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Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat
Journal of Stored Products Research 76 (2018) 43e50
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Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat T. Sonai Rajan a, V. Muralitharan a, G.J. Daglish b, S. Mohankumar c, M.A. Rafter d, S. Chandrasekaran a, S. Mohan a, D. Vimal e, Chitra Srivastava e, M. Loganathan f, G.H. Walter d, * a
Department of Agricultural Entomology, Centre for Plant Protection Studies, Tamil Nadu Agricultural University, Coimbatore e 03, India Department of Agriculture and Fisheries, EcoSciences Precinct, GPO Box 267, Brisbane, Queensland 4001, Australia Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore e 03, India d School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia e Division of Entomology, Indian Agricultural Research Institute, Pusa Campus, New Delhi e 12, India f Department of Primary Processing, Storage and Handling, Indian Institute of Food Processing Technology, Thanjavur e 05, India b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 October 2017 Received in revised form 15 December 2017 Accepted 15 December 2017
The timing, extent and landscape coverage of the flight of stored product insect pests could influence their ecology differentially across climatic zones. We therefore assessed the seasonal flight patterns of Tribolium castaneum (Herbst), Rhyzopertha dominica (F.) and Sitophilus oryzae (L.) monthly, for 18 months, in three habitats (around bulk grain storage, in cropping habitats, and in mixed orchard habitats) in southern India (Coimbatore and Thanjavur) and northern India (New Delhi) using pheromone traps. We tested for species-specificity in their seasonal flight patterns as well as regional variation. Vastly more beetles were trapped near bulk grain storages than in cropping and orchard habitats. In both southern and northern India, T. castaneum was most numerous, with numbers much higher in southern India. Rhyzopertha dominica was more commonly trapped in New Delhi, a wheat producing region, than in the rice producing south. The numbers of T. castaneum trapped across time and geographical location varied significantly, with peak flight activity during the post-monsoon period (October). By contrast, R. dominica in New Delhi peaked once during summer (May) around bulk storage but tended to be more consistent (but far less numerous) in habitats away from storage. Only a few S. oryzae were caught in pheromone traps. The mean trap catches of T. castaneum in Thanjavur and New Delhi showed significant positive correlations with minimum temperatures, whereas those of R. dominica in New Delhi were significantly correlated with maximum temperatures. The patterns recorded are consistent with results recorded on other continents, but temperature thresholds for flight need to be examined in this context. A major difference was that beetles, especially T. castaneum, were captured far less frequently in traps away from storage in India than in Australia, a pattern that needs to be confirmed before a biological basis for it is sought. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Seasonal flight pattern Tribolium castaneum Rhyzopertha dominica Sitophilus oryzae India Pheromone traps
1. Introduction The role of movement in the ecology of insect pests of stored products is difficult to interpret because these organisms are moved in significant numbers with the bulk transport of commodities, and most are also able to fly. Disentangling the relative
* Corresponding author. Present/Permanent Address: School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. E-mail address: [email protected] (G.H. Walter). https://doi.org/10.1016/j.jspr.2017.12.005 0022-474X/© 2017 Elsevier Ltd. All rights reserved.
contributions of these processes to the rate of infestation of bulk stored grain is in its infancy and is, despite its relevance to the environmentally sound management of these pests and the effective management of phosphine resistance, currently a major challenge in understanding the ecology of these species. Each mode of pest movement has to be understood in its own right before their relative contributions can be assessed (Nopsa et al., 2015). The different beetle species involved are known for their differential flight propensities and abilities, but even these are not yet well understood, and the depth of understanding of the movement of
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pest grain beetles varies with species and region. Tribolium castaneum (Herbst) is believed to generate new infestations in bulk grain storage primarily through the anthropogenic transport of commodities (Good, 1933; White, 1981; Campbell and Arbogast, 2004; Drury et al., 2009; Campbell et al., 2010). This view has presumably been nurtured by those who have used this species as a “model organism” in ecology, as insects that do not fly (as explained by Ridley et al. (2011)). Recent investigations of the spatio-temporal pattern of T. castaneum movement across subtropical cropping regions of eastern Australia (a site in which movement of grain between storages is limited) have found that these beetles are routinely captured in flight (throughout the year), even at distances >1 km from bulk-stored grain (Ridley et al., 2011; Daglish et al., 2017). These trapping data, together with population genetic analyses on the trapped insects, indicate that the beetles fly often enough and far enough to render the entire population genetically homogenous over relatively large areas (7000 km2) (Ridley et al., 2011). Rhyzopertha dominica (F.), by contrast, is characterized as a strong flier that can be intercepted in flight at substantial distances from grain storage (Cogburn, 1988; Edde et al., 2006; Ridley et al., 2016), and this species has been demonstrated to disperse across diverse environments (Mahroof et al., 2010). Studies of R. dominica dispersal have been concentrated in temperate and subtropical areas of the United States (Leos-Martinez et al., 1986; Throne and Cline, 1994; Edde et al., 2006; Toews et al., 2006 Mahroof et al., 2010), Canada (Fields et al., 1993) and Australia (Sinclair and Haddrell, 1985; Wright and Morton, 1995; Ridley et al., 2016). Most of these studies have found that R. dominica is active only in summer in temperate areas (Sinclair and Haddrell, 1985; Throne and Cline, 1994), but also in small numbers even in the coldest months in subtropical areas (Ridley et al., 2016; Daglish et al., 2017). Sitophilus oryzae (L.) has been captured in flight in the vicinity of stored grain in several countries, in both passive traps and traps baited with aggregation pheromone lures (Sinclair and Haddrell, 1985; Throne and Cline, 1989; Likhayo and Hodges, 2000). Laboratory studies on this species have evidently revealed variation across populations in their propensity for flight (Grenier et al., 1994; Cox et al., 2007), and only those strains infected with the endosymbiont Wollbachia seem able to fly in the laboratory (Grenier et al., 1994). Despite evidence of flight by S. oryzae in the vicinity of stored grain, only limited information is available on the potential for more extensive flights by this species. Specifically, Sinclair and Haddrell (1985) captured small numbers of beetles in farm fields using sticky traps and with a trap mounted on a moving vehicle. Spatio-temporal data on the flight of storage pests in a heterogeneous agricultural landscape in a tropical monsoonal climate, such as that of India, are not available. We therefore conducted a monthly trapping survey, over 18 months, to determine the movement of T. castaneum, R. dominica and S. oryzae within various habitats close to and at a distance from bulk grain storage in two different climatic regions of India. India stores (and moves) vast quantities of food grains in bulk throughout the year, particularly rice and wheat, and significant post-harvest grain losses caused by insect pests have been reported. Also, households store small quantities of grain for consumption, and our trapping sites were essentially urban (at bulk storage depots) or peri-urban (with respect to the other habitats). Based on earlier reports on pheromone trapping of flying beetle pests of stored grain (Ridley et al., 2011, 2016; Daglish et al., 2017) we predicted that trap catches of T. castaneum and R. dominica would be much higher near bulk storage in India than those captured near bulk stores in Australia. We also anticipated that trap catches in habitats away from bulk storage (in cropping and mixed
orchard habitats) would be disproportionately higher (relative to results from bulk storage sites) than in Australia. These expectations relate to our initial observations in India, where vast numbers of beetles can be readily observed each day in the late afternoon, crawling on the surfaces of bag stacks and taking to flight. In Australia, by contrast, T. castaneum and R. dominica beetles can be observed flying from bulk grain storage and can be trapped near storage, but numbers tend to be low and on some days no beetles take flight (Ridley et al., 2011, 2016; Rafter et al., 2015, 2018). We also anticipated that the flight of these beetles would be less seasonal in southern India than it is in Australia, where temperatures differ more strongly across seasons. In northern India, however, we anticipated strong seasonality in flight activity because of the wider seasonal range in temperatures there than in southern India. 2. Materials and methods 2.1. Study locations Trapping was undertaken at two locations in southern India [at Coimbatore (11.0183 N, 76.9725 E) and Thanjavur (10.7825 N, 79.1313 E), both in Tamil Nadu] and one in northern India [at New Delhi (28.6139 N, 77.2089 E)]. We deployed multidirectional flight traps baited with species-specific aggregation pheromone lures. The distance between the two southern locations is about 250 km, and 1800 km between New Delhi and each of the southern locations. Tamil Nadu is close to the equator and tends to be relatively warm and stable climatically, whereas a wide seasonal range of temperatures typifies New Delhi (Fig. 1). A monsoon season occurs in both northern and southern India. The southwest monsoon affects the entire country from June to September and the northeast monsoon brings rain to Tamil Nadu from October to December (Fig. 1). Rice is the main cereal crop in southern India, whereas wheat is the main crop in northern India. Despite this, rice and wheat are routinely transported in bulk across the whole of India, and is bulk stored in areas where it is not grown. 2.2. Sampling Thirty traps were set at each of the three geographical localities, with 10 traps placed at each of three habitats within each locality. The habitats included areas around bulk grain storage (in warehouses called godowns, with grain held in 50 kg jute sacks), cropping (rice or wheat fields) and mixed orchard (fruit and vegetable crops) habitats. These three habitats within each locality were separated by 5, 3 and 8 km (Coimbatore), 10, 11 and 14 km (Thanjavur), and 1.5, 2.5 and 1.5 km (New Delhi) from one another. Each trap was suspended 1.5 m from the ground on a steel pole and was at least 30 m from any other trap. The traps were custom made of galvanized iron for the study (Melwin Engineering Pvt. Ltd., Coimbatore) (Fig. 2). Each trap was baited with three species-specific pheromone lures, one each for T. castaneum, R. dominica and S. oryzae (Insects Limited Inc., Westfield, IN, USA). Traps were set for the first 7 days of each month, starting from September 2013 and continuing until February 2015 for all three locations, except for the trapping period in November 2014 at Coimbatore, when no trapping could be conducted. New pheromone lures were used for each trapping period. At the end of each week's trapping, the numbers of T. castaneum, R. dominica and S. oryzae adults were counted and sexed. Fifty beetles of each species (if fewer than this were trapped, then all beetles in the sample) from randomly selected traps (one from each habitat at all three locations) were sexed each month. Male and female adults of T. castaneum were identified by the presence (male) or absence (female) of a sub-basal setiferous
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Fig. 2. Multidirectional pheromone trap used in the field study of seasonal flight of stored grain insect pests. The traps were constructed from galvanized iron and were hung 1.5 m from the ground.
77.162018 E), and at each of which data were taken manually, once a day, from a Single Stevenson Screen (IS Standard IMD, Pune) containing a minimum, maximum and wet and dry bulb thermometer. 2.3. Statistical analyses
Fig. 1. Seasonal climatic data for the two trapping locations in southern India A) Coimbatore and B) Thanjavur and the northern trapping location of C) New Delhi. Solid black lines represent the mean monthly temperatures recorded during the study and dashed black lines represent the 25 year monthly average temperature (maximum and minimum temperatures). Dark grey bars represent total rainfall recorded each month during the period of the study and light grey bars the 25 year mean monthly rainfall. The vertical light grey shading represents the north-east monsoon (OctobereNovember) which brings rainfall to A) Coimbatore and B) Thanjavur in the south and the south-west monsoon (JuneeSeptember) which brings rainfall to C) New Delhi in the North.
puncture on the ventral side of the anterior femora (Halstead, 1963). As there are no consistent external differences between adult males and females of R. dominica, they were distinguished by squeezing each beetle until the tip of its genitalia appeared (Crombie, 1941). Sitophilus oryzae was not trapped in numbers high enough to warrant further investigation. The monthly ambient weather data, namely minimum and maximum temperature ( C), total rainfall (mm) and relative humidity (%), were sourced from (i) the Department of Agricultural Meteorology, Tamil Nadu Agricultural University, Coimbatore (11.015186 N, 76.932617 E), (ii) the Soil and Water Management Research Institute, Kattuthottam, Thanjavur (10.7815 N, 79.1767 E), and (iii) the Division of Agricultural Physics, Indian Agricultural Research Institute, New Delhi (28.639256 N,
The numbers of T. castaneum and R. dominica caught at the bulk grain storage habitats in southern India (Coimbatore and Thanjavur) and northern India (New Delhi) were each analyzed using repeated measures ANOVA (Genstat, 2008) to investigate the effects of geographic location (Coimbatore, Thanajvur or New Delhi) and trapping date. Insufficient numbers of T. castaneum and R. dominica were caught within any of the cropping and mixed orchard habitats to be analyzed statistically (see results). The data were transformed (loge (Nþ1)) before analysis to conform to the assumptions of ANOVA. Fisher's Protected LSD was used for multiple comparisons after running the repeated measures ANOVA in GenStat as all the effects in the means must be estimated in the same stratum with the same efficiency factors for methods other than Fisher's Protected LSD. A simple correlation matrix was also created to assess the possible influence of minimum and maximum temperatures, total rainfall, and relative humidity on the seasonal flight patterns of T. castaneum and R. dominica around bulk grain storage areas. A Chisquare test for independence was used to compare the proportions of male T. castaneum caught at the bulk grain storage area of southern India with the proportion of females, but such an analysis was not undertaken for R. dominica trapped near bulk grain storage in New Delhi because of the low numbers of individuals (<50 per month) caught (see results). In all cases the a threshold for assessing statistical significance was 0.05. 3. Results Temperature and rainfall profiles recorded during the study at facilities near each of the three main sampling localities
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Table 1 Total numbers of Tribolium castaneum, Rhyzopertha dominica and Sitophilus oryzae trapped in pheromone traps over 18 months in each of three different habitats (bulk storage (godowns), grain cropping habitats, and mixed orchard habitats) across three geographical localities in India. Location
Coimbatore Thanjavur New Delhi Total
Tribolium castaneum
Rhyzopertha dominica
Sitophilus oryzae
Godown
Cropping
Orchard
Godown
Cropping
Orchard
Godown
Cropping
Orchard
23,746 25,019 5545 54,310
18 0 130 310
35 16 87 138
297 50 2691 3038
57 47 109 213
25 179 171 375
11 0 65 76
3 0 3 6
3 0 2 5
approximated the 25 year averages for those localities (Fig. 1). Significantly more beetles were trapped in bulk grain storage habitats than in cropping and mixed orchard habitats of southern and northern India. The most abundant species caught was T. castaneum across all of the localities sampled (Table 1). Rhyzopertha dominica was caught in higher numbers in northern India (New Delhi) compared to the two southern sampling locations (Table 1). Few S. oryzae were caught at any of the godowns or agricultural environments of southern and northern India (Table 1).
3.1. Tribolium castaneum Substantial numbers of T. castaneum were caught during the 18month trapping period at bulk grain storage habitats in Coimbatore (23,746), Thanjavur (25,019) and New Delhi (5,545) (Table 1). Totals of 310 and 138 T. castaneum were caught in the three cropping and mixed orchard habitats, respectively (Table 1). Repeated measures ANOVA analysis showed significant variation in the numbers of T. castaneum trapped across the three geographical locations
Fig. 3. Seasonal trapping of Tribolium castaneum in New Delhi in the northern monsoonal tropics of India, and in two locations (Coimbatore and Thanjavur) in the southern monsoonal tropics of India. In each locality traps were set in three habitats. (A) Bulk grain storage (godown), where mean numbers (±1SE) of beetles are given for each trapping period at each of the three locations. (B) grain growing area, and (C) mixed orchard, in both of which totals of beetles are given for each trapping period at each location (because captures were so low and included mostly zeros). The pheromone traps were monitored for 7 days each month over 18 months (September 2013eFebruary 2015).
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Table 2 Results of correlation analyses run on trap catches of Tribolium castaneum and Rhyzopertha dominica across three localities in India against maximum and minimum temperatures. Location
Coimbatore Thanjavur New Delhi a
Tribolium castaneum
Rhyzopertha dominica
Minimum Temperature
Maximum Temperature
Minimum Temperature
Maximum Temperature
rs ¼ 0.199, P ¼ .538 rs ¼ 0.525, P ¼ .025a rs ¼ 0.510, P ¼ .031a
rs ¼ 0.309, P ¼ .213 rs ¼ 0.389, P ¼ .111 rs ¼ 0.363, P ¼ .139
rs ¼ 0.290, P ¼ .243 rs ¼ 0.083, P ¼ .744 rs ¼ 0.429, P ¼ .076
rs ¼ 0.030, P ¼ .906 rs ¼ 0.002, P ¼ .993 rs ¼ 0.495, P ¼ .037a
Correlation significant at 0.05 level.
(F2,27 ¼ 60.07, P < .001) and across the 18-month study period (F16,432 ¼ 11.10, P < .001). Also, a significant interaction was evident between geographical location and study period (F32,432 ¼ 6.99, P < .001). In southern India, the monsoonal periods of October and November 2013 and June to August 2014 returned the highest trap catches of T. castaneum around godowns. Trap catches during winter (January to February), and after that (up to May), were relatively low (Fig. 3). In northern India, the highest trap catches of T. castaneum were associated with the post monsoon period of October and September 2014, and only a few were captured during the winter period of December to January (Fig. 3). The mean trap catches of T. castaneum at the bulk grain storage habitats of Thanjavur and New Delhi showed significant positive correlations with minimum temperatures (Pearson correlation analysis) (Table 2). There was no correlation of mean trap catches of T. castaneum and any of the weather variables measured in the other south Indian location, Coimbatore (Table 2). At New Delhi, the mean minimum temperatures associated with T. castaneum flight were 4.8 (January 2014), 7.1 (December 2013), 8.6 (February 2014) and 9.3 C (March 2014). The proportions of T. castaneum females caught in the traps placed around the bulk grain storage areas of Coimbatore (n ¼ 7744) and Thanjavur (n ¼ 4615) were consistently > 50%, with a mean of 59.6 and 56.4% respectively. However, Chi-square analysis showed there were no significant differences in the proportion of male to female T. castaneum (c2 ¼ 0.194; df ¼ 1; p ¼ .723).
3.2. Rhyzopertha dominica The highest numbers of R. dominica were caught in the bulk grain storage habitat of northern India (2,691), whereas only 297 (Thanjavur) and 50 (Coimbatore) individuals were caught throughout the entire study period at bulk grain storage areas in southern India (Table 1). Significant differences were strongly evident in the numbers of R. dominica trapped over 18 months (F16,432 ¼ 7.39, P < .001) as well as across all three geographical locations (F2,27 ¼ 24.31, P < .001). A significant interaction between the locations and study period was also clear (F32,432 ¼ 9.46, P < .001). In Coimbatore, maximum trap catches of R. dominica at godowns were recorded during the pre-monsoon period of June to July 2014, and negligible trap catches were recorded through the rest of the year (Fig. 4). In Thanjavur more R. dominica were trapped in the orchard habitat than around the godown (Fig. 4). Trap captures in the Thanjavur orchard habitat peaked during January and February in both 2014 and 2015 (Fig. 4). Trap catches of R. dominica in northern India were highest in May 2014 and this correlated significantly with maximum temperature (Fig. 4, Table 2). Rhyzopertha dominica was trapped in low numbers in cropping and mixed orchard habitats in southern and northern India, and the catches were more evenly spread across the seasons (Fig. 4). More females than males were caught in the bulk grain storage area of New Delhi.
3.3. Sitophilus oryzae Totals of 11 and 65 individuals of S. oryzae were caught at bulk grain storage areas of Coimbatore and New Delhi, respectively (Table 1). In total, only 11 individuals were caught in grain growing and mixed orchard habitats in Coimbatore and New Delhi. No S. oryzae were caught at any of the three habitats in the second southern Indian location, Thanjavur (Table 1).
4. Discussion We interpret the flight data for each of T. castaneum and R. dominica independently, and these insights allow a comparison, for each species, across other such studies of flight in the field. We can thus deduce what is species-specific with respect to the flight of each species, and then how these species-specific aspects are influenced by local conditions of climate and other variables. The negligible trap catches of S. oryzae (Table 1) are open to interpretation and further investigation is needed to resolve whether these beetles do not fly much or whether flying adults are not much attracted to the pheromone lure, with similar low numbers having been captured in Western Australia (Daglish et al., 2014). Note that Kiritani (1965) reported no flight in a Japanese population of this species. The trapping data show that T. castaneum and R. dominica differ from one another in their relative abundance across the geographical areas sampled in India, but this does assume that the trapping system and pheromone lures have roughly equivalent efficiencies across these two species and across latitudes. Although that assumption is unlikely, the differences across north and south are of an order of magnitude, so comparison is valid. In both northern and southern India, the most prevalent beetle species trapped was T. castaneum, with total catch being much higher in the south (>23,000 beetles in each locality vs 5545 in the north) (Table 1). Rhyzopertha dominica was more prevalent in New Delhi (total of 2691 beetles) than it was in Tamil Nadu (maximum of 297), presumably because the north is where wheat is mainly grown in India, and where it is the predominant commodity in storage (Table 1). Further, the vast majority of beetles of both species were trapped at bulk grain storage areas with far fewer beetles caught in the pheromone traps placed away from these areas (cropping and orchard habitats) (Table 1), a point that is expanded below. Regardless of trap efficiency, the seasonal pattern of T. castaneum flight differed substantially from that of R. dominica. The trap catches of T. castaneum showed that these insects flew throughout the year in southern India (Fig. 3), but flight was seasonal in the north where it was presumably too cold for flight in winter (<20 C maxima in New Delhi (Fig. 1)). The numbers of beetles trapped flying across the agricultural landscape in the north was, again, restricted to the warmer months (mainly July to October) (Fig. 3). Similar flight patterns have been reported in various parts of Australia (Ridley et al., 2011; Daglish et al., 2017) and in the USA (Campbell et al., 2010). In general, all of these results
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Fig. 4. Seasonal trapping of Rhyzopertha dominica in New Delhi in the northern monsoonal tropics of India, and in two locations (Coimbatore and Thanjavur) in the southern monsoonal tropics of India. In each locality traps were set in three habitats. (A) Bulk grain storage (godown), where mean numbers (±1SE) of beetles are given for each trapping period at each of the three locations. (B) grain growing area, and (C) mixed orchard, in both of which totals of beetles are given for each trapping period at each location (because captures were so low and included mostly zeros). The pheromone traps were monitored for 7 days each month over 18 months (September 2013eFebruary 2015).
are consistent with the minimum temperature threshold for T. castaneum flight initiation in the laboratory being 25 C (Cox et al., 2007), with maximum trap catches of T. castaneum coinciding with temperatures above this, and especially when both minima and maxima are above this temperature, as in September, October and November in Thanjavur (with mean minimum and maximum temperatures being 27.6 and 34.8 C, 28.3 and 37.5 C, and 29.4 and 33.1 C, respectively). Tribolium castaneum beetles in flight were strongly associated with storage facilities in southern India, with a ratio of 1:0.001 beetles near bulk storage relative to trapping locations away from bulk storage. Unexpectedly low numbers of beetles (<10 beetles at each sampling occasion) were consistently trapped throughout the year in the south in cropping and orchard habitats, but mainly at the Coimbatore site (Fig. 3). In northern India, the equivalent ratio was 1:0.039 beetles. These ratios are extremely low when compared with the ratio of beetles flying near bulk storage relative to those flying one km away from storage in Australia (1:0.4 beetles, see Fig. 2, Ridley et al., 2011). The difference in these ratios across the continents was against prediction, because we expected beetles to be leaving high density infestations in India at greater relative
frequencies. This result implies that emigration is not driven by density or, at least, is not driven primarily by density, even though these beetles tend to be repelled (whilst walking) by the presence of conspecifics (Duehl et al., 2011). Clearly, tests are required to determine what these beetles do once they walk out onto the surface of the grain bags and take flight above the bag stacks. Rhyzopertha dominica has a different flight pattern from that of T. castaneum, being much more seasonal, even in the south (Fig. 4). The seasonality was, however, evident only in the catches made where grain was stored in bulk. Away from storage, in cropping and mixed orchard habitats, trap catches were much more evenly spread across the year, especially in northern India (Fig. 4). Average numbers in traps were generally much lower than those of T. castaneum, especially in southern India. The substantially greater captures of R. dominica in the north than in southern India are presumably related to the widespread and routine cultivation and storage of wheat in the area of the Gangetic Plain in northern India. It seems, therefore, that the main commodities produced and stored regionally influence the local composition of pest species, and that the bulk transport of grains does not influence this pattern to a great extent, but this needs to be tested more thoroughly,
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perhaps with population genetics markers. The numbers of R. dominica caught in traps was higher at the beginning of the season and then dropped during the winter months (Fig. 4). Maximum trap catches of R. dominica were observed during the summer season of May 2014 in the vicinity of bulk grain storages in northern India, when the average minimum and maximum temperatures were 23.2 and 39.5 C, respectively. A significant positive correlation of trap catches with maximum air temperature was detected (Table 2). Similar observations on R. dominica being most abundant during the warmest months have been reported in Australia (Sinclair and Haddrell, 1985; Ridley et al., 2016), Canada (Fields et al., 1993), and the USA (Dowdy and McGaughey, 1994; Throne and Cline, 1994; McKay et al., 2017). Consequently, the responses of flight to temperature seem quite consistent across the different populations of R. dominica that have been investigated in the field, but some variation is evident. The winter months of northern India recorded nil trap catches of R. dominica, when the mean minimum and maximum temperatures were 9.2 and 22.5 C, respectively. These findings are thus consistent with those of Sinclair and Haddrell (1985) who stated that R. dominica flight activity in the field in Queensland (Australia) was significantly reduced through the cooler months. Wright and Morton (1995) were more explicit, stating that no flight of R. dominica occurred at all when temperatures were below 16 C in northern New South Wales, Australia. In the USA, however, Toews et al. (2006) concluded that R. dominica flight activity in the field stops below 22.5 C during summer and below 17.5 C in the cooler months. Clearly, the flight threshold of this species warrants experimental investigation across different populations, to test how stable this feature is across the species. Differences in trap catches of R. dominica were evident across the traps placed in bulk grain storage areas and those placed in cropping and mixed orchard habitats (in both southern and northern India). As with T. castaneum, trap catches of R. dominica were much higher in traps placed in the vicinity of bulk grain storage than those placed in cropping and mixed orchard habitats (in both southern and northern India). However, the discrepancy was not as high as that for T. castaneum, with the ratio in northern India being 1:0.1 and that in the south being 1:0.9. This latter value was inflated by the Thanjavur traps around storage catching few beetles (Fig. 4), to the extent that the ratio for Thanjavur was 1:4.5. In Australia, the ratio was 1:1 (see Ridley et al., 2016), which implies that the behavior of R. dominica in India may be similar to that suggested for T. castaneum in the beetles being less inclined (than conspecifics in Australia) to disperse from infested bulk-stored grain. Although this behavior may not be so strongly expressed in R. dominica relative to T. castaneum, the interpretation we offer (see above) does warrant further testing. This study is the first detailed analysis of seasonal flight patterns of key stored grain insect pests across different latitudes in the monsoonal tropics of India. Perhaps the main difference, ecologically, from the results obtained by similar means in Australia (Ridley et al., 2011, 2016; Rafter et al., 2015, 2018; Daglish et al., 2017) is in the relatively low numbers of R. dominica captured in flight generally (Table 1), and the relatively low numbers of T. castaneum captured in habitats away from storage areas (Fig. 3). For R. dominica it now seems crucial to establish whether relatively few beetles fly because they are not so numerous in India or whether they do fly less (and if so, why they do so). The question with T. castaneum is whether they do fly long distances less frequently than they do in Australia. We have noticed that vast numbers of T. castaneum take flight inside godowns in the late afternoon, and establishing whether these individuals are in the process of leaving that locality would help to interpret their movement and its consequences more clearly. Ecological
49
information of this nature would facilitate the development of effective management tactics to control the spread and development of phosphine resistance and to reduce the likelihood or severity of infestations caused by these insect pests. Acknowledgements This work was financially supported by the Australia e India Strategic Research Grand Challenge Funded (GCF010006) project entitled “Ensuring food security: harnessing science to protect our grain harvest from insect threats”, jointly sponsored by the Department of Science and Technology (DST), New Delhi, India, and the Department of Innovation, Industry, Science and Research (DIISR), Canberra, Australia. We thank the managers and technical staff of the Food Corporation of India in Coimbatore, Thanjavur and New Delhi for their permission to conduct the experiments and their support throughout. We are also grateful for the thoughtful comments of an anonymous reviewer, which helped to clarify our interpretation. Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.jspr.2017.12.005. References Campbell, J.F., Arbogast, T., 2004. Stored product insects in a flour mill: population dynamics and response to fumigation treatment. Entomol. Exp. Appl. 112, 217e225. Campbell, J.F., Toews, M.D., Arthur, F.H., Arbogast, R.T., 2010. Long-term monitoring of Tribolium castaneum populations in two flour mills: rebound after fumigation. J. Econ. Entomol. 103, 1002e1011. Cogburn, R.R., 1988. Detection, distribution and seasonal abundance of Sitotroga cerealella and Rhyzopertha Dominica as indicated by pheromone-baited adhesive traps. In: Proceedings, XVIII International Congress of Entomology, 3 e 9 July 1988. University of British Columbia, Vancouver, Canada. Cox, P.D., Wakefield, M.E., Jacob, T.A., 2007. The effects of temperature on flight initiation in a range of moths, beetles and parasitoids associated with stored products. J. Stored Prod. Res. 43, 111e117. Crombie, A.C., 1941. On oviposition, olfactory conditioning and host selection in Rhyzopertha Dominica Fab. (Insecta, Coleoptera). J. Exp. Biol. 18, 62e79. Daglish, G.J., Ridely, A.W., Hereward, J.P., Emery, R.N., Holloway, J.C., Ragu, S., Walter, G.H., 2014. Investigation of dispersal and spatio-temporal distributions of stored grain insects in Australia using ecological and molecular tools. In: Arthur, F.H., Kengkanpanich, R., Chayaprasert, W., Suthisut, D. (Eds.), Proceedinsg of the 11th International Working Conference on Stored Product Protection, Chiang Mai, Thailand, November 24-28, 2014, pp. 74e78. Daglish, G.J., Ridley, A.W., Reid, R., Walter, G.H., 2017. Testing the consistency of spatio-temporal patterns of flight activity in the stored grain beetles Tribolium castaneum (Herbst) and Rhyzopertha Dominica (F.). J. Stored Prod. Res. 72, 68e74. Dowdy, A.K., McGaughey, W.H., 1994. Seasonal activity of stored product insects in and around farm stored wheat. J. Econ. Entomol. 87, 1351e1358. Drury, D.W., Siniard, A.L., Wade, M.J., 2009. Genetic differentiation among wild populations of Tribolium castaneum estimated using microsatellite markers. J. Hered. 100, 732e741. Duehl, A.J., Arbogast, R.T., Teal, P.E.A., 2011. Density-related volatile emissions and responses in the red flour beetle, Tribolium castaneum. J. Chem. Ecol. 37, 525e532. Edde, P.A., Phillips, T.W., Nansen, C., Payton, M.E., 2006. Flight activity of the lesser grain borer, Rhyzopertha Dominica F. (Coleoptera: bostrichidae), in relation to weather. Environ. Entomol. 35, 616e624. Fields, P.G., Van Loon, J., Dolinski, M.G., Harris, J.L., Burkholder, W.E., 1993. The distribution of Rhyzopertha Dominica (F.) in Western Canada. Can. Entomol. 125, 317e328. GenStat 11 Committee, 2008. GenStat for Windows, Release 11.1. VSN International Ltd., Oxford, UK. Good, N.E., 1933. Biology of the flour beetles, Tribolium confusum Duv. And Tribolium ferrugineum Fab. J. Agric. Res. 46, 327e334. Grenier, A.M., Nardon, C., Nardon, P., 1994. The role of symbiotes in flight activity of Sitophilus weevils. Entomol. Exp. Appl. 70, 201e208. Halstead, D.G.H., 1963. External sex differences in stored product Coleoptera. Bull. Entomol. Res. 54, 119e134. Kiritani, K., 1965. Biological studies on the Sitophilus complex (Coleoptera; Curculionidae) in Japan. J. Stored Prod. Res. 1, 169e176.
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Leos-Martinez, J., Granovsky, T.A., Williams, H.J., Vinson, B., Burkholder, W.E., 1986. Estimation of aerial density of the lesser grain borer (Coleoptera: bostrichidae) in a warehouse using Dominica lure traps. J. Econ. Entomol. 79, 1134e1138. Likhayo, P.W., Hodges, R.J., 2000. Field monitoring Sitophilus zeamais and Sitophilus oryzae (Coleoptera: Curculionidae) using refuge and flight traps baited with synthetic pheromone and cracked wheat. J. Stored Prod. Res. 36, 341e353. Mahroof, R.M., Edde, P.A., Robertson, B., Puckette, J.A., Phillips, T.W., 2010. Dispersal of Rhyzopertha Dominica (Coleoptera: bostrichidae) in different habitats. Environ. Entomol. 39, 930e938. McKay, T., White, A.L., Starkus, L.A., Arthur, F.H., Campbell, J.F., 2017. Seasonal patterns of stored-product insects at a rice mill. J. Econ. Entomol. 110, 1366e1376. Nopsa, J.F.H., Daglish, G.J., Hagstrum, D.W., Leslie, J.F., Phillips, T.W., Scoglio, C., Thomas-Sharma, S., Walter, G.H., Garrett, K.A., 2015. Ecological networks in stored grain: key postharvest nodes for emerging pests, pathogens, and mycotoxins. Bioscience 65, 985e1002. Rafter, M.A., Ridley, A.W., Daglish, G.J., Burrill, P.R., Walter, G.H., 2015. Flight directionality of Tribolium castaneum soon after take-off under glasshouse and field conditions. Entomol. Exp. Appl. 156, 178e186. Rafter, M.A., McCulloch, G.A., Daglish, G.J., Gurdasani, K., Walter, G.H., 2018. Polyandry, genetic diversity and fecundity of emigrating beetles: understanding new foci of infestation and selection. J. Pest. Sci. https://doi.org/10.1007/s10340017-0902-8 (in press). Ridley, A.W., Hereward, J.P., Daglish, G.J., Raghu, S., Collins, P.J., Walter, G.H., 2011. The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and
gene flow. Mol. Ecol. 20, 1635e1646. Ridley, A.W., Hereward, J.P., Daglish, G.J., Raghu, S., McCulloch, G.A., Walter, G.H., 2016. Flight of Rhyzopertha Dominica (Coleoptera: bostrichidae) e a spatiotemporal analysis with pheromone trapping and population genetics. J. Econ. Entomol. 109, 2561e2571. Sinclair, E.R., Haddrell, R.L., 1985. Flight of stored products beetles over a grain farming area in southern Queensland. J. Aust. Entomol. Soc. 24, 9e15. Throne, J.E., Cline, L.D., 1989. Seasonal flight activity of the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), and the rice weevil, S. oryzae (L.), in South Carolina. J. Agric. Entomol. 6, 183e192. Throne, J.E., Cline, L.D., 1994. Seasonal flight activity and seasonal abundance of selected stored-product Coleoptera around grain storages in South Carolina. J. Agric. Entomol. 11, 321e338. Toews, M.D., Campbell, J.F., Arthur, F.H., Ramaswamy, S.B., 2006. Outdoor flight activity and immigration of Rhyzopertha Dominica into seed wheat warehouses. Entomol. Exp. Appl. 121, 73e85. White, G.G., 1981. Undetected infestation in wheat deliveries from farm. In: Williams, P.A., Amos, T.G. (Eds.), First Australian Stored Grain Pest Control Conference. Commonwealth Scientific and Industrial Research Organization, Melbourne, pp. 13e17. Wright, E.J., Morton, R., 1995. Daily flight activity of Trogoderma variabile (Coleoptera: Dermestidae) and Rhyzopertha Dominica (Coleoptera: bostrichidae). J. Stored Prod. Res. 31, 177e184.
Contents lists available at ScienceDirect
Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat T. Sonai Rajan a, V. Muralitharan a, G.J. Daglish b, S. Mohankumar c, M.A. Rafter d, S. Chandrasekaran a, S. Mohan a, D. Vimal e, Chitra Srivastava e, M. Loganathan f, G.H. Walter d, * a
Department of Agricultural Entomology, Centre for Plant Protection Studies, Tamil Nadu Agricultural University, Coimbatore e 03, India Department of Agriculture and Fisheries, EcoSciences Precinct, GPO Box 267, Brisbane, Queensland 4001, Australia Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore e 03, India d School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia e Division of Entomology, Indian Agricultural Research Institute, Pusa Campus, New Delhi e 12, India f Department of Primary Processing, Storage and Handling, Indian Institute of Food Processing Technology, Thanjavur e 05, India b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 October 2017 Received in revised form 15 December 2017 Accepted 15 December 2017
The timing, extent and landscape coverage of the flight of stored product insect pests could influence their ecology differentially across climatic zones. We therefore assessed the seasonal flight patterns of Tribolium castaneum (Herbst), Rhyzopertha dominica (F.) and Sitophilus oryzae (L.) monthly, for 18 months, in three habitats (around bulk grain storage, in cropping habitats, and in mixed orchard habitats) in southern India (Coimbatore and Thanjavur) and northern India (New Delhi) using pheromone traps. We tested for species-specificity in their seasonal flight patterns as well as regional variation. Vastly more beetles were trapped near bulk grain storages than in cropping and orchard habitats. In both southern and northern India, T. castaneum was most numerous, with numbers much higher in southern India. Rhyzopertha dominica was more commonly trapped in New Delhi, a wheat producing region, than in the rice producing south. The numbers of T. castaneum trapped across time and geographical location varied significantly, with peak flight activity during the post-monsoon period (October). By contrast, R. dominica in New Delhi peaked once during summer (May) around bulk storage but tended to be more consistent (but far less numerous) in habitats away from storage. Only a few S. oryzae were caught in pheromone traps. The mean trap catches of T. castaneum in Thanjavur and New Delhi showed significant positive correlations with minimum temperatures, whereas those of R. dominica in New Delhi were significantly correlated with maximum temperatures. The patterns recorded are consistent with results recorded on other continents, but temperature thresholds for flight need to be examined in this context. A major difference was that beetles, especially T. castaneum, were captured far less frequently in traps away from storage in India than in Australia, a pattern that needs to be confirmed before a biological basis for it is sought. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Seasonal flight pattern Tribolium castaneum Rhyzopertha dominica Sitophilus oryzae India Pheromone traps
1. Introduction The role of movement in the ecology of insect pests of stored products is difficult to interpret because these organisms are moved in significant numbers with the bulk transport of commodities, and most are also able to fly. Disentangling the relative
* Corresponding author. Present/Permanent Address: School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. E-mail address: [email protected] (G.H. Walter). https://doi.org/10.1016/j.jspr.2017.12.005 0022-474X/© 2017 Elsevier Ltd. All rights reserved.
contributions of these processes to the rate of infestation of bulk stored grain is in its infancy and is, despite its relevance to the environmentally sound management of these pests and the effective management of phosphine resistance, currently a major challenge in understanding the ecology of these species. Each mode of pest movement has to be understood in its own right before their relative contributions can be assessed (Nopsa et al., 2015). The different beetle species involved are known for their differential flight propensities and abilities, but even these are not yet well understood, and the depth of understanding of the movement of
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pest grain beetles varies with species and region. Tribolium castaneum (Herbst) is believed to generate new infestations in bulk grain storage primarily through the anthropogenic transport of commodities (Good, 1933; White, 1981; Campbell and Arbogast, 2004; Drury et al., 2009; Campbell et al., 2010). This view has presumably been nurtured by those who have used this species as a “model organism” in ecology, as insects that do not fly (as explained by Ridley et al. (2011)). Recent investigations of the spatio-temporal pattern of T. castaneum movement across subtropical cropping regions of eastern Australia (a site in which movement of grain between storages is limited) have found that these beetles are routinely captured in flight (throughout the year), even at distances >1 km from bulk-stored grain (Ridley et al., 2011; Daglish et al., 2017). These trapping data, together with population genetic analyses on the trapped insects, indicate that the beetles fly often enough and far enough to render the entire population genetically homogenous over relatively large areas (7000 km2) (Ridley et al., 2011). Rhyzopertha dominica (F.), by contrast, is characterized as a strong flier that can be intercepted in flight at substantial distances from grain storage (Cogburn, 1988; Edde et al., 2006; Ridley et al., 2016), and this species has been demonstrated to disperse across diverse environments (Mahroof et al., 2010). Studies of R. dominica dispersal have been concentrated in temperate and subtropical areas of the United States (Leos-Martinez et al., 1986; Throne and Cline, 1994; Edde et al., 2006; Toews et al., 2006 Mahroof et al., 2010), Canada (Fields et al., 1993) and Australia (Sinclair and Haddrell, 1985; Wright and Morton, 1995; Ridley et al., 2016). Most of these studies have found that R. dominica is active only in summer in temperate areas (Sinclair and Haddrell, 1985; Throne and Cline, 1994), but also in small numbers even in the coldest months in subtropical areas (Ridley et al., 2016; Daglish et al., 2017). Sitophilus oryzae (L.) has been captured in flight in the vicinity of stored grain in several countries, in both passive traps and traps baited with aggregation pheromone lures (Sinclair and Haddrell, 1985; Throne and Cline, 1989; Likhayo and Hodges, 2000). Laboratory studies on this species have evidently revealed variation across populations in their propensity for flight (Grenier et al., 1994; Cox et al., 2007), and only those strains infected with the endosymbiont Wollbachia seem able to fly in the laboratory (Grenier et al., 1994). Despite evidence of flight by S. oryzae in the vicinity of stored grain, only limited information is available on the potential for more extensive flights by this species. Specifically, Sinclair and Haddrell (1985) captured small numbers of beetles in farm fields using sticky traps and with a trap mounted on a moving vehicle. Spatio-temporal data on the flight of storage pests in a heterogeneous agricultural landscape in a tropical monsoonal climate, such as that of India, are not available. We therefore conducted a monthly trapping survey, over 18 months, to determine the movement of T. castaneum, R. dominica and S. oryzae within various habitats close to and at a distance from bulk grain storage in two different climatic regions of India. India stores (and moves) vast quantities of food grains in bulk throughout the year, particularly rice and wheat, and significant post-harvest grain losses caused by insect pests have been reported. Also, households store small quantities of grain for consumption, and our trapping sites were essentially urban (at bulk storage depots) or peri-urban (with respect to the other habitats). Based on earlier reports on pheromone trapping of flying beetle pests of stored grain (Ridley et al., 2011, 2016; Daglish et al., 2017) we predicted that trap catches of T. castaneum and R. dominica would be much higher near bulk storage in India than those captured near bulk stores in Australia. We also anticipated that trap catches in habitats away from bulk storage (in cropping and mixed
orchard habitats) would be disproportionately higher (relative to results from bulk storage sites) than in Australia. These expectations relate to our initial observations in India, where vast numbers of beetles can be readily observed each day in the late afternoon, crawling on the surfaces of bag stacks and taking to flight. In Australia, by contrast, T. castaneum and R. dominica beetles can be observed flying from bulk grain storage and can be trapped near storage, but numbers tend to be low and on some days no beetles take flight (Ridley et al., 2011, 2016; Rafter et al., 2015, 2018). We also anticipated that the flight of these beetles would be less seasonal in southern India than it is in Australia, where temperatures differ more strongly across seasons. In northern India, however, we anticipated strong seasonality in flight activity because of the wider seasonal range in temperatures there than in southern India. 2. Materials and methods 2.1. Study locations Trapping was undertaken at two locations in southern India [at Coimbatore (11.0183 N, 76.9725 E) and Thanjavur (10.7825 N, 79.1313 E), both in Tamil Nadu] and one in northern India [at New Delhi (28.6139 N, 77.2089 E)]. We deployed multidirectional flight traps baited with species-specific aggregation pheromone lures. The distance between the two southern locations is about 250 km, and 1800 km between New Delhi and each of the southern locations. Tamil Nadu is close to the equator and tends to be relatively warm and stable climatically, whereas a wide seasonal range of temperatures typifies New Delhi (Fig. 1). A monsoon season occurs in both northern and southern India. The southwest monsoon affects the entire country from June to September and the northeast monsoon brings rain to Tamil Nadu from October to December (Fig. 1). Rice is the main cereal crop in southern India, whereas wheat is the main crop in northern India. Despite this, rice and wheat are routinely transported in bulk across the whole of India, and is bulk stored in areas where it is not grown. 2.2. Sampling Thirty traps were set at each of the three geographical localities, with 10 traps placed at each of three habitats within each locality. The habitats included areas around bulk grain storage (in warehouses called godowns, with grain held in 50 kg jute sacks), cropping (rice or wheat fields) and mixed orchard (fruit and vegetable crops) habitats. These three habitats within each locality were separated by 5, 3 and 8 km (Coimbatore), 10, 11 and 14 km (Thanjavur), and 1.5, 2.5 and 1.5 km (New Delhi) from one another. Each trap was suspended 1.5 m from the ground on a steel pole and was at least 30 m from any other trap. The traps were custom made of galvanized iron for the study (Melwin Engineering Pvt. Ltd., Coimbatore) (Fig. 2). Each trap was baited with three species-specific pheromone lures, one each for T. castaneum, R. dominica and S. oryzae (Insects Limited Inc., Westfield, IN, USA). Traps were set for the first 7 days of each month, starting from September 2013 and continuing until February 2015 for all three locations, except for the trapping period in November 2014 at Coimbatore, when no trapping could be conducted. New pheromone lures were used for each trapping period. At the end of each week's trapping, the numbers of T. castaneum, R. dominica and S. oryzae adults were counted and sexed. Fifty beetles of each species (if fewer than this were trapped, then all beetles in the sample) from randomly selected traps (one from each habitat at all three locations) were sexed each month. Male and female adults of T. castaneum were identified by the presence (male) or absence (female) of a sub-basal setiferous
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Fig. 2. Multidirectional pheromone trap used in the field study of seasonal flight of stored grain insect pests. The traps were constructed from galvanized iron and were hung 1.5 m from the ground.
77.162018 E), and at each of which data were taken manually, once a day, from a Single Stevenson Screen (IS Standard IMD, Pune) containing a minimum, maximum and wet and dry bulb thermometer. 2.3. Statistical analyses
Fig. 1. Seasonal climatic data for the two trapping locations in southern India A) Coimbatore and B) Thanjavur and the northern trapping location of C) New Delhi. Solid black lines represent the mean monthly temperatures recorded during the study and dashed black lines represent the 25 year monthly average temperature (maximum and minimum temperatures). Dark grey bars represent total rainfall recorded each month during the period of the study and light grey bars the 25 year mean monthly rainfall. The vertical light grey shading represents the north-east monsoon (OctobereNovember) which brings rainfall to A) Coimbatore and B) Thanjavur in the south and the south-west monsoon (JuneeSeptember) which brings rainfall to C) New Delhi in the North.
puncture on the ventral side of the anterior femora (Halstead, 1963). As there are no consistent external differences between adult males and females of R. dominica, they were distinguished by squeezing each beetle until the tip of its genitalia appeared (Crombie, 1941). Sitophilus oryzae was not trapped in numbers high enough to warrant further investigation. The monthly ambient weather data, namely minimum and maximum temperature ( C), total rainfall (mm) and relative humidity (%), were sourced from (i) the Department of Agricultural Meteorology, Tamil Nadu Agricultural University, Coimbatore (11.015186 N, 76.932617 E), (ii) the Soil and Water Management Research Institute, Kattuthottam, Thanjavur (10.7815 N, 79.1767 E), and (iii) the Division of Agricultural Physics, Indian Agricultural Research Institute, New Delhi (28.639256 N,
The numbers of T. castaneum and R. dominica caught at the bulk grain storage habitats in southern India (Coimbatore and Thanjavur) and northern India (New Delhi) were each analyzed using repeated measures ANOVA (Genstat, 2008) to investigate the effects of geographic location (Coimbatore, Thanajvur or New Delhi) and trapping date. Insufficient numbers of T. castaneum and R. dominica were caught within any of the cropping and mixed orchard habitats to be analyzed statistically (see results). The data were transformed (loge (Nþ1)) before analysis to conform to the assumptions of ANOVA. Fisher's Protected LSD was used for multiple comparisons after running the repeated measures ANOVA in GenStat as all the effects in the means must be estimated in the same stratum with the same efficiency factors for methods other than Fisher's Protected LSD. A simple correlation matrix was also created to assess the possible influence of minimum and maximum temperatures, total rainfall, and relative humidity on the seasonal flight patterns of T. castaneum and R. dominica around bulk grain storage areas. A Chisquare test for independence was used to compare the proportions of male T. castaneum caught at the bulk grain storage area of southern India with the proportion of females, but such an analysis was not undertaken for R. dominica trapped near bulk grain storage in New Delhi because of the low numbers of individuals (<50 per month) caught (see results). In all cases the a threshold for assessing statistical significance was 0.05. 3. Results Temperature and rainfall profiles recorded during the study at facilities near each of the three main sampling localities
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Table 1 Total numbers of Tribolium castaneum, Rhyzopertha dominica and Sitophilus oryzae trapped in pheromone traps over 18 months in each of three different habitats (bulk storage (godowns), grain cropping habitats, and mixed orchard habitats) across three geographical localities in India. Location
Coimbatore Thanjavur New Delhi Total
Tribolium castaneum
Rhyzopertha dominica
Sitophilus oryzae
Godown
Cropping
Orchard
Godown
Cropping
Orchard
Godown
Cropping
Orchard
23,746 25,019 5545 54,310
18 0 130 310
35 16 87 138
297 50 2691 3038
57 47 109 213
25 179 171 375
11 0 65 76
3 0 3 6
3 0 2 5
approximated the 25 year averages for those localities (Fig. 1). Significantly more beetles were trapped in bulk grain storage habitats than in cropping and mixed orchard habitats of southern and northern India. The most abundant species caught was T. castaneum across all of the localities sampled (Table 1). Rhyzopertha dominica was caught in higher numbers in northern India (New Delhi) compared to the two southern sampling locations (Table 1). Few S. oryzae were caught at any of the godowns or agricultural environments of southern and northern India (Table 1).
3.1. Tribolium castaneum Substantial numbers of T. castaneum were caught during the 18month trapping period at bulk grain storage habitats in Coimbatore (23,746), Thanjavur (25,019) and New Delhi (5,545) (Table 1). Totals of 310 and 138 T. castaneum were caught in the three cropping and mixed orchard habitats, respectively (Table 1). Repeated measures ANOVA analysis showed significant variation in the numbers of T. castaneum trapped across the three geographical locations
Fig. 3. Seasonal trapping of Tribolium castaneum in New Delhi in the northern monsoonal tropics of India, and in two locations (Coimbatore and Thanjavur) in the southern monsoonal tropics of India. In each locality traps were set in three habitats. (A) Bulk grain storage (godown), where mean numbers (±1SE) of beetles are given for each trapping period at each of the three locations. (B) grain growing area, and (C) mixed orchard, in both of which totals of beetles are given for each trapping period at each location (because captures were so low and included mostly zeros). The pheromone traps were monitored for 7 days each month over 18 months (September 2013eFebruary 2015).
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Table 2 Results of correlation analyses run on trap catches of Tribolium castaneum and Rhyzopertha dominica across three localities in India against maximum and minimum temperatures. Location
Coimbatore Thanjavur New Delhi a
Tribolium castaneum
Rhyzopertha dominica
Minimum Temperature
Maximum Temperature
Minimum Temperature
Maximum Temperature
rs ¼ 0.199, P ¼ .538 rs ¼ 0.525, P ¼ .025a rs ¼ 0.510, P ¼ .031a
rs ¼ 0.309, P ¼ .213 rs ¼ 0.389, P ¼ .111 rs ¼ 0.363, P ¼ .139
rs ¼ 0.290, P ¼ .243 rs ¼ 0.083, P ¼ .744 rs ¼ 0.429, P ¼ .076
rs ¼ 0.030, P ¼ .906 rs ¼ 0.002, P ¼ .993 rs ¼ 0.495, P ¼ .037a
Correlation significant at 0.05 level.
(F2,27 ¼ 60.07, P < .001) and across the 18-month study period (F16,432 ¼ 11.10, P < .001). Also, a significant interaction was evident between geographical location and study period (F32,432 ¼ 6.99, P < .001). In southern India, the monsoonal periods of October and November 2013 and June to August 2014 returned the highest trap catches of T. castaneum around godowns. Trap catches during winter (January to February), and after that (up to May), were relatively low (Fig. 3). In northern India, the highest trap catches of T. castaneum were associated with the post monsoon period of October and September 2014, and only a few were captured during the winter period of December to January (Fig. 3). The mean trap catches of T. castaneum at the bulk grain storage habitats of Thanjavur and New Delhi showed significant positive correlations with minimum temperatures (Pearson correlation analysis) (Table 2). There was no correlation of mean trap catches of T. castaneum and any of the weather variables measured in the other south Indian location, Coimbatore (Table 2). At New Delhi, the mean minimum temperatures associated with T. castaneum flight were 4.8 (January 2014), 7.1 (December 2013), 8.6 (February 2014) and 9.3 C (March 2014). The proportions of T. castaneum females caught in the traps placed around the bulk grain storage areas of Coimbatore (n ¼ 7744) and Thanjavur (n ¼ 4615) were consistently > 50%, with a mean of 59.6 and 56.4% respectively. However, Chi-square analysis showed there were no significant differences in the proportion of male to female T. castaneum (c2 ¼ 0.194; df ¼ 1; p ¼ .723).
3.2. Rhyzopertha dominica The highest numbers of R. dominica were caught in the bulk grain storage habitat of northern India (2,691), whereas only 297 (Thanjavur) and 50 (Coimbatore) individuals were caught throughout the entire study period at bulk grain storage areas in southern India (Table 1). Significant differences were strongly evident in the numbers of R. dominica trapped over 18 months (F16,432 ¼ 7.39, P < .001) as well as across all three geographical locations (F2,27 ¼ 24.31, P < .001). A significant interaction between the locations and study period was also clear (F32,432 ¼ 9.46, P < .001). In Coimbatore, maximum trap catches of R. dominica at godowns were recorded during the pre-monsoon period of June to July 2014, and negligible trap catches were recorded through the rest of the year (Fig. 4). In Thanjavur more R. dominica were trapped in the orchard habitat than around the godown (Fig. 4). Trap captures in the Thanjavur orchard habitat peaked during January and February in both 2014 and 2015 (Fig. 4). Trap catches of R. dominica in northern India were highest in May 2014 and this correlated significantly with maximum temperature (Fig. 4, Table 2). Rhyzopertha dominica was trapped in low numbers in cropping and mixed orchard habitats in southern and northern India, and the catches were more evenly spread across the seasons (Fig. 4). More females than males were caught in the bulk grain storage area of New Delhi.
3.3. Sitophilus oryzae Totals of 11 and 65 individuals of S. oryzae were caught at bulk grain storage areas of Coimbatore and New Delhi, respectively (Table 1). In total, only 11 individuals were caught in grain growing and mixed orchard habitats in Coimbatore and New Delhi. No S. oryzae were caught at any of the three habitats in the second southern Indian location, Thanjavur (Table 1).
4. Discussion We interpret the flight data for each of T. castaneum and R. dominica independently, and these insights allow a comparison, for each species, across other such studies of flight in the field. We can thus deduce what is species-specific with respect to the flight of each species, and then how these species-specific aspects are influenced by local conditions of climate and other variables. The negligible trap catches of S. oryzae (Table 1) are open to interpretation and further investigation is needed to resolve whether these beetles do not fly much or whether flying adults are not much attracted to the pheromone lure, with similar low numbers having been captured in Western Australia (Daglish et al., 2014). Note that Kiritani (1965) reported no flight in a Japanese population of this species. The trapping data show that T. castaneum and R. dominica differ from one another in their relative abundance across the geographical areas sampled in India, but this does assume that the trapping system and pheromone lures have roughly equivalent efficiencies across these two species and across latitudes. Although that assumption is unlikely, the differences across north and south are of an order of magnitude, so comparison is valid. In both northern and southern India, the most prevalent beetle species trapped was T. castaneum, with total catch being much higher in the south (>23,000 beetles in each locality vs 5545 in the north) (Table 1). Rhyzopertha dominica was more prevalent in New Delhi (total of 2691 beetles) than it was in Tamil Nadu (maximum of 297), presumably because the north is where wheat is mainly grown in India, and where it is the predominant commodity in storage (Table 1). Further, the vast majority of beetles of both species were trapped at bulk grain storage areas with far fewer beetles caught in the pheromone traps placed away from these areas (cropping and orchard habitats) (Table 1), a point that is expanded below. Regardless of trap efficiency, the seasonal pattern of T. castaneum flight differed substantially from that of R. dominica. The trap catches of T. castaneum showed that these insects flew throughout the year in southern India (Fig. 3), but flight was seasonal in the north where it was presumably too cold for flight in winter (<20 C maxima in New Delhi (Fig. 1)). The numbers of beetles trapped flying across the agricultural landscape in the north was, again, restricted to the warmer months (mainly July to October) (Fig. 3). Similar flight patterns have been reported in various parts of Australia (Ridley et al., 2011; Daglish et al., 2017) and in the USA (Campbell et al., 2010). In general, all of these results
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Fig. 4. Seasonal trapping of Rhyzopertha dominica in New Delhi in the northern monsoonal tropics of India, and in two locations (Coimbatore and Thanjavur) in the southern monsoonal tropics of India. In each locality traps were set in three habitats. (A) Bulk grain storage (godown), where mean numbers (±1SE) of beetles are given for each trapping period at each of the three locations. (B) grain growing area, and (C) mixed orchard, in both of which totals of beetles are given for each trapping period at each location (because captures were so low and included mostly zeros). The pheromone traps were monitored for 7 days each month over 18 months (September 2013eFebruary 2015).
are consistent with the minimum temperature threshold for T. castaneum flight initiation in the laboratory being 25 C (Cox et al., 2007), with maximum trap catches of T. castaneum coinciding with temperatures above this, and especially when both minima and maxima are above this temperature, as in September, October and November in Thanjavur (with mean minimum and maximum temperatures being 27.6 and 34.8 C, 28.3 and 37.5 C, and 29.4 and 33.1 C, respectively). Tribolium castaneum beetles in flight were strongly associated with storage facilities in southern India, with a ratio of 1:0.001 beetles near bulk storage relative to trapping locations away from bulk storage. Unexpectedly low numbers of beetles (<10 beetles at each sampling occasion) were consistently trapped throughout the year in the south in cropping and orchard habitats, but mainly at the Coimbatore site (Fig. 3). In northern India, the equivalent ratio was 1:0.039 beetles. These ratios are extremely low when compared with the ratio of beetles flying near bulk storage relative to those flying one km away from storage in Australia (1:0.4 beetles, see Fig. 2, Ridley et al., 2011). The difference in these ratios across the continents was against prediction, because we expected beetles to be leaving high density infestations in India at greater relative
frequencies. This result implies that emigration is not driven by density or, at least, is not driven primarily by density, even though these beetles tend to be repelled (whilst walking) by the presence of conspecifics (Duehl et al., 2011). Clearly, tests are required to determine what these beetles do once they walk out onto the surface of the grain bags and take flight above the bag stacks. Rhyzopertha dominica has a different flight pattern from that of T. castaneum, being much more seasonal, even in the south (Fig. 4). The seasonality was, however, evident only in the catches made where grain was stored in bulk. Away from storage, in cropping and mixed orchard habitats, trap catches were much more evenly spread across the year, especially in northern India (Fig. 4). Average numbers in traps were generally much lower than those of T. castaneum, especially in southern India. The substantially greater captures of R. dominica in the north than in southern India are presumably related to the widespread and routine cultivation and storage of wheat in the area of the Gangetic Plain in northern India. It seems, therefore, that the main commodities produced and stored regionally influence the local composition of pest species, and that the bulk transport of grains does not influence this pattern to a great extent, but this needs to be tested more thoroughly,
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perhaps with population genetics markers. The numbers of R. dominica caught in traps was higher at the beginning of the season and then dropped during the winter months (Fig. 4). Maximum trap catches of R. dominica were observed during the summer season of May 2014 in the vicinity of bulk grain storages in northern India, when the average minimum and maximum temperatures were 23.2 and 39.5 C, respectively. A significant positive correlation of trap catches with maximum air temperature was detected (Table 2). Similar observations on R. dominica being most abundant during the warmest months have been reported in Australia (Sinclair and Haddrell, 1985; Ridley et al., 2016), Canada (Fields et al., 1993), and the USA (Dowdy and McGaughey, 1994; Throne and Cline, 1994; McKay et al., 2017). Consequently, the responses of flight to temperature seem quite consistent across the different populations of R. dominica that have been investigated in the field, but some variation is evident. The winter months of northern India recorded nil trap catches of R. dominica, when the mean minimum and maximum temperatures were 9.2 and 22.5 C, respectively. These findings are thus consistent with those of Sinclair and Haddrell (1985) who stated that R. dominica flight activity in the field in Queensland (Australia) was significantly reduced through the cooler months. Wright and Morton (1995) were more explicit, stating that no flight of R. dominica occurred at all when temperatures were below 16 C in northern New South Wales, Australia. In the USA, however, Toews et al. (2006) concluded that R. dominica flight activity in the field stops below 22.5 C during summer and below 17.5 C in the cooler months. Clearly, the flight threshold of this species warrants experimental investigation across different populations, to test how stable this feature is across the species. Differences in trap catches of R. dominica were evident across the traps placed in bulk grain storage areas and those placed in cropping and mixed orchard habitats (in both southern and northern India). As with T. castaneum, trap catches of R. dominica were much higher in traps placed in the vicinity of bulk grain storage than those placed in cropping and mixed orchard habitats (in both southern and northern India). However, the discrepancy was not as high as that for T. castaneum, with the ratio in northern India being 1:0.1 and that in the south being 1:0.9. This latter value was inflated by the Thanjavur traps around storage catching few beetles (Fig. 4), to the extent that the ratio for Thanjavur was 1:4.5. In Australia, the ratio was 1:1 (see Ridley et al., 2016), which implies that the behavior of R. dominica in India may be similar to that suggested for T. castaneum in the beetles being less inclined (than conspecifics in Australia) to disperse from infested bulk-stored grain. Although this behavior may not be so strongly expressed in R. dominica relative to T. castaneum, the interpretation we offer (see above) does warrant further testing. This study is the first detailed analysis of seasonal flight patterns of key stored grain insect pests across different latitudes in the monsoonal tropics of India. Perhaps the main difference, ecologically, from the results obtained by similar means in Australia (Ridley et al., 2011, 2016; Rafter et al., 2015, 2018; Daglish et al., 2017) is in the relatively low numbers of R. dominica captured in flight generally (Table 1), and the relatively low numbers of T. castaneum captured in habitats away from storage areas (Fig. 3). For R. dominica it now seems crucial to establish whether relatively few beetles fly because they are not so numerous in India or whether they do fly less (and if so, why they do so). The question with T. castaneum is whether they do fly long distances less frequently than they do in Australia. We have noticed that vast numbers of T. castaneum take flight inside godowns in the late afternoon, and establishing whether these individuals are in the process of leaving that locality would help to interpret their movement and its consequences more clearly. Ecological
49
information of this nature would facilitate the development of effective management tactics to control the spread and development of phosphine resistance and to reduce the likelihood or severity of infestations caused by these insect pests. Acknowledgements This work was financially supported by the Australia e India Strategic Research Grand Challenge Funded (GCF010006) project entitled “Ensuring food security: harnessing science to protect our grain harvest from insect threats”, jointly sponsored by the Department of Science and Technology (DST), New Delhi, India, and the Department of Innovation, Industry, Science and Research (DIISR), Canberra, Australia. We thank the managers and technical staff of the Food Corporation of India in Coimbatore, Thanjavur and New Delhi for their permission to conduct the experiments and their support throughout. We are also grateful for the thoughtful comments of an anonymous reviewer, which helped to clarify our interpretation. Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.jspr.2017.12.005. References Campbell, J.F., Arbogast, T., 2004. Stored product insects in a flour mill: population dynamics and response to fumigation treatment. Entomol. Exp. Appl. 112, 217e225. Campbell, J.F., Toews, M.D., Arthur, F.H., Arbogast, R.T., 2010. Long-term monitoring of Tribolium castaneum populations in two flour mills: rebound after fumigation. J. Econ. Entomol. 103, 1002e1011. Cogburn, R.R., 1988. Detection, distribution and seasonal abundance of Sitotroga cerealella and Rhyzopertha Dominica as indicated by pheromone-baited adhesive traps. In: Proceedings, XVIII International Congress of Entomology, 3 e 9 July 1988. University of British Columbia, Vancouver, Canada. Cox, P.D., Wakefield, M.E., Jacob, T.A., 2007. The effects of temperature on flight initiation in a range of moths, beetles and parasitoids associated with stored products. J. Stored Prod. Res. 43, 111e117. Crombie, A.C., 1941. On oviposition, olfactory conditioning and host selection in Rhyzopertha Dominica Fab. (Insecta, Coleoptera). J. Exp. Biol. 18, 62e79. Daglish, G.J., Ridely, A.W., Hereward, J.P., Emery, R.N., Holloway, J.C., Ragu, S., Walter, G.H., 2014. Investigation of dispersal and spatio-temporal distributions of stored grain insects in Australia using ecological and molecular tools. In: Arthur, F.H., Kengkanpanich, R., Chayaprasert, W., Suthisut, D. (Eds.), Proceedinsg of the 11th International Working Conference on Stored Product Protection, Chiang Mai, Thailand, November 24-28, 2014, pp. 74e78. Daglish, G.J., Ridley, A.W., Reid, R., Walter, G.H., 2017. Testing the consistency of spatio-temporal patterns of flight activity in the stored grain beetles Tribolium castaneum (Herbst) and Rhyzopertha Dominica (F.). J. Stored Prod. Res. 72, 68e74. Dowdy, A.K., McGaughey, W.H., 1994. Seasonal activity of stored product insects in and around farm stored wheat. J. Econ. Entomol. 87, 1351e1358. Drury, D.W., Siniard, A.L., Wade, M.J., 2009. Genetic differentiation among wild populations of Tribolium castaneum estimated using microsatellite markers. J. Hered. 100, 732e741. Duehl, A.J., Arbogast, R.T., Teal, P.E.A., 2011. Density-related volatile emissions and responses in the red flour beetle, Tribolium castaneum. J. Chem. Ecol. 37, 525e532. Edde, P.A., Phillips, T.W., Nansen, C., Payton, M.E., 2006. Flight activity of the lesser grain borer, Rhyzopertha Dominica F. (Coleoptera: bostrichidae), in relation to weather. Environ. Entomol. 35, 616e624. Fields, P.G., Van Loon, J., Dolinski, M.G., Harris, J.L., Burkholder, W.E., 1993. The distribution of Rhyzopertha Dominica (F.) in Western Canada. Can. Entomol. 125, 317e328. GenStat 11 Committee, 2008. GenStat for Windows, Release 11.1. VSN International Ltd., Oxford, UK. Good, N.E., 1933. Biology of the flour beetles, Tribolium confusum Duv. And Tribolium ferrugineum Fab. J. Agric. Res. 46, 327e334. Grenier, A.M., Nardon, C., Nardon, P., 1994. The role of symbiotes in flight activity of Sitophilus weevils. Entomol. Exp. Appl. 70, 201e208. Halstead, D.G.H., 1963. External sex differences in stored product Coleoptera. Bull. Entomol. Res. 54, 119e134. Kiritani, K., 1965. Biological studies on the Sitophilus complex (Coleoptera; Curculionidae) in Japan. J. Stored Prod. Res. 1, 169e176.
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T.S. Rajan et al. / Journal of Stored Products Research 76 (2018) 43e50
Leos-Martinez, J., Granovsky, T.A., Williams, H.J., Vinson, B., Burkholder, W.E., 1986. Estimation of aerial density of the lesser grain borer (Coleoptera: bostrichidae) in a warehouse using Dominica lure traps. J. Econ. Entomol. 79, 1134e1138. Likhayo, P.W., Hodges, R.J., 2000. Field monitoring Sitophilus zeamais and Sitophilus oryzae (Coleoptera: Curculionidae) using refuge and flight traps baited with synthetic pheromone and cracked wheat. J. Stored Prod. Res. 36, 341e353. Mahroof, R.M., Edde, P.A., Robertson, B., Puckette, J.A., Phillips, T.W., 2010. Dispersal of Rhyzopertha Dominica (Coleoptera: bostrichidae) in different habitats. Environ. Entomol. 39, 930e938. McKay, T., White, A.L., Starkus, L.A., Arthur, F.H., Campbell, J.F., 2017. Seasonal patterns of stored-product insects at a rice mill. J. Econ. Entomol. 110, 1366e1376. Nopsa, J.F.H., Daglish, G.J., Hagstrum, D.W., Leslie, J.F., Phillips, T.W., Scoglio, C., Thomas-Sharma, S., Walter, G.H., Garrett, K.A., 2015. Ecological networks in stored grain: key postharvest nodes for emerging pests, pathogens, and mycotoxins. Bioscience 65, 985e1002. Rafter, M.A., Ridley, A.W., Daglish, G.J., Burrill, P.R., Walter, G.H., 2015. Flight directionality of Tribolium castaneum soon after take-off under glasshouse and field conditions. Entomol. Exp. Appl. 156, 178e186. Rafter, M.A., McCulloch, G.A., Daglish, G.J., Gurdasani, K., Walter, G.H., 2018. Polyandry, genetic diversity and fecundity of emigrating beetles: understanding new foci of infestation and selection. J. Pest. Sci. https://doi.org/10.1007/s10340017-0902-8 (in press). Ridley, A.W., Hereward, J.P., Daglish, G.J., Raghu, S., Collins, P.J., Walter, G.H., 2011. The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and
gene flow. Mol. Ecol. 20, 1635e1646. Ridley, A.W., Hereward, J.P., Daglish, G.J., Raghu, S., McCulloch, G.A., Walter, G.H., 2016. Flight of Rhyzopertha Dominica (Coleoptera: bostrichidae) e a spatiotemporal analysis with pheromone trapping and population genetics. J. Econ. Entomol. 109, 2561e2571. Sinclair, E.R., Haddrell, R.L., 1985. Flight of stored products beetles over a grain farming area in southern Queensland. J. Aust. Entomol. Soc. 24, 9e15. Throne, J.E., Cline, L.D., 1989. Seasonal flight activity of the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), and the rice weevil, S. oryzae (L.), in South Carolina. J. Agric. Entomol. 6, 183e192. Throne, J.E., Cline, L.D., 1994. Seasonal flight activity and seasonal abundance of selected stored-product Coleoptera around grain storages in South Carolina. J. Agric. Entomol. 11, 321e338. Toews, M.D., Campbell, J.F., Arthur, F.H., Ramaswamy, S.B., 2006. Outdoor flight activity and immigration of Rhyzopertha Dominica into seed wheat warehouses. Entomol. Exp. Appl. 121, 73e85. White, G.G., 1981. Undetected infestation in wheat deliveries from farm. In: Williams, P.A., Amos, T.G. (Eds.), First Australian Stored Grain Pest Control Conference. Commonwealth Scientific and Industrial Research Organization, Melbourne, pp. 13e17. Wright, E.J., Morton, R., 1995. Daily flight activity of Trogoderma variabile (Coleoptera: Dermestidae) and Rhyzopertha Dominica (Coleoptera: bostrichidae). J. Stored Prod. Res. 31, 177e184.