Introduction

Trogoderma granarium Everts, commonly known as the khapra beetle, is a major insect pest of stored products of both animal and plant origin, including cereal grains, oilseeds, pulses, dried fruits, nuts, spices, powdered milk, and packaged food, particularly in hot and dry regions of the world1,2,3. Trogoderma granarium is a quarantine pest species in several countries4, and it has also been listed among the worst invasive species worldwide5. Originally described in the Indian Subcontinent by the Cotes in 1894, T. granarium has since spread worldwide via trade6. This species has been reported from Africa (e.g. Sudan, Senegal, Zimbabwe, Libya, Morocco, Niger, Algeria, Libya, Mali, Egypt, Mauritania, Burkina Faso), Asia (e.g., Pakistan, Sri Lanka, Iran, Afghanistan, Syria, Yemen, Russia, China, Saudi Arabia, Bangladesh, India, Israel, Iraq, South Korea, Myanmar), Europe (e.g., Cyprus, Spain, Greece), the United States, Australia and Canada, mainly because of international trade2,5,7,8. Larvae of T. granarium are voracious primary feeders of both grain and non-grain commodities, with the potential to cause up to 70% losses of infested products within a short period of time2,3,9. There are different insecticides used to manage T. granarium worldwide; however, controlling T. granarium is difficult because of its ability to develop resistance to insecticides10,11,12,13,14.

Studies have revealed that T. granarium preferably feeds and expands its population rapidly on grain-based commodities2,15,16,17,18,19; however, it can also feed and survive in non-grain commodities, including nuts1. Nuts are consumed all over the world either through indigenous production or through trade20. Therefore, careful attention should be given to nuts during trade since infested commodities could easily enhance T. granarium be able to invade new areas. For the management of insect pests in a particular habitat, for instance, the management of stored insect pests in food commodities, it is necessary to study biology/life tables of insect pests in that situation. Life table studies are important tools for determining the relative suitability of feeding substrates for insect pests, which ultimately form the basis of population ecology and pest management21,22. The data generated in life stable studies, such as development, reproduction and survival, enable the prediction of future population projections and population dynamics of insect pests in specific habitats. However, conventional life tables often overlook a number of important factors, such as male populations, individual differences and variable performance of developmental stages, which can lead to misinterpretation of population dynamics. The age-stage, two-sex life table is a comprehensive tool that accounts for both sexes, eliminates many of these inherent limitations, and can be useful in decision making in pest management programs23. This method has been employed in studies to assess the relative suitability of hosts for the management of insect pests24,25,26,27,28,29. However, such studies on the management of stored insect pests are lacking.

Despite the fact that T. granarium can feed, survive and expand its population on nuts, there is limited knowledge about its biology and life table analysis on nuts. For example, Borzoui, et al.18 studied biology of T. granarium on four grain commodities (rye, rice, wheat and barley) and a nut (walnut) and reported that biological performance was weaker on walnuts than that on grain commodities. Recently, Kavallieratos, et al.1 studied the population growth of T. granarium on several non-grain commodities, including seven nuts (pumpkin seeds, sunflower seeds, almond, walnut, pistachio, hazelnut and roasted chickpeas) and reported rapid population growth of this species on pumpkin seeds, sunflower seeds, almond, walnut and pistachio. The biological traits of stored insect pests, such as fecundity, longevity, survival and developmental period, are strongly influenced by the type of feeding substrate30,31,32. Although the effects of different types of stored grain commodities on the biology of T. granarium have been explored, the effects of non-grain commodities such as nuts on biological traits and population parameters of this species have received little attention. Thus, in the present study we explored the impact of selected nuts on the biology of T. granarium via the age–stage, two-sex life table method. Understanding life table analyses on different nuts would help to devise effective management plans against T. granarium.

Materials and methods

Commodities

Four different nuts such as peanut, Arachis hypogaea L., cashew, Anacardium occidentale L., pine nut, Pinus gerardiana Wall, and pecan, Carya illinoinensis (Wangenh.) K. Koch, were purchased from a local nuts-market in Lahore (31.5204° N, 74.3587° E) and used for the experiments. Clean grains of soft wheat, Triticum aestivum L. var. Anaj-2017, served as a control. All the nuts were verified infestation-free pre-trial through: (a) freezing at −18 °C for 14 days, (b) visual observation for the presence of adults or larvae of T. granarium, and (c) stereomicroscopic examination (40×) of dissected nuts (n = 100 per commodity). Wheat was sourced from a laboratory colony with no history of T. granarium exposure. The moisture content of all the commodities was adjusted to 13.0 ± 0.5% by either adding distilled water or drying in an oven as needed, and the moisture content was measured via a moisture meter33,34.

Insects

A laboratory strain of T. granarium, which has been reared in the laboratory since 201310, was used for experiments. The strain was maintained in the laboratory on wheat at 30 °C and 65% relative humidity. Before starting the experiments, we subdivided the laboratory strain (approximately 100 unsexed adults in each subdivision) and reared them separately on peanuts, cashews, pine nut or pecans for five generations to allow them to acclimatize to new food commodities, remove previous food effects, and observe the actual effects of nuts on the biology of the insects more clearly35,36. For this purpose, 100 unsexed newly emerged adults of the laboratory strain were introduced into glass jars (500 ml) containing 200 g of each food commodity. Hereafter, we designated each subdivision as peanut strain, cashew strain, pine nut strain, pecan strain or wheat strain (control) of T. granarium.

Effects of different food commodities on the biology of Trogoderma granarium

After five generations on a specific food, 60 eggs of each strain (F5) were carefully separated via a fine hair brush from their respective food commodity and placed in Petri dishes (one egg per Petri dish) containing one gram of peanut, cashew, pine nut, pecan or wheat for the upcoming larva and adult. To prevent escape, upper inner walls of petri dishes were coated with polytetrafluoroethylene. The Petri dishes were placed in incubators set at 33 °C and 65% relative humidity. The Petri dishes were observed daily to record the egg hatch rate, time required for each developmental stage, survival and longevity. The effects of each food on the fecundity of T. granarium were studied following Borzoui, et al.18, with a few modifications. A newly emerged male and female pair of each strain of T. granarium was introduced into a Petri dish containing 1 gram of their respective food. The pair was shifted daily to a new petri dish with fresh food. The dishes with adult pairs were observed daily until the death of the female, and approximately 20–25 pairs (replicates) of each strain were used to record fecundity. The experiments were conducted following completely randomized design (CRD).

Statistical analyses

The population parameters such as finite and intrinsic rate of increase, net reproductive rate, mean generation time, age-specific survival rate, age-specific fecundity, age-stage life expectancy, age-stage reproductive value (Table 1)21,29, and data of biology of T. granarium such as the duration of developmental stages (egg, larva, pupa), longevity, survival, fecundity and oviposition days were analyzed by the TWOSEX-MSChart program23,37. The significance of mean values, based on confidence interval methods38, of population parameters and biological traits of T. granarium in different treatments were analyzed through the paired bootstrap test using TWOSEX-MSChart with 100,000 resampling technique39,40.

Table 1 Population parameters£ of Trogoderma granarium used in the present study to observe the effects of different food commodities £adapted from21,29.
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Results

Biological traits of Trogoderma granarium strains on different food commodities

Biological traits of T. granarium after being fed on different nuts are presented in Table 2. The data revealed significant effects of nuts on the biology of T. granarium. For example, the egg hatch period of T. granarium was the longest on pecan, followed by those on pine nut, cashew and peanut, whereas the eggs of the strain that fed on wheat (control) presented a minimum number of days to hatch (p < 0.05). The larval duration of the pecan and pine nut strains of T. granarium was the longest (65.14 and 62.35 d, respectively) compared to the wheat strain, followed by those of cashew and peanut (p < 0.05). The pupae of the pecan strain took 7.54 d to eclose followed by 7.06, 6.67, 6.19 and 5.60 d for the pine nut, cashew, peanut and wheat strains of T. granarium, respectively (p < 0.05). In comparison to wheat, the longevity of females and males was greater on pecan and pine nut than on the rest of the nuts. Compared with wheat, the effects of different nuts were non-significant (p > 0.05) in terms of the sex ratio. Among the nuts, the preoviposition period of T. granarium was the lowest on peanut, cashew, pine nut and pecan, both the latter were statistically similar. The oviposition period of T. granarium on peanut and cashew was the longest, followed by that of the pecan and pine nut strains (p < 0.05). Females of T. granarium laid significantly more eggs on peanut and cashew than on pine nut and pecan. Similarly, the preadult survival rate was greater in peanut and cashew than in pecan and pine nut (Table 2). Adult emergence was the highest on peanut (76.67) followed by cashew (65.00%) and the lowest (58.33%) on pine nut and pecan.

Table 2 Biological traits of Trogoderma granarium on different nuts, and wheat as a control.
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Nuts and wheat had a non-significant effect (p > 0.05) on population parameters such as the finite rate of increase and intrinsic rate of increase of T. granarium, whereas the net reproductive rate and mean generation time were significantly affected by different types of nuts and wheat (Table 3). The pecan and pine nut strains of T. granarium presented the lowest net reproductive rate, followed by the cashew strain, whereas the wheat and peanut strains presented the highest net reproductive rate. Compared to the wheat strain, the pecan and pine nut strains presented the longest mean generation times, followed by the cashew and peanut strains of T. granarium. The gross reproductive rate was the highest on peanut and the lowest on pecan. The doubling time was the highest on pecan and pine nut followed by cashew and the lowest on wheat and peanut (Table 3).

Table 3 The effects of nuts and wheat (control) on the population parameters of Trogoderma granarium.
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Impact of feeding media on the population parameters of Trogoderma granarium

Nuts and wheat had a significant effect on the age-stage-specific survival rate (Sxj) of T. granarium (Fig. 1). The analysis of different curves, which show the survival probability of different stages at a specific age, revealed that adult male and female T. granarium emerged from pupae earlier in the control treatment (i.e., on the 51 st and 49th days, respectively) than in the other treatments. In the case of nuts, adult males and females on peanut eclosed earlier from pupae on the 55th and 50th days, followed by the 60th and 58th days, 65th and 66th days, and 67th days on cashew, pine nut and pecan (p < 0.05), respectively. Moreover, the survival rate was lower in the larval and pupal stages than in the other life stages in the pecan and pine nut strains, followed by the cashew and peanut strains compared with the wheat strains of T. granarium (Fig. 1).

Fig. 1
Fig. 1
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The effects of nuts and wheat (control) on the age-stage-specific survival rate of Trogoderma granarium.

The data for the age-stage-survival rate (lx), age-stage-specific fecundity (fxj), total fecundity of a strain (mx), and net maternity (lxmx) of different strains of T. granarium are presented in Fig. 2. All these parameters significantly varied (p < 0.05) among the different strains of T. granarium. For example, females of the wheat strain started oviposition on the 54th day followed by the 56th, 63rd, 70th and 71 st days, by the females of the peanut, cashew, pine nut and pecan strains of T. granarium, respectively. The highest peaks of lxmx were observed on the 62nd, 69th, 71 st, 79th and 91 st days in the control, peanut, cashew, pine nut and pecan treatments, respectively, with 3.55, 1.70, 1.90, 1.33 and 1.03 eggs, respectively (Fig. 2).

Fig. 2
Fig. 2
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The effects of nuts and wheat (control) on the age-specific survival rate (lx), fecundity (mx) and maternity (lx mx) of Trogoderma granarium.

There was a significant effect of different nuts and wheat on the values of life expectancy (exj) at different stages of T. granarium (Fig. 3). For example, the exj values of newly hatched eggs laid by females of the wheat, peanut, cashew, pine nut and pecan strains of T. granarium are 60.07, 57.53, 59.15, 59.32 and 57.72, respectively (Fig. 3). Similarly, different diets had a significant effect on the reproductive value (vxj) of T. granarium strains. These values are assumed to predict the rate of population growth in the future. The peak reproductive values of the wheat, peanut, cashew, pine nut and pecan strains of T. granarium occurred at 56, 75, 71, 95 and 70 days of age, respectively (Fig. 4). This implies that females aged 56, 75, 71, 95 and 70 days make the major contribution to the rate of future population growth when fed on wheat, peanut, cashew, pine nut and pecan, respectively.

Fig. 3
Fig. 3
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The effects of nuts and wheat (control) on the life expectancy of different stages of Trogoderma granarium.

Fig. 4
Fig. 4
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The effects of nuts and wheat (control) on the reproductive value of Trogoderma granarium.

Discussion

The findings of the present study clearly indicate that the use of nuts as a feeding substrate significantly affects the performance of biological traits. Overall, a lengthened developmental time; reduced survival, fecundity, and net reproductive rate; and a lengthened mean generation time of T. granarium were noted for pecan and pine nuts, whereas the reverse was observed for wheat (control), peanut and cashew.

Differences in the feeding substrates of insect pests are often associated with variations in their developmental duration, survival at different stages and reproduction41,42. The data of the present study showed that the egg hatch period of T. granarium significantly varied among different nuts, with values ranging from 5.74 d for peanut to 7.39 d for pecan. The egg hatch period observed in the present study was shorter than those reported by Burges19 for wheat feed, and Shahid, et al.43 for different wheat varieties. Naseri and Borzoui17 reported that the egg hatch period of T. granarium ranged from 6.51 d to 8.09 d for different wheat cultivars. However, in contrast to these studies, Kavallieratos, et al.16 reported shorter egg hatch periods in T. granarium, ranging from 4.68, 4.81 and 4.82 d for peeled oats, triticale and peeled barley, respectively. The inconsistent data of the egg hatch period in the present and previous studies might be due to variations in feeding substrates, experimental protocols and/or differences in the geographical origins of different strains of T. granarium41,44,45.

The developmental duration of immature T. granarium has been reported to be affected by the type of commodity46. The data of the present study clearly revealed that the larval duration, pupal duration and total preadult duration were greater in pecan and pine nut than in peanut, cashew and the control. The larval duration ranged from 45.94 to 65.14 d; the pupal duration ranged from 5.60 to 7.54 d; and the total preadult duration ranged from 56.70 to 80.00 d for different commodities. The larval, pupal and total preadult periods in wheat were significantly shorter than those recorded in nuts. The total preadult duration of T. granarium was 56.71 d on wheat in the present study compared with 53.54 d on wheat, as reported by Borzoui, et al.18. Kavallieratos, et al.16 reported 27.00, 34.64 and 35.75 d larval durations of T. granarium on barley, oats and triticale, respectively. Moreover, in that study, the total preadult duration of T. granarium was recorded to be 35.06, 42.87 and 43.58 d on barley, oats and triticale, respectively. Shahid, et al.43 reported that the total preadult duration of T. granarium ranged from 48.44 to 64.16 for different wheat- varieties. The development of larvae and pupae was 62.13, 82.38, 54.02, 53.54 and 91.30 d in barley, rice, rye, wheat and walnut, respectively18. In contrast, the development of larvae to the adult stage ranged from 24.7 to 31 d for the different sorghum fractions46. Differences in host commodities and/or their geographical variations could be responsible for the variable developmental times of the immature stages of T. granarium. The results of the present study are in broad agreement with those reported by Khan, et al.47, who reported that variation in feeding substrates could strongly affect the developmental time of different immature stages in Musca domestica Linnaeus. A lengthened developmental time of T. granarium was observed on pecan and pine nut, suggesting that these hosts might be less favorable for its feeding and development. Conversely, peanuts and cashews may be favorable hosts, as T. granarium exhibits a relatively short developmental period on these commodities.

The extended larval development of T. granarium on pecan and pine nut, versus other commodities, is concerning. The larval stage is assumed to be responsible for the population spread of T. granarium, which is also reported to be resistant or less susceptible to insecticides10,48,49. It can be concluded that business activities involving the trade of these nuts could be a potential path for the expansion of T. granarium in different areas.

The fecundity data of T. granarium on different hosts also varied. Relatively greater numbers of eggs were produced by the wheat strain, followed by the peanut and cashew strains, than by the pecan and pine nut strains of T. granarium. In addition, a lower net reproductive rate, survival rate, and longer mean generation time were noted for the pecan and pine nut strains than for the other strains. Feeding on less favorable food commodities is often linked with fitness costs in insects, which ultimately results in prolonged development and reduced fecundity and survival rates50,51. Hence, pecan and pine nuts seem to be less favorable hosts for T. granarium.

Life table studies form the basis of population ecology and pest management. Life tables of insect pests are usually affected by their feeding substrates52. Hence, it is important to construct life tables of insect pests on diverse feeding hosts in order to generate databases that can be used to develop effective pest management programs. Studying biology of T. granarium on grain commodities has been the preferred choice in earlier studies. Given that T. granarium is a polyphagous and invasive species, knowledge of biology in diverse commodities could help devise effective management strategies against this pest in different scenarios. In conclusion, the findings of the present study provide insights into the development and life history of T. granarium after rearing on different nut species. Trogoderma granarium has completed development on all types of hosts. Peanuts and cashews favor the rapid development of T. granarium, with increased fecundity, a high net reproductive rate and a reduced generation time. Although the biological performance of T. granarium was affected on pecans and pine nuts, these hosts also favored the completion of their life stages. However, any host commodity that negatively affects biological fitness could be an important tool to successfully manage T. granarium16. The development of T. granarium is significantly faster on peanut and cashew hosts than that on pine nuts and pecans under optimal temperature and relative humidity conditions. Management of T. granarium must target high-risk nuts in warm, dry conditions to prevent rapid infestation in stored commodities. Careful attention should be given to non-grain commodities, including nuts, during trade since infested commodities could easily help T. granarium be able to infest new areas. Hence, the nut industry should implement a risk-based pest management strategy. This strategy should prioritize strict sanitation, enhanced monitoring, and targeted phytosanitary treatments for high-risk stored commodities such as wheat, peanuts, and cashews on which T. granarium grow rapidly. Simultaneously, vigilance must be maintained for pine nuts and pecans, as their role as potential pathways for the initial introduction and spread of T. granarium remains a critical concern. In addition, the optimal diets identified in the present study can be utilized to improve the efficiency and cost-effectiveness of mass-rearing of T. granarium for crucial bioassay research. This knowledge also allows stakeholders to better predict and mitigate risks associated with T. granarium host switching and cross-contamination within facilities, ultimately safeguarding economic interests, enabling smarter resource allocation, and ensuring the integrity of the global nut supply chain through more informed and proactive decisions. Future studies should explore the fitness of T. granarium on other nuts and/or non-grain commodities to improve existing management practices for this species.