutathione System and Volatiles Released by Insect-Damaged Sweet Pepper Roots
Previous Article in Journal
Functional Response of Four Phytoseiid Mites to Eggs and First-Instar Larvae of Western Flower Thrips, Frankliniella occidentalis
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 15
Issue 10
10.3390/insects15100804
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Sublethal Effects of α-Cypermethrin on the Behavioral Asymmetries and Mating Success of Alphitobius diaperinus

by
Demeter Lorentha S. Gidari
,
Nickolas G. Kavallieratos
* and
Maria C. Boukouvala
Laboratory of Agricultural Zoology and Entomology, Faculty of Crop Science, Agricultural University of Athens, 75 Iera Odos Str., 11855 Athens, Greece
*
Author to whom correspondence should be addressed.
Insects 2024, 15(10), 804; https://doi.org/10.3390/insects15100804
Submission received: 12 September 2024 / Revised: 4 October 2024 / Accepted: 8 October 2024 / Published: 15 October 2024
(This article belongs to the Section Insect Pest and Vector Management)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

This study investigated the behavioral asymmetries and mating success of Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae) under sublethal exposures to α-cypermethrin. Control males exhibited a right-side bias, which increased the likelihood of successful copulation, especially when head butts preceded mounting. A similar pattern was observed for LC10-exposed males, though their success rate slightly declined. In females, the right-side approach also enhanced copulation success. The direction of approach and mounting influenced the time required for key mating behaviors like mate detection and mounting. Males exposed to LC30 of α-cypermethrin needed a longer time for mate detection compared to control and LC10, especially when approaching from the back or front side. Females of the LC30 group were also influenced, with shorter copulation times when approaching from the right. These findings demonstrate that α-cypermethrin affects both mating success and the duration of related behaviors.

Abstract

Sublethal exposure to insecticides can adversely impact various biological and behavioral characteristics of insects. Although α-cypermethrin has been previously tested for its effects on control of Alphitobius diaperinus, there is no knowledge about the effect of this insecticide on its behavioral asymmetries and mating success. Μales at all exposures (control, LC10, and LC30), that first approached their mate, showed right-biased tendency (approached their mate from their right side) in mate recognition. Females, however, showed variation in this behavior between the three exposures. Right-biased tendency of males in all treatment scenarios led to a higher percentage of successful copulations compared to the three other directions. For males that first approached their mate, the insecticide did not affect their lateralization of the first approach but did affect their copulation success. The duration of copulation time was reduced after the exposure to the insecticide, with the longest duration noted in the control females (63.0 s) and the lowest in the α-cypermethrin LC30 females (46.9 s). Moreover, at the α-cypermethrin LC10 exposure, mate recognition time was reduced, as opposed to α-cypermethrin LC30 exposure where mate recognition time was increased. These results can be further utilized to uncover the behavioral impacts of insecticides, enhancing the effectiveness of pest management in warehouses and poultry production facilities.

Graphical Abstract

1. Introduction

Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae) is a key species in poultry production and storage facilities [1], as a vector of many dangerous pathogens, such as Escherichia coli, turkey coronavirus, Marek’s disease, Salmonella typhimurium, and avian leukemia [2,3,4]. These pathogens can also affect humans and cause symptoms such as gastrointestinal disorders and fever [5,6]. The ability of A. diaperinus to cause allergic reactions to people who come into frequent contact with this species has also been observed [7]. In intensive poultry production, populations of A. diaperinus can reach extremely high levels. For example, around 34.7 million A. diaperinus adults, nymphs, and larvae may exist in a poultry production facility [8]. Alphitobius diaperinus is a secondary pest of grains, e.g., wheat, rye, barley, flour, bran, and hay [9]. So far, numerous insecticides (both natural and synthetic) have been employed to control A. diaperinus larvae or adults [10,11,12,13,14,15,16,17,18].
α-Cypermethrin, a non-systemic pyrethroid (type II) insecticide, is effective through contact and ingestion. It consists of the active isomer of cypermethrin and is highly efficient against a wide range of insect species, e.g., mosquitoes, flies, and other pests commonly found in animal and public housing [19,20,21]. When used according to recommended guidelines and application rates, α-cypermethrin is safe for the general public, occupational exposure, and the environment [22,23]. Despite its efficiency, excessive reliance on α-cypermethrin has led to the development of resistance in various insect pests worldwide [24,25]. This resistance has necessitated higher concentrations, thus increasing control costs and causing negative impacts to the environment and public health [26,27,28]. In addition to causing death in storage insects, synthetic insecticides also produce sublethal effects that can affect their biology and behavior [29,30]. These sublethal effects may include aggressive behavior and adverse impacts on lifespan, fertility, fecundity, courtship, movement, or physical structure [31,32].
Brain lateralization, which refers to the differences in structures and functions between the left and right side of the brain, can improve its capacity to perform cognitive tasks by simultaneously engaging both hemispheres in distinct ways [33]. Lateralization has been investigated in many vertebrates [34,35,36,37,38,39,40,41,42], but in invertebrates and especially insects the knowledge related to this topic is low, except bees [43,44,45,46,47]. Recent studies have concentrated on the laterality behavior of species in the order Coleoptera during mating and courtship, with a particular emphasis on pests of stored products, i.e., Dermestidae, Bostrychidae, Tenebrionidae, Laemophloeidae, Curculionidae, and Silvanidae [48,49,50,51,52,53,54,55]. For A. diaperinus, there is limited knowledge about mating behavior and laterality [56,57,58]. Renault [56] revealed that the reproduction success of cold-acclimated A. diaperinus adults was superior to that of non-acclimated individuals. Moreover, it is already known that prior sexual experience enables A. diaperinus to choose potential mates. Calla-Quispe et al. [57] showed that virgin female adults were significantly more attracted to virgin male adults, while sexually experienced female adults were significantly more attracted to sexually experienced male adults. Although there have beenare former studies of the efficacy of α-cypermethrin against A. diaperinus [59], there are no data on the effects of its sublethal concentrations on A. diaperinus mating behavior. Therefore, this research piece is focused on assessing the effects of LC10 and LC30 of α-cypermethrin on A. diaperinus asymmetries and mating success.

2. Materials and Methods

2.1. Alphitobius diaperinus Colonies

Female and male A. diaperinus adults were collected from cultures maintained in a mass-rearing facility at the Laboratory of Agricultural Zoology and Entomology, Athens, Greece. The beetles were maintained in continuous darkness, 65% relative humidity (RH), and 30 °C [60]. As a rearing medium, wheat bran and yeast (75% and 25%, respectively), adding apple slices for additional moisture, were used [61].

2.2. Sex Recognition

Recognition of males and females was conducted at the pupal stage according to the description of Esquivel et al. [62]. Afterward, pupae of the same age and sex were separately kept under the same conditions, until the beginning of the observations.

2.3. Insecticide

For the experiment, the insecticide used was Fendona Top SC (provided by BASF Hellas, Amarousion, Greece). This insecticide contains 1.58% w/w α-cypermethrin active ingredient (a.i.).

2.4. Insecticide Contact Toxicity Bioassays

LC10, LC30, or LC50 of α-cypermethrin were determined by impregnating separate pieces of filter paper (Whatman No. 1) with various amounts of the insecticide. This paper was cut in a circular shape to fit in the bottom of the Petri dishes, which had an area of 50.27 cm2. A series of α-cypermethrin solutions (0.11, 0.055, 0.0366, 0.0275, and 0.022 mg/cm) in water were prepared. Next, a micropipette was used to spread 1 mL of each α-cypermethrin solution on a different piece of filter paper. Petri dishes with impregnated filter papers were left to dry at 30 °C for 2 h. The same procedure was used to impregnate the control filter papers, with 1 mL distilled water. Within each dish that had been treated with the respective concentration of α-cypermethrin (five dishes per concentration), 20 adults of A. diaperinus were released. All dishes remained in continuous darkness in incubators set at 65% RH and 30 °C for 24 h. After that period, the number of dead adults was counted. The aforementioned protocol was repeated twice for both the insecticide and the control. Before starting the behavioral experiments, male and female individuals underwent a 24 h exposure to α-cypermethrin LC10 and LC30 values, under the same procedure as described above.

2.5. Behavioral Experiments

Virgin mature A. diaperinus males and females from the control and the group exposed to α-cypermethrin were used. For the observations, a Petri dish arena was used (height: 2 cm and ⌀: 10 cm). A wall made of filter paper was placed around the arena to prohibit any visual signals by the person monitoring the experiments, which may affect the insects’ behavior during observations [48]. Before starting each observation, all individuals were exposed for three hours to the natural conditions of light, which is a sufficient interval for the adjustment of the beetles, as mentioned in previous studies of various stored-products species [49,50,51,52,53,54]. Then, two α-cypermethrin LC10-exposed adults of different sexes were introduced in the arena for visual observation of their sexual interaction for 60 min or until the termination of the copulation [49]. During the sexual interaction, if any, the following phases were recorded: (i) time of mate recognition (i.e., the duration from the transfer of the pair to the arena until the male locates the female or conversely), (ii) precopulation (i.e., the time during which the male mounts the female to perform copulation), (iii) copulation success (i.e., the duration from genital contact till genital disengagement), and (iv) total duration of the sexual interaction [48,51,53]. It was also investigated: whether the individual that first approached its mate was male or female and the side of the mate that was first approached (i.e., male or female first approached its mate from the back, front, left, or right side); whether the individuals (male and female) performed headbutts and from which side (back, front, right, or left) the male mounted the female. The same procedure was followed for the control and A. diaperinus males and females exposed to α-cypermethrin LC30. The numbers of tested pairs of α-cypermethrin LC10, LC30, and control A. diaperinus were 130, 153, and 110 respectively. Pairs that were in proximity to the walls of the arena or did not show any copulation activity for 60 min were discarded [55].

2.6. Statistical Analysis

The values of α-cypermethrin that kill 10, 30, and 50% of the exposed individuals, LC10, LC30, and LC50 respectively, were evaluated, with a 95% confidence interval (CI), using probit analysis [63] and the R statistical software (version 2.15.1) [64]. Data analysis of the laterality behavior of A. diaperinus was run with the software JMP 16.2 [65]. The effect of orientation when approaching a mate and the lateralization of mounting on the duration of the main behavioral mating traits (mate recognition, mounting, and copula) did not follow a normal distribution and were analyzed using the Steel–Dwass test with a significance level of α = 0.05 [51,53].

3. Results

3.1. Contact Toxicity on A. diaperinus

Insecticide contact toxicity bioassays revealed that LC10, LC30, and LC50 for A. diaperinus were 0.0000666, 0.000120, and 0.000180 mg a.i. cm−2, respectively (Table 1).

3.2. Impact of α-Cypermethrin on A. diaperinus Mating Behavior and Laterality

The majority of the control males that first approached their mates showed a right-side tendency (38.6% out of 100%). Most of these performed head butts (24.3% out of 38.6%) and 12.9% out of 24.3% of males mounted the females from the left side of their bodies, achieving successful copulations (Figure 1).
Most of the control females that approached their mates first exhibited a back-side tendency (40% out of 100%). Half of these (20% out of 40%) performed head butts. A 7.5% out of 20% that performed head butts were mounted by the males from their right side, achieving successful copulations. A 10% out of 20% of females that did not perform head butts were mounted by the males from their left side, achieving successful copulations (Figure 2).
A similar pattern to that in the control male group was recorded for α-cypermethrin LC10-exposed males that approached their mates first. A 48% out of 100% approached the females from the right side. Almost all of these (43.9% out of 48%) performed head butts. A percentage of 21.4% out of 43.9% mounted the female individuals from their left side, with 16.3% out of 21.4% performing successful copulations. The same percentage of males (i.e., 21.4% out of 43.9%) mounted the females from their right side, achieving 16.3% out of 21.4% mating success (Figure 3).
For females exposed to α-cypermethrin LC10 that approached their mates first, 34.4% out of 100% exhibited a right-side tendency and performed head butts. A percentage of 18.8% out of 34.4% of females were mounted by males from their left side, with 15.6% out of 18.8% performing successful copulations. Fewer females were mounted by males from their right side (15.6% out of 34.4%), achieving only 9.4% out of 15.6% successful mating. (Figure 4).
As in the two previous cases (LC10 and control), α-cypermethrin LC30 exposure revealed right-biased tendency (42% out of 100%) for males that approached their mates first. Most of them performed head butts (33.3% out of 42%) and the 20.3% out of this 33.3% mounted females from their right side, with 16% out of this 20.3% achieving successful copulations. The remaining 13% out of 33.3% of males mounted females from their left side, leading to 8.7% out of 13% achieving successful copulations (Figure 5).
α-Cypermethrin LC30-exposed females that approached their mates first showed left-biased tendency in 45% out of 100% and the majority of them performed head butts (40% out of 45%). The 23.3% out of 40% were mounted by the males from their left side, leading to 13.3% out of 23.3% successful copulations (Figure 6).
The duration of mating traits of A. diaperinus was significantly influenced by the laterality of direction of the first approach and mounting side in all three exposures (control, LC10, and LC30) (Table 2, Table 3, Table 4 and Table 5). Regarding the effect of the side from which males first approached their mates on the mating traits of A. diaperinus, the mate detection duration was significantly higher for all directions of the LC30-exposed males and for left-biased control males (338.4 s for back-, 435.6 s for front-, 366.3 s for left-, and 355.4 s for right-biased male individuals of the LC30 exposure and 303.0 s for the left-biased male individuals of the control group, respectively). The shortest mate detection was observed in the back-biased control males (46.1 s) (Table 2).
The effect of the approaching side, when females approached their mates first, caused the lowest and the highest duration of copulation, 46.9 s for the right-biased females exposed to the LC30 and 63.0 s for the right-biased females of the control group (Table 3).
This laterality aspect also affected the time needed for the mounting, with the left-biased male individuals of the control group achieving the lowest times of all scenarios tested (287.5 s) (Table 3). In contrast, mounting side laterality, when males approached their mate first, caused the highest time needed for mounting (2139.3 s) in the back-biased males of the LC30 exposure (Table 4).
For the LC30-exposed males, no front-biased mating traits were recorded, and this was also the case for the copulation direction of the LC10 exposed males. Τhe shortest mate detection (15.5 s) was noted in the front-biased females of the control group when they approached their mates first (Table 5). This laterality aspect did not result in any front-biased mating trait for either LC10 or LC30 exposure.

4. Discussion

To date, there has been just one study on the lateralization of A. diaperinus mating behavior [58]. The authors examined how directional displacement during the mating behavior of a Peruvian strain (specifically, movements that were either lateralized or non-lateralized) affected both mating success (defined as the occurrence of copulation) and efficiency (measured by the time taken to achieve copulation). The fact that virgin males and females from the Peruvian strain did not show any lateralized approaches in contrast to the tested Greek strain, where males of all exposures showed a right-biased first approach and left-biased mounting approach and females a variety of lateral approaches, is probably due to the different geographical origins. The influence of the geographical origin was also reported in behavioral experiments on Turkish and Czech strains of Trogoderma granarium Everts (Coleoptera: Dermestidae), where a higher percentage of males of the Czech strain approached females from the left (53%), while Turkish-strain males exhibited a preference for approaching females from the right (50%) [55].
The findings of this research indicate that laterality significantly influenced the mating success of A. diaperinus. Males that first approached their mates from their right side accomplished the highest percentage of successful copulations vs. males that first approached their mates from a different side. Previous studies related to tenebrionids have reported a left-biased tendency. Tenebrio molitor L. (Coleoptera: Tenebrionidae) displayed a left-biased preference in recognition and mounting attempts to potential mates which resulted in higher copulation success compared to males that showed a right-side bias [52]. The same tendency was also reported for Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) and T. confusum Jacquelin du Val [48,50]. Earlier studies on other coleopteran families found that right-biased males achieved higher mating success vs. left-biased males. For instance, strains of Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) from three countries (Greece, Romania, and Turkey) demonstrated a preference for right-sided mating, leading to a greater success rate in copulation compared to left-sided and back-side-approaching male individuals [51]. Likewise, Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae) males exhibited a tendency to initiate mating attempts from the right side of female individuals, resulting in higher rates of successful mating compared to left-sided males [53]. However, there are several studies with opposite results, where other stored-product coleopteran pests revealed a left-biased tendency. For example, Romano et al. [48] revealed that Sitophilus oryzae (L.) (Coleoptera: Curculionidae) males displayed a preference for left-sided copulation attempts towards potential mates, followed by periodic head wagging biased towards the right. This behavior persisted despite the majority of males initially attempting left-sided copulations.
Based on previous studies, α-cypermethrin is effective against A. diaperinus adults, causing 100% mortality after 14 days of exposure at 10% of LC50 [59]. However, the impact of sublethal concentrations of this insecticide on A. diaperinus is yet to be investigated. According to previous research, low doses of insecticides influence the physiology and behavior of various insect species in different ways [32,66,67]. Kavallieratos et al. [67] studied how chlorantraniliprole affects the movement behavior of Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) and S. oryzae at low concentrations. Analysis of their mobility behavior revealed notable differences between chlorantraniliprole-treated specimens and controls, in the absence and presence of food. Sitophilus oryzae demonstrated altered movement patterns and fewer approaches to food at sublethal doses, whereas S. zeamais presented increased walking time and shorter periods of immobility [67]. Concerning T. granarium, the exposure to low chlorfenapyr and pirimiphos-methyl concentrations caused detrimental mobility. Beetles exposed to an LC30 concentration of pirimiphos-methyl displayed a noticeably shorter walking duration compared to those exposed to LC10 of the tested insecticides, LC30 of chlorfenapyr, and control [66]. In the case of insecticides based on plants, the walking and mating behavior of adult Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae) was significantly impacted when exposed to the asteraceous hexane extract (HE) of Acmella oleracea (L.) R.K. Jansen at LC10 and LC30 [32]. The current study documents that even low concentrations of α-cypermethrin are able to negatively affect copulation success, reduce the time of copulation, and increase the time needed to recognize the mate. The process of mating is crucial for the expansion of insects as the way to increase their population, become established in new locations, and co-exist with other species [68]. It is already known that an increase in mate recognition time and a reduction in copulation time may lead to unfavorable results for the insect, such as facing issues in their reproduction and population growth [69,70]. Therefore, using smaller quantities of the insecticide, management of A. diaperinus is feasible while causing less interruption to the storage and/or poultry environment. Alternative methods to control A. diaperinus have been suggested previously. For example, all A. diaperinus larvae died when exposed to 40 ppm of O3 36 h post-treatment [71]. Moreover, the use of different strains of Beauveria bassiana (Balsamo-Crivelli) Vuillemin (Hypocreales: Cordycipitaceae) resulted in 95% and 62.5% mortality of A. diaperinus larvae and adults, respectively, when immersed in a 1 mL suspension containing 107 conidia [72].
This study clearly demonstrated that α-cypermethrin negatively affected the mating process of A. diaperinus under sublethal concentrations. Nevertheless, more research is needed to ascertain the effect of α-cypermethrin on insemination success, egg hatching, and offspring morphology. In addition to the management point of view, studying the laterality of mating success may be useful in the A. diaperinus mass rearing process, using selected behavioral patterns that enhance the reproduction of this species.

Author Contributions

Conceptualization, D.L.S.G. and N.G.K.; methodology, D.L.S.G., N.G.K. and M.C.B.; software, D.L.S.G., N.G.K. and M.C.B.; validation, D.L.S.G., N.G.K. and M.C.B.; formal analysis, D.L.S.G., N.G.K. and M.C.B.; investigation, D.L.S.G., N.G.K. and M.C.B.; resources, N.G.K.; data curation, D.L.S.G.; writing—original draft preparation, D.L.S.G., N.G.K. and M.C.B.; writing—review and editing, D.L.S.G., N.G.K. and M.C.B.; visualization, D.L.S.G., N.G.K. and M.C.B.; supervision, N.G.K.; project administration, N.G.K.; funding acquisition, N.G.K. All authors have read and agreed to the published version of the manuscript.

Funding

Project 34.0889 (Agricultural University of Athens, Account for Research Funds) supported this study in partial.

Data Availability Statement

Data is available within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Bertola, M.; Mutinelli, F. A systematic review on viruses in mass-reared edible insect species. Viruses 2021, 13, 2280. [Google Scholar] [CrossRef]
  2. Eidson, C.S.; Schmittle, S.C.; Goode, R.B.; Lal, J.B. Induction of leukosis tumors with the beetle Alphitobius diaperinus. Am. J. Vet. Res. 1966, 27, 1053–1057. [Google Scholar] [PubMed]
  3. de las Casas, E.; Pomeroy, B.S.; Harein, P.K. Infection and quantitative recovery of Salmonella typhimurium and Escherichia coli from within the lesser mealworm, Alphitobius diaperinus (Panzer). Poul. Sci. 1968, 47, 1871–1875. [Google Scholar] [CrossRef] [PubMed]
  4. Goodwin, M.A.; Waltman, W.D. Transmission of Eimeria, viruses, and bacteria to chicks: Darkling beetles (Alphitobius diaperinus) as vectors of pathogens. J. Appl. Poult. Res. 1996, 5, 51–55. [Google Scholar] [CrossRef]
  5. Litrup, E.; Torpdahl, M.; Malorny, B.; Huehn, S.; Helms, M.; Christensen, H.; Nielsen, E.M. DNA microarray analysis of Salmonella serotype Typhimurium strains causing different symptoms of disease. BMC Microbiol. 2010, 10, 96. [Google Scholar] [CrossRef] [PubMed]
  6. Brubaker, J.; Zhang, X.; Bourgeois, A.L.; Harro, C.; Sack, D.A.; Chakraborty, S. Intestinal and systemic inflammation induced by symptomatic and asymptomatic enterotoxigenic E. coli infection and impact on intestinal colonization and ETEC specific immune responses in an experimental human challenge model. Gut Microbes 2021, 13, e1891852. [Google Scholar] [CrossRef]
  7. Schroeckenstein, D.C.; Meier-Davis, S.; Graziano, F.M.; Falomo, A.; Bush, R.K. Occupational sensitivity to Alphitobius diaperinus (Panzer) (lesser mealworm). J. Allergy Clin. Immunol. 1988, 82, 1081–1088. [Google Scholar] [CrossRef]
  8. Singh, N. Chemical Ecology, Population Dynamics and Insecticide Susceptibility of Lesser Mealworm Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae). Ph.D. Dissertation, University of Arkansas, Fayetteville, AR, USA, 2011. [Google Scholar]
  9. Hagstrum, D.W.; Subramanyam, B. Stored-Product Insect Resource; AACC International, Inc.: St. Paul, MN, USA, 2009. [Google Scholar]
  10. Kaufman, P.E.; Strong, C.; Rutz, D.A. Susceptibility of lesser mealworm (Coleoptera: Tenebrionidae) adults and larvae exposed to two commercial insecticides on unpainted plywood panels. Pest Manag. Sci. 2008, 64, 108–111. [Google Scholar] [CrossRef]
  11. Szołyga, B.; Gniłka, R.; Szczepanik, M.; Szumny, A. Chemical composition and insecticidal activity of Thuja occidentalis and Tanacetum vulgare essential oils against larvae of the lesser mealworm, Alphitobius diaperinus. Entomol. Exp. Appl. 2014, 151, 1–10. [Google Scholar] [CrossRef]
  12. Wolf, J.; Potrich, M.; Lozano, E.R.; Gouvea, A.; Pegorini, C.S. Combined physical and chemical methods to control lesser mealworm beetles under laboratory conditions. Poult. Sci. 2015, 94, 1145–1149. [Google Scholar] [CrossRef]
  13. Zorzetti, J.; Constanski, K.; Santoro, P.H.; Fonseca, I.C.; Neves, P.M. Growth regulator insecticides for the control of the lesser mealworm beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae). Rev. Colomb. Entomol. 2015, 41, 24–32. [Google Scholar]
  14. Volpato, A.; Baretta, D.; Zortéa, T.; Campigotto, G.; Galli, G.M.; Glombowsky, P.; Santos, R.C.V.; Quatrin, P.M.; Ourique, A.F.; Baldissera, M.D.; et al. Larvicidal and insecticidal effect of Cinnamomum zeylanicum oil (pure and nanostructured) against mealworm (Alphitobius diaperinus) and its possible environmental effects. J. Asia-Pac. Entomol. 2016, 19, 1159–1165. [Google Scholar] [CrossRef]
  15. Volpato, A.; Lorenzetti, W.R.; Zortea, T.; Giombelli, L.C.D.D.; Baretta, D.; Santos, R.C.V.; Vaucher, R.A.; Raffin, R.P.; Souza, M.E.; Stefani, L.M.; et al. Melaleuca alternifolia essential oil against the lesser mealworm (Alphitobius diaperinus) and its possible effect on the soil fauna. Rev. Bras. Ciênc. Avíc. 2016, 18, 41–46. [Google Scholar] [CrossRef]
  16. Tomasi, T.; Zortéa, T.; dos Reis, T.R.; Lopes, L.Q.S.; Baldissera, M.D.; Santos, R.C.V.; Baretta, D.; Stefani, L.M.; da Silva, A.S. Insecticidal action of glycerol monolaurate against the lesser mealworm (Alphitobius diaperinus) and its ecotoxicological effect on Enchytraeus crypticus. Acta Sci. Vet. 2018, 46, 6. 1581. [Google Scholar] [CrossRef]
  17. Fernandes, T.A.P.; Marcomini, M.C.; Ferreira, F.P.; Guide, B.A.; Alves, V.S.; Neves, P.M.O.J. Native isolates and the effect of aviary litter on the pathogenicity and virulence of entomopathogenic nematodes for the control of the lesser mealworm, Alphitobius diaperinus (panzer) (Coleoptera: Tenebrionidae). Semin. Ciênc. Agrar. 2021, 42, 1–18. [Google Scholar] [CrossRef]
  18. Hassemer, M.J.; Lopes, R.B.; Borges, M.; Alves, L.F.; Withall, D.M.; Pickett, J.A.; Laumann, R.A.; Birkett, M.A.; Blassioli-Moraes, M.C. Development of an attract-and-infect device for biological control of lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae) in poultry houses. Biol. Control 2020, 149, 104326. [Google Scholar] [CrossRef]
  19. Pessoa, G.C.D.; Lopes, J.V.; Roch, M.F.; Pinheiro, L.C.; Rosa, A.C.L.; Michalsky, É.M.; Dias, E.S. Baseline susceptibility to alpha-cypermethrin in Lutzomyia longipalpis (Lutz & Neiva, 1912) from Lapinha Cave (Brazil). Parasit. Vectors 2015, 8, 469. [Google Scholar]
  20. Arena, M.; Auteri, D.; Barmaz, S.; Brancato, A.; Brocca, D.; Villamar-Bouza, L. Peer review of the pesticide risk assessment of the active substance alpha-cypermethrin. EFSA J. 2018, 16, e05403. [Google Scholar]
  21. Ngufor, C.; Agbevo, A.; Fagbohoun, J.; Fongnikin, A.; Rowland, M. Efficacy of Royal Guard, a new alpha-cypermethrin and pyriproxyfen treated mosquito net, against pyrethroid-resistant malaria vectors. Sci. Rep. 2020, 10, 12227. [Google Scholar] [CrossRef]
  22. World Health Organization (WHO). Alpha-Cypermethrin; Environmental Health Criteria 142; WHO: Geneva, Switzerland, 1992. [Google Scholar]
  23. World Health Organization (WHO). Specifications and Evaluations for Public Health Pesticides Alpha-Cypermethrin Long-Lasting (Incorporated into Filaments) Insecticidal Net; A racemic mixture of: (S)-α-cyano-3-phenoxybenzyl-(1R,3R)-3-(2,2-dichlorovinyl)-2,2-dimethylcyclopropane-carboxylate and (R)-α-cyano-3-phenoxybenzyl-(1S,3S)-3-(2,2-dichlorovinyl)-2,2-dimethylcyclopropane-carboxylate; WHO: Geneva, Switzerland, 2014. [Google Scholar]
  24. Abbas, N.; Hafez, A.M. Alpha-cypermethrin resistance in Musca domestica: Resistance instability, realized heritability, risk assessment, and insecticide cross-resistance. Insects 2023, 14, 233. [Google Scholar] [CrossRef]
  25. Rodríguez-Hidalgo, R.; Pérez-Otáñez, X.; Garcés-Carrera, S.; Vanwambeke, S.O.; Madder, M.; Benítez-Ortiz, W. The current status of resistance to alpha-cypermethrin, ivermectin, and amitraz of the cattle tick (Rhipicephalus microplus) in Ecuador. PLoS ONE 2017, 12, e0174652. [Google Scholar] [CrossRef] [PubMed]
  26. Salem, A.; Bouhsira, E.; Liénard, E.; Mélou, A.B.; Jacquiet, P.; Franc, M. Susceptibility of two European strains of Stomoxys calcitrans (L.) to cypermethrin, deltamethrin, fenvalerate, lambda-cyhalothrin, permethrin and phoxim. Int. J. Appl. Res. Vet. Med. 2012, 10, 249–257. [Google Scholar]
  27. Tainchum, K.; Shukri, S.; Duvallet, G.; Etienne, L.; Jacquiet, P. Phenotypic susceptibility to pyrethroids and organophosphate of wild Stomoxys calcitrans (Diptera: Muscidae) populations in southwestern France. Parasitol. Res. 2018, 117, 4027–4032. [Google Scholar] [CrossRef]
  28. Lorn, S.; Klakankhai, W.; Nusen, P.; Sumarnrote, A.; Tainchum, K. Pyrethroid susceptibility in Stomoxys calcitrans and Stomoxys indicus (Diptera: Muscidae) collected from cattle farms in southern Thailand. Insects 2022, 13, 711. [Google Scholar] [CrossRef] [PubMed]
  29. Guedes, R.N.C.; Guedes, N.M.P.; Rosi-Denadai, C.A. Sub-lethal effects of insecticides on stored-product insects: Current knowledge and future needs. Stewart Postharvest Rev. 2011, 3, 5. [Google Scholar]
  30. Zinhoum, R. Sublethal effects of malathion on biology and population growth of khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). Egypt. Acad. J. Biol. Sci. A Entomol. 2020, 13, 57–72. [Google Scholar]
  31. Campbell, B.; Baldwin, R.; Koehler, P. Locomotion inhibition of Cimex lectularius L. following topical, sublethal dose application of the chitin synthesis inhibitor lufenuron. Insects 2017, 8, 94. [Google Scholar] [CrossRef]
  32. Boukouvala, M.C.; Kavallieratos, N.G.; Maggi, F.; Angeloni, S.; Ricciutelli, M.; Spinozzi, E.; Ferrati, M.; Petrelli, R.; Canale, A.; Benelli, G. Being exposed to Acmella oleracea-based insecticides extract reduces mobility and mating success in Prostephanus truncatus, the major pest of maize in storages. J. Stored Prod. Res. 2023, 104, 102151. [Google Scholar] [CrossRef]
  33. Rogers, L.J.; Zucca, P.; Vallortigara, G. Advantages of having a lateralized brain. Proc. R. Soc. Lond. B Biol. Sci. 2004, 271, 420–422. [Google Scholar] [CrossRef]
  34. Bisazza, A.; Rogers, L.J.; Vallortigara, G. The origins of cerebral asymmetry: A review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neurosci. Biobehav. Rev. 1998, 22, 411–426. [Google Scholar] [CrossRef]
  35. Vallortigara, G.; Rogers, L.J.; Bisazza, A. Possible evolutionary origins of cognitive brain lateralization. Brain Res. Rev. 1999, 30, 164–175. [Google Scholar] [CrossRef] [PubMed]
  36. Vallortigara, G. Comparative neuropsychology of the dual brain: A stroll through animals’ left and right perceptual worlds. Brain Lang. 2000, 73, 189–219. [Google Scholar] [CrossRef] [PubMed]
  37. Rogers, L.J.; Andrew, R.J. Comparative Vertebrate Lateralization; Cambridge University Press: Cambridge, UK, 2002. [Google Scholar]
  38. Vallortigara, G.; Rogers, L.J. Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 2005, 28, 575–633. [Google Scholar] [CrossRef] [PubMed]
  39. MacNeilage, P.F.; Rogers, L.J.; Vallortigara, G. Origins of the left and right brain. Sci. Am. 2009, 301, 60–67. [Google Scholar] [CrossRef] [PubMed]
  40. Vallortigara, G.; Chiandetti, C.; Sovrano, V.A. Brain asymmetry (animal). Wiley Interdiscip. Rev. Cogn. Sci. 2011, 2, 146–157. [Google Scholar] [CrossRef]
  41. Rogers, L.J.; Vallortigara, G.; Andrew, R.J. Divided Brains: The Biology and Behaviour of Brain Asymmetries; Cambridge University Press: Cambridge, UK, 2013. [Google Scholar]
  42. Güntürkün, O.; Ströckens, F.; Ocklenburg, S. Brain lateralization: A comparative perspective. Physiol. Rev. 2020, 100, 1019–1063. [Google Scholar] [CrossRef]
  43. Letzkus, P.; Boeddeker, N.; Wood, J.T.; Zhang, S.W.; Srinivasan, M.V. Lateralization of visual learning in the honeybee. Biol. Lett. 2007, 4, 16–19. [Google Scholar] [CrossRef]
  44. Frasnelli, E.; Anfora, G.; Trona, F.; Tessarolo, F.; Vallortigara, G. Morphofunctional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav. Brain Res. 2010, 209, 221–225. [Google Scholar] [CrossRef]
  45. Frasnelli, E.; Vallortigara, G.; Rogers, L.J. Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav. Brain Res. 2010, 209, 36–41. [Google Scholar] [CrossRef]
  46. Anfora, G.; Frasnelli, E.; Maccagnani, B.; Rogers, L.J.; Vallortigara, G. Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav. Brain Res. 2010, 206, 236–239. [Google Scholar] [CrossRef]
  47. Anfora, G.; Rigosi, E.; Frasnelli, E.; Ruga, V.; Trona, F.; Vallortigara, G. Lateralization in the invertebrate brain: Left-right asymmetry of olfaction in bumble bee, Bombus terrestris. PLoS ONE 2011, 6, 18903. [Google Scholar] [CrossRef]
  48. Romano, D.; Kavallieratos, N.G.; Athanassiou, C.G.; Canale, A.; Stefanini, C.; Benelli, G. Impact of geographical origin and rearing medium on mating success and lateralization in the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J. Stored Prod. Res. 2016, 69, 106–112. [Google Scholar] [CrossRef]
  49. Benelli, G.; Romano, D.; Kavallieratos, N.G.; Conte, G.; Stefanini, C.; Mele, M.; Athanassiou, C.G.; Canale, A. Multiple behavioural asymmetries impact male mating success in the khapra beetle, Trogoderma granarium. J. Pest Sci. 2017, 90, 901–909. [Google Scholar] [CrossRef]
  50. Boukouvala, M.C.; Romano, D.; Kavallieratos, N.G.; Athanassiou, C.G.; Stefanini, C.; Canale, A.; Benelli, G. Asymmetric courtship boosts male mating success in the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Stored Prod. Res. 2019, 81, 1–6. [Google Scholar] [CrossRef]
  51. Boukouvala, M.C.; Romano, D.; Kavallieratos, N.G.; Athanassiou, C.G.; Stefanini, C.; Canale, A.; Benelli, G. Does geographical origin affect lateralization and male mating success in Rhyzopertha dominica beetles? J. Stored Prod. Res. 2020, 88, 101630. [Google Scholar] [CrossRef]
  52. Boukouvala, M.C.; Romano, D.; Kavallieratos, N.G.; Stefanini, C.; Canale, A.; Benelli, G. Behavioral asymmetries affecting male mating success in Tenebrio molitor (Coleoptera: Tenebrionidae), an important edible species. J. Econ. Entomol. 2021, 114, 454–461. [Google Scholar] [CrossRef]
  53. Boukouvala, M.C.; Romano, D.; Kavallieratos, N.G.; Stefanini, C.; Canale, A.; Benelli, G. Do asymmetric sexual interactions affect copulation in the saw-toothed grain beetle, Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae)? J. Stored Prod. Res. 2022, 96, 101946. [Google Scholar] [CrossRef]
  54. Boukouvala, M.C.; Kavallieratos, N.G.; Canale, A.; Benelli, G. Functional asymmetries routing the mating behavior of the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae). Insects 2022, 13, 699. [Google Scholar] [CrossRef]
  55. Kavallieratos, N.G.; Boukouvala, M.C.; Gidari, D.L.S.; Di Giuseppe, G.; Canale, A.; Benelli, G. Does cross-mating affect behavioral asymmetries and mating success of khapra beetle (Trogoderma granarium) strains? Entomol. Gen. 2023, 43, 409–419. [Google Scholar] [CrossRef]
  56. Renault, D. Long-term after-effects of cold exposure in adult Alphitobius diaperinus (Tenebrionidae): The need to link survival ability with subsequent reproductive success. Ecol. Entomol. 2011, 36, 36–42. [Google Scholar] [CrossRef]
  57. Calla-Quispe, E.; Martel, C.; Ibañez, A.J. Gender identity and sexual experience affect mating behaviour and chemical profile in the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). bioRxiv 2021. [Google Scholar] [CrossRef]
  58. Calla-Quispe, E.; Irigoin, E.; Mansurova, M.; Martel, C.; Ibáñez, A.J. Lateralized movements during the mating behavior, which are associated with sex and sexual experience, increase the mating success in Alphitobius diaperinus (Coleoptera: Tenebrionidae). Insects 2023, 14, 806. [Google Scholar] [CrossRef] [PubMed]
  59. Subekti, N.; Cahyaningrum, S.H.; Maulana, S. Effective control of Alphitobius diaperinus using natural bioinsecticides. J. Trop. Life Sci. 2022, 12, 289–297. [Google Scholar] [CrossRef]
  60. Renault, D.; Nedved, O.; Hervant, F.; Vernon, P. The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiol. Entomol. 2004, 29, 139–145. [Google Scholar] [CrossRef]
  61. Rice, S.J.; Lambkin, T.A. A new culture method for lesser mealworm, Alphitobius diaperinus. J. Appl. Entomol. 2009, 133, 67–72. [Google Scholar] [CrossRef]
  62. Esquivel, J.F.; Crippen, T.L.; Ward, L.A. Improved Visualization of Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae)—Part I: Morphological Features for Sex Determination of Multiple Stadia. Psyche. J. Entomol. 2012, 7, 328478. [Google Scholar]
  63. Finney, D.J. Statistical Methods in Biological Assay; Charles Griffin: London, UK, 1978. [Google Scholar]
  64. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available online: https://www.Rproject.org/ (accessed on 30 June 2024).
  65. SAS Institute Inc. Using JMP 16.2; SAS Institute Inc.: Cary, NC, USA, 2021. [Google Scholar]
  66. Kavallieratos, N.G.; Boukouvala, M.C.; Pappa, A.P.A.; Canale, A.; Benelli, G. Being exposed to low concentrations of pirimiphos-methyl and chlorfenapyr has detrimental effects on the mobility of Trogoderma granarium. Pest Manag. Sci. 2023, 79, 5230–5236. [Google Scholar] [CrossRef]
  67. Kavallieratos, N.G.; Boukouvala, M.C.; Eleftheriadou, N.; Filintas, C.S.; Gidari, D.L.S.; Kyrpislidi, V.P.C. Sublethal Effects of Chlorantraniliprole on the Mobility Patterns of Sitophilus spp.: Implications for Pest Management. Insects 2024, 15, 451. [Google Scholar] [CrossRef]
  68. Kavallieratos, N.G.; Athanassiou, C.G.; Guedes, R.N.; Drempela, J.D.; Boukouvala, M.C. Invader competition with local competitors: Displacement or coexistence among the invasive khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), and two other major stored-grain beetles? Front. Plant Sci. 2017, 8, 1837. [Google Scholar] [CrossRef]
  69. Hardy, I.C.; Ode, P.J.; Siva-Jothy, M. Mating behavior. In Insects as Natural Enemies: A Practical Perspective, 1st ed.; Jervis, M.A., Ed.; Springer: Dordrecht, The Netherlands, 2005; pp. 219–260. [Google Scholar]
  70. Hoppe, K.R.; Roush, R.T. Mate finding, dispersal, number released, and the success of biological control introductions. Ecol. Entomol. 1993, 18, 321–331. [Google Scholar] [CrossRef]
  71. Soares, C.E.D.S.; Weber, A.; Moecke, E.S.; Reiter, M.G.; Scussel, V.M.; De Souza, C.K. Use of ozone gas as a green control alternative to beetles Alphitobius diaperinus (panzer) infestation in aviary bed utilized in the poultry industry. Chem. Eng. Trans. 2018, 64, 589–594. [Google Scholar]
  72. Rezende, S.R.F.; Curvello, F.A.; Fraga, M.E.; Reis, R.C.S.; Castilho, A.M.C.; Agostinho, T.S.P. Control of the Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae) with entomopathogenic fungi. Braz. J. Poult. Sci. 2009, 11, 121–127. [Google Scholar] [CrossRef]
Insects 15 00804 g001
Figure 1. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to water-impregnated filter paper (control). Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 70 pairs).
Figure 1. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to water-impregnated filter paper (control). Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 70 pairs).
Insects 15 00804 g001
Insects 15 00804 g002
Figure 2. Flow chart of mating behavior and courtship behavior of Alphitobius diaperinus female adults exposed to water-impregnated filter paper (control). Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 40 pairs).
Figure 2. Flow chart of mating behavior and courtship behavior of Alphitobius diaperinus female adults exposed to water-impregnated filter paper (control). Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 40 pairs).
Insects 15 00804 g002
Insects 15 00804 g003
Figure 3. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to α-cypermethrin LC10. Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 98 pairs).
Figure 3. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to α-cypermethrin LC10. Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 98 pairs).
Insects 15 00804 g003
Insects 15 00804 g004
Figure 4. Flow chart of mating and courtship behavior of Alphitobius diaperinus female adults exposed to α-cypermethrin LC10. Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 32 pairs).
Figure 4. Flow chart of mating and courtship behavior of Alphitobius diaperinus female adults exposed to α-cypermethrin LC10. Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 32 pairs).
Insects 15 00804 g004
Insects 15 00804 g005
Figure 5. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to α-cypermethrin LC30. Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 93 pairs).
Figure 5. Flow chart of mating and courtship behavior of Alphitobius diaperinus male adults exposed to α-cypermethrin LC30. Different lateralized traits exhibited by the males during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 93 pairs).
Insects 15 00804 g005
Insects 15 00804 g006
Figure 6. Flow chart of mating and courtship behavior of Alphitobius diaperinus female adults exposed to α-cypermethrin LC30. Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 60 pairs).
Figure 6. Flow chart of mating and courtship behavior of Alphitobius diaperinus female adults exposed to α-cypermethrin LC30. Different lateralized traits exhibited by the females during each behavioral phase are indicated by the color of the arrows: orange for back-biased, red for front-biased, black for left-biased, and green for right-biased males. The width of each arrow indicates the percentage of insects engaging in each behavior (n = 60 pairs).
Insects 15 00804 g006
Table 1. Contact toxicity of α-cypermethrin on Alphitobius diaperinus adults.
Table 1. Contact toxicity of α-cypermethrin on Alphitobius diaperinus adults.
Active IngredientUnitLC10 (95% CI)LC30 (95% CI)LC50 (95% CI)χ2 (df = 23)p
α-cypermethrinmg a.i./cm20.0000666
(0.000024–0.000109)		0.000120
(0.0000596–0.000169)		0.000180
(0.000112–0.000229)		10.70.986
LC = lethal concentration that kills 10%, 30%, and 50% of the exposed beetles. 95% CI = lower and upper limits of the 95% confidence interval.
Table 2. Effect of the approaching side, when males approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
Table 2. Effect of the approaching side, when males approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
TreatmentDirection of the ApproachBehavioral Traits
Laterality ♂ Mate recognition (s)♂ Mounting (s)Copulation (s)
ControlBack46.1 ± 15.5 b513.3 ± 80.3 f57.7 ± 1.9 abc
Front123.4 ± 25.4 b1046.9 ± 140.4 e58.8 ± 1.0 ab
Left303.0 ± 112.6 a1008.7 ± 156.6 ef61.5 ± 3.4 a
Right108.4 ± 22.1 b1191.7 ± 121.6 de60.0 ± 1.5 a
Tested beetles (n = back- + front- + left- + right-biased)11 + 18 + 14 + 27 = 7011 + 18 + 14 + 27 = 7011 + 18 + 8 + 25 = 62
LC10Back49.8 ± 18.1 b1434.1 ± 179.3 bcde52.1 ± 0.9 cd
Front73.4 ± 12.3 b1120.7 ± 109.3 de51.7 ± 0.8 d
Left88.5 ± 18.5 b1811.4 ± 159.1 ac52.2 ± 0.6 cd
Right56.7 ± 8.0 b1438.4 ± 89.2 bd51.3 ± 0.4 d
Tested beetles (n = back- + front- + left- + right-biased)13 + 20 + 18 + 47 = 9813 + 20 + 18 + 47 = 9810 + 15 + 16 + 36 = 77
LC30Back338.4 ± 33.7 a1768.1 ± 165.0 abc50.7 ± 0.7 cd
Front435.6 ± 60.3 a1993.4 ± 332.6 abc51.0 ± 0.7 bcd
Left366.3 ± 28.7 a1878.5 ± 131.8 a50.4 ± 0.7 d
Right355.4 ± 23.9 a1745.8 ± 94.8 ac48.3 ± 0.7 d
Tested beetles (n = back- + front- + left- + right-biased)14 + 5 + 35 + 39 = 9314 + 5 + 35 + 39 = 936 + 4+ 21 + 29 = 60
χ2, df, p152.32, 11, <0.00169.63, 11, <0.001104.37, 11, <0.001
Values are means (± standard errors). Within each column, different letters indicate significant differences (Steel–Dwass test, p < 0.05).
Table 3. Effect of the approaching side, when females approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
Table 3. Effect of the approaching side, when females approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
TreatmentDirection of the ApproachBehavioral Traits
Laterality ♀ Mate recognition (s)♂ Mounting (s)Copulation (s)
ControlBack188.3 ± 76.2 ab994.9 ± 170.1 bc57.8 ± 1.4 abc
Front68.7 ± 20.8 b813.9 ± 132.5 c58.4 ± 1.1 ab
Left266.3 ± 157.0 ab287.5 ± 74.1 abc54.0 ± 2.0 abcd
Right226.4 ± 69.5 ab1132.7 ± 205.3 abc63.0 ± 0.8 a
Tested beetles (n = back- + front- + left- + right-biased)16 + 12 + 3 + 9 = 4016 + 12 + 3 + 9 = 4016 + 11 + 2 + 8 = 37
LC10Back99.7 ± 39.2 ab1038.8 ± 165.5 abc50.8 ± 0.6 bcd
Front69.2 ± 19.0 b1656.1 ± 283.0 abc51.9 ± 1.4 cd
Left121.8 ± 26.1 ab1203.3 ± 313.5 abc51.0 ± 1.6 cd
Right76.7 ± 17.4 b1170.0 ± 243.5 abc51.0 ± 0.7 d
Tested beetles (n = back- + front- + left- + right-biased)6 + 9 + 6 + 11 = 326 + 9 + 6 + 11 = 324 + 7 + 5 + 8 = 24
LC30Back331.0 ± 81.2 ab1717.0 ± 354.9 abc51.3 ± 2.6 bcd
Front320.5 ± 52.4 a1809.9 ± 159.4 ab49.4 ± 1.6 d
Left347.0 ± 22.1 a1791.6 ± 111.0 a49.6 ± 0.7 d
Right349.1 ± 37.4 a1716.1 ± 134.9 ab46.9 ± 1.4 d
Tested beetles (n = back- + front- + left- + right-biased)6 + 11 + 27 + 16 = 606 + 11 + 27 + 16 = 603 + 8 + 18 + 12 = 41
χ2, df, p152.32, 11, <0.00169.63, 11, <0.00157.48, 11, <0.001
Values are means (± standard errors). Within each column, different letters indicate significant differences (Steel–Dwass test, p < 0.05).
Table 4. Effect of the mounting side, when males approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
Table 4. Effect of the mounting side, when males approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
TreatmentDirection of MountingBehavioral Traits
Laterality ♂ Mate recognition (s)♂ Mounting (s)Copulation (s)
ControlBack490.7 ± 368.5 a1175.3 ± 51.7 abcde58.0 ± 0.0 ab
Front78.3 ± 41.5 bc601.0 ± 26.3 de59.8 ± 2.7 a
Left144.6 ± 35.7 bc982.9 ± 107.6 d59.4 ± 1.3 a
Right104.7 ± 23.4 bc1100.4 ± 115.0 cde59.6 ± 1.1 a
Tested beetles (n = back- + front- + left- + right-biased)3 + 4 + 38 + 25 = 703 + 4 + 38 + 25 = 701 + 4 + 35 + 22 = 62
LC10Back57.3 ± 11.7 bc1901.7 ± 399.2 abcde52.3 ± 1.5 ab
Front82.2 ± 0.0 abc762.0 ± 0.0 abcde-
Left51.5 ± 7.7 c1350.2 ± 83.8 bcde51.7 ± 0.5 b
Right76.5 ± 9.8 c1504.7 ± 96.5 abce51.6 ± 0.4 b
Tested beetles (n = back- + front- + left- + right-biased)3 + 1 + 43 + 51 = 983 + 1+ 43 + 51 = 983 + 0 + 33 + 41 = 77
LC30Back330.5 ± 74.0 ab2139.3 ± 165.9 abcde48.3 ± 3.3 b
Front---
Left379.4 ± 25.0 a1874.7 ± 115.9 a49.7 ± 0.7 b
Right363.2 ± 21.5 a1735.0 ± 91.0 ab49.3 ± 0.6 b
Tested beetles (n = back- + front- + left- + right-biased)4 + 0 + 40 + 49 = 934 + 0 + 40 + 49 = 933 + 0 + 24 + 33 = 60
χ2, df, p145.61, 10, <0.00159.3, 10, <0.001100.31, 9, <0.001
Values are means (± standard errors). Within each column, different letters indicate significant differences (Steel–Dwass test, p < 0.05). Where dashes are shown, no front-biased mounting was observed.
Table 5. Effect of the mounting side, when females approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
Table 5. Effect of the mounting side, when females approached their mate first, on the main mating traits of Alphitobius diaperinus exposed to impregnated filter paper with water (control), or LC10 or LC30 of α-cypermethrin.
TreatmentDirection of MountingBehavioral Traits
Laterality ♀ Mate recognition (s)♂ Mounting (s)Copulation (s)
ControlBack33.4 ± 12.4 c463.6 ± 145.5 c57.2 ± 3.2 abc
Front15.5 ± 18.5 c549.5 ± 28.2 c59.5 ± 2.5 ab
Left191.3 ± 56.1 bc1143.4 ± 157.7 c58.1 ± 1.3 a
Right230.9 ± 76.8 abc1061.2 ± 134.8 c60.5 ± 1.0 a
Tested beetles (n = back- + front- + left- + right-biased)5 + 4 + 18 + 13 = 405 + 4 + 18 + 13 = 405 + 4+16+12 = 37
LC10Back145.8 ± 40.6 abc1248.6 ± 367.3 abc53.4 ± 1.1 abcd
Front---
Left65.6 ± 10.1 c1446.9 ± 212.4 abc49.9 ± 0.7 cd
Right88.4 ± 20.1 c1132.9 ± 200.4 bc51.4 ± 0.8 bcd
Tested beetles (n = back- + front- + left- + right-biased)5 + 0 + 14 + 13 = 325 + 0 + 14 + 13 = 325 + 0 + 10 + 9 = 24
LC30Back287.5 ± 74.1 abc1606.3 ± 263.2 abc48.7 ± 2.3 d
Front---
Left357.8 ± 24.5 a1728.8 ± 91.6 ab49.4 ± 0.8 d
Right325.6 ± 27.7 ab1898.2 ± 145.9 a48.0 ± 1.2 d
Tested beetles (n = back- + front- + left- + right-biased)6 + 11 + 27 + 16 = 606 + 11 + 27 + 16 = 603 + 8 + 18 + 12 = 41
χ2, df, p64.17, 9, <0.00140.99, 9, <0.00157.04, 9, <0.001
Values are means (± standard errors). Within each column, different letters indicate significant differences (Steel–Dwass test, p < 0.05). Where dashes are shown, no front-biased mounting was observed.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Gidari, D.L.S.; Kavallieratos, N.G.; Boukouvala, M.C. Sublethal Effects of α-Cypermethrin on the Behavioral Asymmetries and Mating Success of Alphitobius diaperinus. Insects 2024, 15, 804. https://doi.org/10.3390/insects15100804

AMA Style

Gidari DLS, Kavallieratos NG, Boukouvala MC. Sublethal Effects of α-Cypermethrin on the Behavioral Asymmetries and Mating Success of Alphitobius diaperinus. Insects. 2024; 15(10):804. https://doi.org/10.3390/insects15100804

Chicago/Turabian Style

Gidari, Demeter Lorentha S., Nickolas G. Kavallieratos, and Maria C. Boukouvala. 2024. "Sublethal Effects of α-Cypermethrin on the Behavioral Asymmetries and Mating Success of Alphitobius diaperinus" Insects 15, no. 10: 804. https://doi.org/10.3390/insects15100804

APA Style

Gidari, D. L. S., Kavallieratos, N. G., & Boukouvala, M. C. (2024). Sublethal Effects of α-Cypermethrin on the Behavioral Asymmetries and Mating Success of Alphitobius diaperinus. Insects, 15(10), 804. https://doi.org/10.3390/insects15100804

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop