Spatio-Temporal Distribution of Stored Product Insects in a Feed Mill in Greece

Abstract

Floor traps were placed in a feed mill in Greece for a period of approx. 13 months to illustrate the relative abundance and distribution of the stored product insects found. More than 20 taxa were found, with most of them belonging to Coleoptera. The most abundant species found were the rice weevil, Sitophilus oryzae (L.), and the granary weevil, Sitophilus granarius (L.), which are common primary colonizers of grains, and the confused flour beetle, Tribolium confusum Jacquelin du Val, and the red flour beetle, Tribolium castaneum (Herbst), which are secondary colonizers that usually occur in processed amylaceous commodities. Interestingly, the highest population densities of all four species were recorded during the same period, with the secondary colonizers slightly preceding the primary colonizers. Although competition among these species has been recorded in previous studies, we found that these four species could coexist during the entire trapping period in the same sampling units, which indicates possible spatial segregation and different colonization patterns in space and time. Our results demonstrate that trapping in storage and processing facilities is an essential component of decision-making regarding stored product pest management strategies in localized applications, and can drastically reduce the need for treating the entire facility.

1. Introduction

The stored product ecosystem is considered a man-made environment, which is not affected much by abiotic conditions that are determinative in the case of other ecosystems, such as those in agroforestry environments [1,2]. For instance, in bulked grains, heat conduction is considered to occur much more gradually than that of the surrounding air, a phenomenon that has been characterized as “hysteresis” [3,4,5]. As a result, the grain cools down slowly during winter months, allowing insect acclimation to the extreme temperature conditions, constituting stored product insects tolerant to cold [6]. Indicatively, in an earlier study, Athanassiou and Arthur [7] found that several stored product insects remained unaffected by exposure at 0 °C for 7 days.

In a similar way to bulked grains, food processing facilities retain temperatures that are higher than those in the surrounding environment during the cold period of the year, given that these facilities usually operate throughout the year and have to be heated when this is considered necessary [8,9,10,11,12]. Hence, insect activity is continuous in these areas during the entire year [11,13,14]. For instance, Morrison et al. [12] found that the population fluctuation of stored product insects in different processing facilities in Greece indicated larger insect numbers in summer and early fall, but there were considerable insect numbers during winter months as well.

Based on the above, and in contrast with pests that occur in different types of crops and orchards, stored product insects have a dynamic presence all year round, with often overlapping generations and, as such, their presence requires continuous trapping and sampling [12,15,16]. In fact, often, detection during the cold period of the year is even more important than that in the warm period, in order to estimate hidden infestations and initial colonization foci [9,14,17]. For instance, Athanasiou et al. [17] found that insect colonization in silos starts from the upper bulk part. Nevertheless, large insect populations may likely occur in the bottom layers of silos with false floors [4,17,18].

Floor traps have been proven to be important tools for the detection of insects in processing facilities, and have been tested with success in different application scenarios [9,10]. Not surprisingly, these traps can even be used unbaited to take advantage of the stereotropism of crawling insects [12]. Several studies have shown that even the addition of a pheromone may not affect captures. At the same time, floor traps may capture and retain insects without the need for a killing agent [12,13,14,19,20]. In an extensive surveillance projectbased on floor traps that was carried out a few years ago, Morrison et al. [12] indicated that these traps could depict the spatio-temporal distribution of stored product insects in processing facilities, as well as the dominance and frequency of the main species, and eventually provide guidance on specific control measures. As a continuance of that work, we used floor traps in order to illustrate the population dynamics of major stored product insects in a feed mill in an effort to locate increased insect presence and time-localized control measures.

2. Materials and Methods

2.1. Facility Description

The trapping was conducted in a feed mill in Northern Greece, which stored and processed soft and hard wheat, but also barley and maize in smaller quantities. The traps were deployed in the facility on 24 February 2022 (Figure 1). In the case of the silo, it was constructed of concrete and consisted of eight levels. The traps were deployed on the ground of the basement, 1st, and 8th level.

2.2. Experimental Design

The trap type that was used in our experiments was Dome Trap (Trécé Inc., Adair, OK, USA), and the attractant was Storgard^TM Oil kairomone food (Oil, Trécé Inc., Adair, OK, USA). In total, 36 traps (Figure 1) were used and were checked every 15 days (replacing those traps that were damaged), except for periods when access to trapping areas was limited due to periodical spraying with insecticides in the warehouses with Actellic 50 EC (48% AI) obtained from Syngenta International AG (Basel, Switzerland) or fumigations with phosphine in the case of silos. The attractant oil was refilled when it was considered necessary. Before the refilling, the traps were cleaned, the debris was removed using paper, and then the oil was placed. In particular, during the winter period, the attractant oil was refilled once a month, whereas when the temperature increased (spring–summer), the attractant oil was refilled every two weeks. All captured insects were removed individually using a fine paint brush (Lineo, No. 1; Mesko-Pinsel GmbH, Wieseth, Germany) and kept in plastic cylindrical vials (Rotilabo^® sample tins with snap-on lids, 3 cm in diameter, 8 cm in height, Carl Roth Gmbh & Co., Kg, Karlsruhe, Germany). After that, the vials were transferred to the Laboratory of Entomology and Agricultural Zoology (LEAZ), Department of Agriculture, Crop Production and Rural Environment, at the University of Thessaly, where counting and identification were carried out. The insects found were identified using different taxonomic keys [21,22,23].

2.3. Data Analysis

The insect numbers captured were analyzed according to the criteria of “Dominance” and “Frequency” as used by Curry [24] and Buchelos and Athanassiou [25]. The term Dominance signifies the percentage of individuals belonging to a particular species compared to the individuals of all species identified in total. Thus, a given species can be classified as Dominant, Influent, and Recedent, corresponding to >5, 2–5, and <2% of the total number of individuals found. A species “Frequency” is measured by the percentage of samples in which the particular species was reported. Thus, a given species can be classified as Constant, Accessory, and Accidental, when individuals of this species have been found to make up >50, 25–50, or less than 25% of the total number of samples [25]. Additionally, the spatio-temporal distribution was visualized using Python (version 3.12), specifically employing the Matplotlib library for visualization and the SciPy library’s interpolation module for handling data points in multiple dimensions.

3. Results

A total of 2.113 individuals were collected, corresponding to several taxa. The individuals found corresponded to 5 Orders, 15 Families, and at least 16 species. The most dominant species were the confused flour beetle, Tribolium confusum Jacquelin DuVal (Coleoptera: Tenebrionidae); the red flour beetle, Tribolium castaneum (Herbst) (Coleopetra: Tenebrionidae); the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae); the granary weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae); and members of the Orders of Lepidoptera and Diptera (

Table 1. Dominance and Frequency of the species found during the trapping period.

Family/Taxa	Species	% of the Total Number of Adults	Dominance	% of the Total Number of Samples	Frequency
Tenebrionidae	Tribolium confusum	19.21	Dominant	82.76	Constant
	Tribolium castaneum	15.09	Dominant	65.51	Constant
	Latheticus oryzae	3.02	Influent	48.27	Accessory
	Others	0.28	Recedent	13.79	Accidental
Silvanidae	Oryzaephilus surinamensis	3.73	Influent	68.96	Constant
Anobiidae	Lasioderma serricorne	3.97	Influent	44.82	Accessory
	Stegobium paniceum	0.28	Recedent	17.24	Accidental
Bostrychidae	Rhyzopertha dominica	0.70	Recedent	31.03	Accessory
Curculionidae	Sitophilus oryzae	11.16	Dominant	31.03	Accessory
	Sitophilus granarius	19.40	Dominant	82.75	Constant
	Sitophilus zeamais	0.66	Recedent	6.89	Accidental
Laemophloeidae	Cryptolestes ferrugineus	0.04	Recedent	11.11	Accidental
	Cryptolestes sp.	0.14	Recedent	10.34	Accidental
Nititulidae	Carpophilus sp.	3.73	Influent	34.48	Accessory
Dermestidae	Trogoderma sp.	0.91	Recedent	41.37	Accessory
Ptinidae	Ptinus sp.	0.18	Recedent	13.79	Accidental
Mycetophagidae	Typhaea sp.	0.37	Recedent	13.79	Accidental
Lepidoptera		6.29	Dominant	65.51	Constant
Formicidae		1.65	Recedent	13.79	Accidental
Staphilinidae		1.37	Recedent	31.03	Accessory
Diptera		7.52	Dominant	68.96	Constant
Hemiptera		0.14	Recedent	3.44	Accidental

). The most frequently found species were T. confusum (406 adults), T. castaneum (319 adults), O. surinamensis (79 adults), and S. granarius (410 adults) (Table 1).

The highest number of stored product insect individuals was captured in August, September, and October 2022, with 307, 305, and 331 individuals recorded, respectively (Figure 2). Regarding the dominant species, in the case of T. confusum and T. castaneum, the majority of the individuals were recorded in August and September, respectively (Figure 3). On the other hand, the highest number of individuals of S. oryzae was found in March, at the beginning of the trapping period, but high numbers were also recorded in autumn. In a similar pattern, the peak number of S. granarius individuals in the traps was noted in October (Figure 3).

Figure 4, Figure 5 and Figure 6 illustrate the spatial distribution of stored product insects in the feed mill at three different times during the trapping period: 23 March 2022 (Figure 4), August 18, 2022 (Figure 5), and 2 February 2023 (Figure 6). These figures show how the presence of insects in the facility changed over time; the three time intervals that are presented here are selected as being indicative of the spatial distribution of the species found throughout the trapping period. Similar figures for other dates were also generated during the study but could not all be presented in this paper, for brevity. In Figure 4, representing March 2022, the insect distribution appears relatively uniform, with moderate insect activity throughout the facility. Higher insect counts were concentrated in the central and storage areas associated with product storage and processing. By August 2022, as shown in Figure 5, the insect numbers increased significantly, with a notable concentration of insects in the central and northern parts of the facility. The spatial concentration in these areas suggests increased insect activity, particularly in the vicinity of the product handling areas. This period marks the highest insect population density recorded during the entire trapping period, with a widespread presence throughout the facility. In contrast, Figure 6 (February 2023) shows a decrease in insect numbers compared to those in August. However, certain zones, particularly near the storage areas, still show moderate insect activity. The distribution in this figure highlights the persistence of insect presence in localized areas despite the overall reduction in numbers.

4. Discussion

Interestingly, the most abundant species that were found during the entire trapping period were categorized into primary and secondary pests. Specifically, two relative primary colonizers (that attack the whole grain and are capable of penetrating undamaged seed coats), S. orzyae and S. granarius, and two secondary colonizers (that feed on grain products or grains that have already been damaged by primary colonizers and fungus feeders or as a result of harvesting, handling, and transporting), T. castaneum and T. confusum were found. This could be attributed to the fact that the same facility had quantities of both product categories, i.e., sound grain kernels, which are prone to infestation by primary colonizers, and bran and related processed commodities, which are prone to infestation by secondary colonizers. These two groups of species, although they are often found in a complementary way in the same locations, also compete for the same food source [26,27,28,29,30,31,32]. Trematerra et al. [31] found that secondary colonizers are more prone to infesting kernels that have been previously infested by primary colonizers, rather than undamaged kernels. In this regard, this ecological succession can retain its dynamics in a given facility for a long period, with minor spatial segregations [5,11,14,17].

Surprisingly, the relative species that have been found here are direct competitors, and, often, only one is the superior colonizer. For instance, Athanassiou et al. [32] found that in vials with wheat and rice, the coexistence of S. oryzae, S. granaries, and the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), resulted in the gradual displacement of the latter species in both commodities. This could be attributed to the fact that the population growth and reproductive rates of S. oryzae are superior to those of S. granarius, which is more obvious when both species are in a confined area with limited food availability [32]. In contrast, T. castaneum and T. confusum may coexist for a long time in the same conditions without displacement, probably due to the fact that these species can easily switch infestation foci and food preferences within the same facility [11,13,14]. The co-occurrence of Sitophilus spp. may further contribute to this coexistence indirectly, due to the production of damaged kernels as a result of the infestation that are concomitantly suitable for the colonization of secondary colonizers. Periodically, insecticidal applications may favor population outbursts of one of these species that may be more tolerant/resistant than the other species found in certain active ingredients, but the population rebound for all four species has similar trends. At the same time, control measures may periodically change the spatio-temporal distribution of stored product insects [33].

Although it is theoretically expected that, based on what has been mentioned above, the peaks of the primary colonizers usually precede those of the secondary ones, we found that all the peaks of the most abundant species found occurred pretty much within the same period, and, in fact, often, the peaks of the secondary colonizers preceded those of their primary counterparts. Apparently, this is partially due to the presence of processed products throughout the entire period in most of the areas of the facility, which means that there was no need for the primary colonizers to produce cracked kernels. Nevertheless, there are reports where species that are considered secondary colonizers have been able to infest sound grain kernels [34]. It is commonly reported that different species of secondary colonizers occur together in grain, but it is less common to find the co-occurence of different colonizing species [5,17]. For example, Nansen et al. [35] conducted sampling in a corn facility for 13 consecutive weeks and found high densities of secondary colonizers such as T. castaneum; the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae); and the foreign grain beetle, Ahasverous advena (Waltl) (Coleoptera: Silvanidae), and found only one colonizer, S. zeamais. One more example, T. castaneum has been found to infest the embryos of wheat kernels [36]. Furthermore, there are cases where primary colonizers have developed in cracked kernels or processed amylaceous commodities [36]. For instance, Kavallieratos et al. [37] found that adults of the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae), could oviposit better in broken rice kernels as compared to whole rice kernels. Based on previous studies and the data reported here, it is evident that spatial segregation is temporary, and that secondary colonizers can establish high population outbursts in areas that had previously been infested by primary colonizers, such as warehouses with grains, that lay much further than areas with processed commodities, such as flour or bran.

To enhance the practical point of our findings, we propose several pest management strategies informed by the spatio-temporal distribution patterns observed in this study. Targeted insecticide applications should be prioritized in high-activity zones identified through trapping data, allowing for localized treatments that reduce overall chemical use. Seasonal monitoring data further underscore the importance of aligning control measures with high infestation levels, particularly during summer and early autumn, when populations are observed to surge. This timing enables pest management schedules to focus resources efficiently, ensuring that infestations are addressed before they become widespread. Additionally, the spatial distribution patterns provide critical insights into optimal trap placement and inspection frequencies, focusing on areas with consistently high insect densities. These patterns can also guide decisions on supplementary measures, such as fumigation in heavily infested zones or enhanced sanitation protocols to disrupt pest habitats and food sources. These strategies demonstrate how trap data may be directly translated into a practical point of view, reducing the infestation level of stored products, and minimizing the use of chemicals.

5. Conclusions

What we saw in this study is the dynamic succession of stored product insect populations in a confined area, and the potential “synchronization” of their population fluctuations, suggesting that abiotic conditions, such as temperature, may be more important than biotic ones, such as food resources. From a practical point of view, the results of the present work underline the importance of continuous trapping in a given area, which may reveal the need for localized control measures at the initial infestation locations and at certain periods, rather than treating the entire facility blindly.