Weight Loss and Germination Failure Caused by Psocids in Different Wheat Varieties

Transcription

1 Weight Loss and Germination Failure Caused by Psocids in Different Wheat Varieties Author(s): S. G. Gautam, G. P. Opit, K. L. Giles, and B. Adam Source: Journal of Economic Entomology, 106(1): Published By: Entomological Society of America URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 STORED-PRODUCT Weight Loss and Germination Failure Caused by Psocids in Different Wheat Varieties S. G. GAUTAM, 1 G. P. OPIT, 1,2 K. L. GILES, 1 AND B. ADAM 3 J. Econ. Entomol. 106(1): 491Ð498 (2013); DOI: ABSTRACT We investigated weight loss caused by Liposcelis entomophila (Enderlein) feeding in damaged (cracked) and intact kernels of ÔJaggerÕ variety of hard red winter wheat over a 90-d period at 30 1 C and 75 5% relative humidity. L. entomophila caused 8.5% weight loss in damaged wheat kernels, which was signiþcantly greater than the weight loss found in intact wheat kernels (0.2%). We also evaluated the suitability of six wheat varieties commonly grown in Oklahoma, namely, Jagger, ÔEndurance,Õ ÔOverley,Õ ÔJagalene,Õ ÔOK Bullet,Õ and ÔDeliverÕ to support populations of four psocid species, namely, Liposcelis bostrychophila Badonnel, L. decolor (Pearman), L. entomophila, and L. paeta Pearman over a 30-d period. The greatest population increase was observed in L. bostrychophila followed by L. paeta. Subsequently, weight loss of damaged and intact wheat kernels and germination of intact kernels infested by L. paeta over a 45-d period were assessed in OK Bullet variety. L. paeta caused weight loss of 3.3% in damaged kernels, which was signiþcantly greater than the weight loss found in intact kernels (0.4%). Based on our data, 40% of infested intact kernels failed to germinate after 45 d of infestation by L. paeta, but this decreased to 32% when adjusted using germination failure of uninfested kernels. Our data show that psocid infestations do not only cause considerable loss in weight of wheat, but also result in signiþcant germination failure. These data call for the formulation of effective integrated psocid management strategies for stored wheat to mitigate the negative impacts of psocid pests. KEY WORDS stored product, Psocoptera, booklouse, Liposcelis, insect pest Stored food commodities around the world require protection from deterioration and loss of value as a result of loss of quality and weight during storage. During the last two decades, some insects in the order Psocoptera (psocids, dustlice, booklice, or barklice) have emerged as serious pests of stored commodities worldwide (Kučerová 2002; Rees 2003, 2004; Nayak 2006; Phillips and Throne 2010). In the past, psocids were viewed as nuisance secondary pests of low economic importance. This misleading view of psocids could have been because of their small size and limited information available on their ecology (Athanassiou et al. 2009). Psocids are now known to be capable of surviving and reproducing on whole kernels of rice, Oryza sativa L.; oat, Avena sativa L.; sorghum, Sorghum bicolor (L.) Moench; and maize, Zea mays L. (Athanassiou et al. 2010). The ability of psocids to feed on sound raw grain kernels enhances their economic risk compared with secondary stored-product pest species Trade names or commercial products mentioned in this publication is solely for the purpose of providing speciþc information and does not imply recommendation or endorsement by Oklahoma State University. 1 Department of Entomology and Plant Pathology, Oklahoma State University, 127 Noble Research Center, Stillwater, OK Corresponding author, george.opit@okstate.edu. 3 Department of Agricultural Economics, Oklahoma State University, 413 Ag Hall, Stillwater, OK (Athanassiou et al. 2010). In certain parts of some countries such as Australia, they have now become the most frequently encountered pest in recent years (Rees 2003). The relative importance of psocids as stored-product pests has risen because of the weight losses psocids cause by consumption of germ and endosperm (McFarlane 1982, Kučerová 2002), their ability to spread fungal pathogens thereby making them a potential human health threat (Obr 1978, Kalinovic et al. 2006), allergic responses they cause in sensitized people (Turner et al. 1996), frequent failure of standard practices of protection and disinfestation to control psocids (Wang et al. 1999, Beckett and Morton 2003, Nayak et al. 2003, Nayak and Daglish 2007), and the fact that commodities infested by psocids can be rejected for export (Kučerová 2002, Nayak 2006). As previously mentioned, psocids can cause significant weight losses in stored food commodities (Mc- Farlane 1982, Kučerová 2002). Psocids caused weight losses of up to 10% over a 90-d period in damaged wheat (broken wheat kernels) (Kučerová 2002). In Bogor, Indonesia, a psocid population density as high as 4,262 insects per kilogram has been reported infesting stored rice (Haines 1983). Psocid numbers this high probably result in signiþcant weight losses and product deterioration. Kučerová (1999) investigated the suitability of 10 Czech Republic wheat varieties for their susceptibility to infestation by Liposcelis bostry /13/0491Ð0498$04.00/ Entomological Society of America

3 492 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1 chophila Badonnel (Psocoptera: Liposcelididae). In that study, psocid progeny production and damage to whole kernels were criteria used to assess susceptibility of wheat varieties. SigniÞcant differences in progeny production and in the percentage of kernels damaged by psocid feeding were found among varieties (Kučerová 1999). That study also showed that seeds that had their germ damaged by psocids did not germinate. This means that not only do psocids cause product deterioration and weight losses, but they also result in reduced germination of seeds. Despite the United States being a world leader in wheat production, there is no published information on weight losses caused by psocids in United States wheat varieties and on the suitability of these varieties for psocid population growth. Additionally, there is a lack of information on the relationship between psocid infestation and seed germination in these varieties. Therefore, the objectives of this study were to determine weight losses caused by psocids in different wheat varieties, assess the suitability of these varieties to support psocid population growth, and evaluate the impact of psocid infestation on germination. Materials and Methods Insects. Cultures of L. bostrychophila and Liposcelis paeta Pearman used in the study were started using insects collected from a grain elevator located at the Center for Grain and Animal Health Research (CGAHR), Manhattan, KS. Cultures of Liposcelis decolor (Pearman) and Liposcelis entomophila (Enderlein) were started using insects collected from steel bins containing wheat located at CGAHR. Voucher specimens of 100 female L. bostrychophila, and 100 male and female L. decolor, L. entomophila, and L. paeta preserved in 95% ethyl alcohol that were used in this study were deposited at K. C. Emerson Entomology Museum at Oklahoma State University under lot numbers 106, 108 and 107; 109 and 110; and 112 and 111, respectively. Psocids were reared on a mixture of 77% cracked hard red winter wheat (Triticum aestivum L.) (ÔJaggerÕ), 15% Rice Krispies (Kellogg North America Company, Battle Creek, MI), and 8% wheat germ (The Quaker Oats Company, Chicago, IL) (wt: wt) in 360-ml glass canning jars with mite-proof lids (Opit and Throne 2008). The top one-third of the inner surface of each jar was covered with Fluon (polytetraßuoroethylene; Northern Products, Woonsocket, RI) to prevent psocids accessing and gathering on the inside of the lid. Cultures were maintained at 30 1 C and 75 5% relative humidity (RH). Weight Loss Caused by L. entomophila Feeding. Kernels of Jagger variety of hard red winter wheat were ground using a Cast Iron Grain Grinder (Corona Landers CIA.S.A., Medellin, Colombia) to obtain 100 g of cracked wheat that were stored in a freezer for 2 wk before use to prevent insect infestation. The cracked wheat will subsequently be referred to as damaged kernels or wheat. The same weight of intact wheat kernels was obtained by examining kernels under a stereomicroscope (Stemi 2000-C, Carl Zeiss, Thornwood, NY) and selecting intact ones, which were then stored in a freezer. The kernels were examined under a stereomicroscope to ensure that they did not have any surface cracks or holes that could have resulted from handling and/or prior infestation. Thirty six plastic vials (35 60 mm high) were used for the experiment. Fluon was applied to the top one-third of the inner portion of each vial which had a snap cap screen lid to allow movement of air and moisture and to prevent psocids from escaping. Two grams of damaged kernels were weighed out using a milligram scale (Denver Instruments M-220, Cambridge ScientiÞc, Watertown, MA) and placed in each of 18 plastic vials and the same weight of intact kernels was placed in each of the remaining 18 vials. This 2-g weight will be referred to as the initial weight. Thirty adult female L. entomophila were added to each of six vials containing damaged kernels and to each of six vials containing intact kernels. Similarly, 60 adult females were added to each of six vials containing damaged kernels and to each of six vials containing intact kernels. Six vials containing damaged kernels and another six with intact kernels were kept as control treatment vials and no psocids were added to them. The weight of wheat in the control vials was used to adjust for the weight loss in the vials containing psocids to facilitate the accurate determination of weight loss because of psocid feeding at the end of the experiment. All vials were kept in a plastic box ( cm high) that had saturated NaCl solution beneath the false ßoor to maintain 75 5% RH (Greenspan 1977). The box was placed in an incubator maintained at 30 1 C. After 90 d, the psocids in each vial were counted and removed using a moist camelõs hair-brush to separate them from the damaged and intact kernels. The experimental design was a completely randomized design (CRD) and each treatment was replicated six times. Statistical procedures were accomplished using Statistical Analysis System software (SAS Institute 2010). PROC GLM was used for analysis of variance (ANOVA) to determine the effect of initial population of L. entomophila and type of diet (damaged or intact kernels) on number of psocids and percentage of weight loss at the end of the experiment. The numbers of psocids and percentages of weight loss were transformed using the square-root and arcsine squareroot transformations, respectively, to stabilize variances. Untransformed means and standard errors are reported to simplify interpretation. Suitability of Wheat Varieties for Liposcelis Species. Six hard red winter wheat varieties commonly grown in Oklahoma, namely, Jagger, ÔEndurance,Õ ÔOverley,Õ ÔJagalene,Õ ÔOK Bullet,Õ and ÔDeliverÕ were tested for their suitability to support population growth of L. bostrychophila, L. decolor, L. entomophila, and L. paeta. The latter three species were investigated because they are commonly found infesting wheat in large numbers in storage facilities in the United States whereas L. bostrychophila was included to enable us to compare data for this species with that obtained from previous studies (Kučerová 1999, 2002). One hundred grams of each wheat variety were weighed out and

4 February 2013 GAUTAM ET AL.: WEIGHT LOSS AND GERMINATION FAILURE CAUSED BY PSOCIDS 493 ground for 2 min using a Cast Iron Grain Grinder (Corona Landers CIA.S.A.). Grinding was done to obtain small pieces of cracked wheat that were then kept in a freezer for 2 wk before use to prevent infestation by insects. Before grinding different varieties of wheat, the grinder was washed thoroughly and placed in an oven for 1 h to minimize mixing of varieties. Five grams of damaged (ground) kernels of each variety was placed in each of 16 plastic vials (35 60 mm high), that is, there were a total of 96 vials for the six varieties. The top one-third of the inner surface of each vial had a coat of Fluon to prevent psocids from escaping. Plastic vials had snap-cap screen lids to allow air and moisture movement. The 96 vials containing wheat were equilibrated in a plastic box ( cm high) that had saturated NaCl solution beneath the false ßoor to maintain 75 5% RH for 4 wk, at room temperature, before use. The RH in each box was monitored weekly using HOBO data logger (Onset Computer Corporation, Bourne, MA; model U12-011). After 4 wk of wheat equilibration, 16 vials containing damaged kernels of each variety were randomly divided into four groups of four vials each and each group was assigned one of four psocid species, namely, L. bostrychophila, L. decolor, L. entomophila, or L. paeta. Accordingly, Þve adult female psocids from our cultures were placed in each vial. Vials were then placed in a plastic box ( cm high) containing saturated NaCl solution beneath the false ßoor to maintain 75 5% RH. The box was placed in an incubator maintained at 30 1 C. After 30 d, all motile insects in each vial were counted by pouring the contents of each vial into a 15-cm petri dish with Fluon-coated walls, and examining contents under a stereomicroscope. The number of nymphs and adult males and females in each vial were counted and removed using a moist camelõs hair-brush. The experiment consisted of three replications over time and the experimental design used was a randomized complete block design with subsampling. Statistical procedures were accomplished using Statistical Analysis System software (SAS Institute 2010). PROC MIXED was used for the ANOVA to determine the effect of wheat variety and psocid species on psocid population after 30 d. We used a least signiþcant difference (LSD) test to determine differences among mean numbers of psocids of the four species and six wheat varieties. Effects of L. paeta Infestation on Kernel Weight and Germination. As previously mentioned, the three Liposcelis species that commonly infest wheat in commercial storage facilities in the United States are L. decolor, L. entomophila, and L. paeta. We determined, from the experiment on suitability of wheat varieties for Liposcelis species, that L. paeta populations were numerically higher on nearly all wheat varieties and across wheat varieties. The numbers of L. paeta were numerically greater than those of L. entomophila and L. decolor. Based on this, we investigated weight loss caused by L. paeta on the wheat variety where its population was numerically the highest, OK Bullet. Intact kernels of OK Bullet were ground as previously described. The ground wheat was then sieved using a U.S. Standard #14 sieve (1.41-mm openings) (Seedburo Equipment Company, Chicago, IL) to remove smaller particles and dust to obtain 24 g of damaged (cracked) kernels used for the experiment. Smaller particles and dust were removed to accurately determine the weight of wheat consumed by psocids. Small particles and dust stick to vials, petri dishes, and sieves during processing thereby reducing accuracy of weight measurements. A similar weight (24 g) of intact kernels of OK Bullet was also obtained as previously described. Twenty four vials with the top one-third inner portion of each vial coated with Fluon were used for this experiment. Two grams of damaged kernels were placed in each of 12 vials and a similar weight (2 g) of intact kernels was placed in each of the remaining 12 vials. Twenty four vials containing damaged and intact kernels were equilibrated in a plastic box ( cm high) containing saturated NaCl solution beneath the false ßoor to maintain 75 5% RH. The box was maintained at room temperature (22Ð23 C). The RH in the box was monitored weekly using a HOBO data logger. After 4 wk of wheat equilibration, the weight of damaged or intact kernels in each vial, referred to as initial weight, was determined. Each group of 12 vials containing either damaged or intact kernels was divided into two groups of six vials. Sixty adult female L. paeta were placed in each of six vials containing damaged kernels; however, psocids were not added to the remaining six vials that comprised the control treatment. Similarly, 60 adult female L. paeta were placed in each of six vials containing intact kernels whereas the remaining six vials had no psocids added to them. The 24 vials were kept in a plastic box ( cm high) that had saturated NaCl solution beneath the false ßoor to maintain 75 5% RH. The box was placed in an incubator maintained at 30 1 C. The temperature in the incubator and RH in the plastic box were monitored using HOBO data loggers. After 45 d, the contents of each vial were sieved using a U.S. Standard #14 sieve. All live L. paeta sieved out were collected in a 15-cm petri dish whose inner walls were coated with Fluon to prevent psocids from escaping. It was found at the end of the experiment that sieving was a faster method of separating live and dead L. paeta from wheat to allow the wheat to be weighed as quickly as possible after removal of the vials from the box. Collecting psocids in a 15-cm petri dish after sieving facilitates counting because the psocids are moving freely, and not hiding in or among wheat particles or kernels. After sieving, the wheat in each vial was weighed to determine the Þnal weight. Weight loss in each vial with psocids was determined by subtracting the Þnal weight of wheat in the vial from the initial weight. The changes in weight of the vials containing damaged and intact kernels that did not receive psocids (control vials) were used to adjust the weight in vials that received psocids to accurately determine weight loss caused by psocid feeding. The experiment consisted of three replications over time.

5 494 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1 Table 1. Populations of L. entomophila (mean SE) and percentages of wt loss after 90 d of infestation Type of diet Initial pop Final pop a Weight loss (%) b Damaged kernels a c b a a Intact kernels b c b c a In relation to Þnal psocid pop, ANOVA results for type of diet, initial psocid pop, and type of diet and initial psocid pop interaction were F 321.6, df 1,20, P 0.001; F 0.1, df 1,20, P 0.77; and F 0.5, df 1,20, P 0.49; respectively. b In relation to percentage wt loss, ANOVA results for type of diet, initial psocid pop, and type of diet and initial psocid pop interaction were F 391.7, df 1,20, P 0.001; F 9.5, df 1,20, P 0.06; and F 8.0, df 1,20, P c Means within a column followed by different letters are signiþcantly different. After weight measurements were conducted, intact wheat kernels that had been infested with psocids and those that had not been infested were used to evaluate the effects of L. paeta infestation on germination. The procedure of Kawamura et al. (1992) was used to determine the difference in germination between the two groups of intact kernels. The contents (intact kernels) of each of the 12 vials from each replication were placed in a 9-cm petri dish that was lined with a Þlter paper moistened with distilled water. The dishes were placed in a plastic box ( cm high) that was kept in an incubator maintained at 30 1 C. After 7 d, kernels in each dish were examined for germination and root and shoot growth. The latter two were deþned as the protrusion of the root or shoot to the extent of at least 0.5 mm. Altogether, three boxes containing 12 dishes each were used, that is, each treatment was replicated three times. For both the weight loss and germination parts of this experiment, there were three replications and the experimental design was a randomized complete block (RCBD) design with subsampling. Statistical procedures were accomplished using Statistical Analysis System software (SAS Institute 2010). PROC MIXED was used for ANOVA to determine the effects of type of diet (damaged or intact kernels) on numbers of psocids after 45 d and weight loss, and the effects of psocid infestation on kernel germination. Psocid numbers were transformed using the squareroot transformation, whereas percentages of weight loss and germination were transformed using the arcsine square-root transformation to stabilize variances before analysis. Untransformed means and SEs are reported to simplify interpretation. We used a LSD test to determine differences between means for numbers of psocids and percentages of weight loss and germination. Results Weight Loss Caused by L. entomophila Feeding. As expected, signiþcantly more psocids were found on a diet of damaged kernels than intact kernels (Table 1). The mean number of psocids found on the damaged kernels was and on the intact kernels Initial number of L. entomophila placed in vials had no signiþcant effect on the Þnal number of psocids found in vials after 90 d (Table 1). The pattern of percentage weight loss for damaged and intact kernels was not similar for initial populations of 30 and 60 psocids (Table 1). This signiþcant interaction was because of the fact that there was only little difference in percentage weight loss for intact kernels at the two initial populations of psocids used whereas the difference in weight loss for these two initial populations was much larger in damaged kernels (Table 1). The germ was observed as the favorite part of the kernel for psocids to feed on in both damaged and intact kernels (Fig. 1). Suitability of Wheat Varieties for Liposcelis Species. Across the six wheat varieties, the mean SE number of L. bostrychophila ( ) was higher than that of all other species after 30 d. On average, the population of L. bostrychophila increased 23-fold from an initial population of Þve psocids. Numerically, the population of L. paeta ( ) was the second highest; it was signiþcantly higher than the population of L. decolor ( ), but did not differ from that of L. entomophila ( ). Wheat variety had no signiþcant effect on psocid populations (Table 2). Effects of L. paeta Infestation on Kernel Weight and Germination. As expected, the number of L. paeta on damaged kernels was signiþcantly greater than on intact kernels (Table 3). Starting from an initial number of 60, the number of psocids on damaged kernels increased six-fold in 45 d. On intact kernels, the number of psocids declined (Table 3). Percentage weight loss was also greater on damaged kernels compared with intact kernels (Table 3). Percentage weight loss on damaged kernels was nine times greater than on intact kernels after 45 d of L. paeta infestation. Compared with uninfested intact kernels, L. paeta feeding signiþcantly reduced kernel germination in infested intact kernels (Table 3). Discussion Based on our data, L. entomophila is capable of causing weight losses of up to 8.5% by feeding on damaged wheat kernels over a 90-d period. Damaged kernels infested by L. paeta for 45 d had 3.3% weight loss. Other studies have shown psocid species of the genus Liposcelis to cause similar weight losses in stored grains. A study by Kučerová (2002) showed that L. bostrychophila causes weight losses of up to 9.7% in cracked wheat kernels over a 90-d period. McFarlane (1982) recorded 4Ð5% weight loss caused by L. bostrychophila in rice after 180 d of storage. A study by Pike (1994) reported 2.9% weight loss in lightly milled rice after 105 d of L. paeta infestation. According to Kučerová (1999), psocids appear to prefer feeding on the germ but will also feed on the soft endosperm of damaged kernels. We also observed that psocids hollow out damaged and intact kernels by preferentially feeding on the germ. Easy access to the germ and

6 February 2013 GAUTAM ET AL.: WEIGHT LOSS AND GERMINATION FAILURE CAUSED BY PSOCIDS 495 Fig. 1. Intact wheat kernels before infestation (A) and after infestation (BÐD). Circles and arrows indicate the location and head of the psocid, respectively. Notice the head of the psocid protruding out of the eaten-out germ area of the kernel with most of the seed coat still intact (B and C). (Online Þgure in color.) endosperm in damaged kernels is a logical reason for the signiþcantly larger numbers of psocids and weight losses found in damaged kernels compared with intact kernels. It is important to point out that most of the wheat in storage has damaged kernels as a result of harvesting and handling operations (Rees 2004). The abundance of damaged kernels in stored wheat, the presence large numbers of psocids in grain storages during warm and humid times of the year, and the fact that most wheat, whether for grain or seed, is stored one to Table 2. Numbers of psocids (mean SE) found on six varieties of hard red winter wheat and numbers of psocids of four species after 30 d of infestation Factor Factor levels No. of psocids Wheat variety Deliver a Endurance a Jagalene a Jagger a OK Bullet a Overley a Psocid species L. bostrychophila a L. paeta b L. entomophila bc L. decolor c ANOVA results for wheat variety, psocid species, and wheat variety and psocid species interaction were F 0.9, df 5,46, P 0.48; F 10.4, df 3,46, P 0.001; and F 0.7, df 15,46, P 0.81; respectively. Means for each factor followed by different letters are signiþcantly different. several months after harvest means the potential for psocids to cause weight losses of up to 8.5% is real. In comparison, Sitophilus oryzae (L.) (Coleoptera: Curculionidae) causes 30% weight loss of wheat kernels during development (White 1953), whereas Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) larval feeding causes weight losses that average 0.5% per day (Rao and Wilbur 1972). Psocid populations were signiþcantly much higher on damaged kernels than on intact kernels. We found L. entomophila populations to be 135 times greater on damaged kernels than on intact kernels. Athanassiou et al. (2010) also found that population growth of L. bostrychophila, L. decolor, and L. paeta was higher on damaged wheat kernels than intact kernels. However, Table 3. Numbers of psocids (mean SE), percentages of wt loss, and percentages of germination after 45 d of L. paeta infestation Treatment No. of psocids Weight loss (%) Germination (%) Damaged kernels a a Ñ Intact kernels b b Ñ Uninfested intact kernels Ñ Ñ a Infested intact kernels Ñ Ñ b ANOVA results for Þnal no. of psocids, percentage of wt loss, and percentage of germination were F 453.9, df 1,2, P 0.002; F 74.7, df 1,2, P 0.013; and F 64.1, df 1,2, P 0.015; respectively. Means within a column followed by different letters are signiþcantly different.

7 496 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1 data from that study showed that progeny production does not increase with increase in the percentage of damaged kernels but peaks at 10, 20, and 50% for L. decolor, L. bostrychophila, and L. paeta, respectively. From a pest management perspective, this means clean grain stored in clean storage structures probably would not develop heavy psocid infestation because of the limited availability of easily accessible food (damaged kernels). Across the psocid species L. bostrychophila, L. decolor, L. paeta, and L. entomophila, the wheat varieties Jagger, Endurance, Overley, Jagalene, OK Bullet, and Deliver had no signiþcant effect on psocid populations. This implies all six varieties are suitable for these four species of psocids and given optimal RH, temperature, and grain storage time to allow psocid reproduction, their numbers on all these varieties can increase exponentially to very high levels. Oklahoma is a high-risk state for grain storage because of the high ambient temperatures and long wheat storage period (Hagstrum and Heid 1988). The latter is a result of early summer wheat harvest. Therefore, weight losses caused by psocids would be expected to be signiþcant in stored wheat. Of the four psocid species investigated, L. bostrychophila populations were the highest across the six wheat varieties (Jagger, Endurance, Overley, Jagalene, OK Bullet, and Deliver) followed by L. paeta and L. entomophila. L. decolor populations were the lowest. This is intriguing because L. decolor and L. entomophila are usually the most abundant psocid species found infesting wheat in storage facilities in the United States based on the few studies conducted to date (Opit et al. 2009a,b). Perhaps other environmental conditions besides diet, such as, temperature and RH, take a more prominent role in determining the abundance of these species in grain storage facilities (Opit et al. 2010). In commercial wheat storage facilities sampled up to the present time in Kansas and Oklahoma, L. bostrychophila has rarely been found or has been found in only low numbers. Based on our data, there are no varietal differences in the suitability of wheat varieties tested for psocid population growth. This may be explained by the fact that all the varieties tested were from the same wheat class, hard red winter wheat. Athanassiou et al. (2010) found that progeny production of L. bostrychophila, L. decolor, and L. paeta is affected by wheat class. That study found that there was greater progeny production on durum than on hard red winter, hard red spring, soft white winter, soft white spring, soft club, soft red winter, and hard white wheat classes. Kučerová (1999) found varieties had a signiþcant effect on psocid population growth. That study showed some varieties of wheat to be unsuitable for L. bostrychophila population growth whereas other varieties were quite suitable. The fact that different wheat varieties and a different strain of L. bostrychophila were investigated over a 90-d period during the Kučerová (1999) study may explain the difference in results between that study and the current study. Psocids are capable of gaining access into the germ by breaching the seed coat and thereafter hollowing out the kernel by consuming the germ tissue and parts of the endosperm, but with most of the seed coat still in place. This cryptic feeding behavior of psocids means their current classiþcation as external-feeding or secondary stored-product pests is not entirely accurate. According to Pedersen (1992), there are cases of externally feeding stored-product pests penetrating under the pericarp in the area where the embryo is located thereby becoming internal-feeding pests. This clearly describes the feeding behavior of psocids. Therefore, it is appropriate to classify stored-product psocid pests with this type of feeding behavior as both external- and internal-feeding pests. Before the current study, there had been no formal assessment of physical losses caused by psocids in stored wheat in the United States. Most wheat producers in Oklahoma and United States as a whole store their wheat in round steel bins immediately after harvest, before moving it to better storage space or to market (Cuperus et al. 1990, Bailey 1992). Take, for example, small steel bins with capacities of 25Ð80 MT (1,000Ð3,000 bu). If an 80-MT steel bin with 13.5% moisture content wheat develops a heavy psocid infestation for 90 d and losses 8.5% of its weight, this will be equivalent to a loss of 6.8 MT ( 250 bu). The bushel is the standard unit for buying and selling grain in the United States. However, the number of bushels in wheat trade is determined by weighing wheat (1 bu 60 lb 27.2 kg). Given that the United States 12-mo average price for wheat in 2010 and 2011 was $6.31 per bushel (Hanavan 2011); this means the Þ- nancial penalty resulting from this psocid infestation is $1,578. This is not an insigniþcant loss given the small proþt margins in wheat production. Besides causing weight loss in both damaged and intact kernels, psocids also cause germination failure. Based on our data, 40% of psocid-infested intact wheat kernels did not germinate. When adjusted using the uninfested kernel germination percentage, 32% of the infested kernels failed to germinate as a result of psocid infestation. As previously mentioned, we observed that psocids make small holes in the seed coat to gain access to the germ, which is then completely consumed. No psocid feeding injury was observed at the end of the kernel opposite the germ. Watt (1965 and references therein) and Kučerová (1999) also report on the ability of psocids to cause a reduction in seed germination. This is particularly important in grain stored for seed because a germination failure rate of 40% could cause signiþcant economic loss. Other stored-product insect pests such as Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae), and R. dominica also preferentially feed on the germ and endosperm (Lustig et al. 1977, Demianyk and Sinha 1981) resulting in reduced seed viability. Clearly, psocids are capable of reducing seed germination levels under typical storage conditions, but the consequences of this injury are likely dependent upon guarantees associated with high quality seed, the type of wheat production system, and/or production costs. Relative to high quality seed, certiþed wheat

8 February 2013 GAUTAM ET AL.: WEIGHT LOSS AND GERMINATION FAILURE CAUSED BY PSOCIDS 497 seed suppliers guarantee high levels of germination (Edwards 2009a), and reductions caused by psocids could void contracts with growers. In forage only and forage plus grain wheat systems that are common in the Southern Plains of the United States, low seed germination levels can result in reduced forage production and subsequently lower beef gains (Redmon et al. 1995, Edwards 2008). Producers that grow wheat as forage use high seeding rates to account for variations in germination (Hossain et al. 2004, Edwards 2009b), but the combination of reduced germination and extreme environmental conditions in the Southern Plains can result in forage levels low enough to severely reduce beef gain (Redmon et al. 1995, Edwards 2008). Southern Plains wheat producers focused on grain production also use high seeding rates to account for potential reductions in germination but yield loss is unlikely (Shroyer et al. 1997, Edwards 2009b). Indeed, at typical seeding rates ( 70 kg/ha), a 40% reduction in germination has little impact on grain yields because wheat is able to compensate (produces additional tillers) when plant density is low (Collins and Fowler 1992, Edwards 2009b). However, it is important to point out that this is not always the case because there are varieties that cannot compensate easily because their ability to produce more tillers is limited. Germination issues caused by psocids will be more important in the future as seed prices continue to rise (certiþed seed and future genetically modiþed cultivars). In response to higher seed costs, producers are likely reduce seeding rates to optimize net proþts ( 40 kg/ha), and thus, will be susceptible to losses associated with reduced germination caused by psocids. Our data conþrm that psocids are stored-product pests of signiþcant economic importance. Under optimal environmental conditions, psocids can cause weight losses of up to 8.5% and germination failure of 40% in stored wheat. This weight loss and germination failure can represent serious economic loss. Therefore, effective management strategies need to be developed and implemented for the control of psocids in stored wheat. Acknowledgments We thank Kandara Shakya for her technical support; we also thank James Throne, Richard Grantham, and Ali Zarrabi for reviewing an earlier draft of this manuscript. In addition, we would like to extend our appreciation to E. Mockford who conþrmed the identity of L. bostrychophila, L. decolor, L. entomophila, and L. paeta. 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