STORED-PRODUCT Evaluation of Five Sampling Methods for the Psocids entomophila and L. decolor (: ) in Steel Bins Containing Wheat

1 G. P. OPIT, J. E. THRONE, AND P. W. FLINN

USDAÐARS, Grain Marketing and Production Research Center, 1515 College Ave., Manhattan, KS 66502Ð2736

J. Econ. Entomol. 102(3): 1377Ð1382 (2009) ABSTRACT An evaluation of Þve sampling methods for studying psocid population levels was conducted in two steel bins containing 32.6 tonnes of wheat in Manhattan, KS. Psocids were sampled using a 1.2-m open-ended trier, corrugated cardboard refuges placed on the underside of the bin hatch or the surface of the grain, and manual or automated electronic counts from Insector probe traps. Only two species were identiÞed in this study: (Enderlein) in 2005 and L. decolor (Pearman) in 2006. In both years, psocid numbers started to increase in early September, peaked earliest in surface refuges, and peaked at nearly the same time in grain samples and manual and electronic Insector counts. No psocids were found in hatch refuges in December to February, although psocids were detected by the other sampling methods during this time. Numbers of psocids in the grain samples could be estimated from the numbers of psocids obtained using the cardboard refuges and Insector probe traps in both years. The results indicate that cardboard refuges or Insectors may provide an effective method for sampling psocids in bins of wheat.

KEY WORDS Insector probe traps, population dynamics, cardboard refuges, stored products

Psocids are pests in grain storages, grain processing Sampling is an important aspect of integrated pest facilities, product warehouses, railway boxcars, and management (IPM) that has not been well studied for shipsÕ holds (Broadhead 1954, Tada 1956, Sinha 1965, psocids in stored grain. Sinha (1988) used brass tor- Rees 2004). Heavy psocid infestations can lead to pedo probes to study the population ßuctuation and serious germ damage in stored grain (Watt 1965, spatial distribution patterns of psocids in oats and Kucˇerova´ 2002) and can cause health problems by wheat stored in 12- to 14-tonne wooden granaries transferring microorganisms and by contaminating and in barley and rapeseed stored in 34- to 52-tonne food materials with feces and cast skins (Obr 1978, steel bins for 2Ð6 yr in Canada. Roesli and Jones (1994) Sidik et al. 1986). Most psocid pests of stored products studied the use of spear sampling and probe, pitfall, are in the genus Liposcelis (Psocoptera: Liposcelidi- and bait bag traps for studying psocid populations in dae) (Lienhard and Smithers 2002). 8- to 10-m-diameter silos Þlled with barley, maize, oats, Before 1990, psocids were not considered serious and sorghum in Australia. Rees and Starick (2002) pests of stored products; however, in some countries used cardboard refuges to monitor psocid numbers in such as Australia, they have become the most fre- a study to assess the efÞcacy of a combination of quently encountered storage pest in some areas (Rees phosphine fumigation and fogged dichlorvos for the 2003). The rise of psocids to prominence can be at- control of (Pearman) in 1,600-tonne tributed to their varied response to management tac- open-topped, concrete vertical bins Þlled with wheat tics that have been developed for coleopteran pestsÑ or barley. Arbogast et al. (2000) used an electronic e.g., some psocid species are resistant to residual probe trap to study the temporospatial distribution of insecticides and the fumigant phosphine (Nayak et al. L. entomophila in 36 tonnes of oats stored in a 5.5-m- 1998, 2002a, b, 2003; Nayak 2006). In addition, markets diameter by 5.5-m-high galvanized steel bin in Florida. increasingly view psocids as contaminants (Kucˇerova´ Currently, information is lacking on the use of var- 2002, Nayak 2006). ious sampling devices for monitoring psocid popula- tions in wheat stored in steel bins, a common method Mention of trade names or commercial products in this article is for wheat storage in the United States. The objective solely for the purpose of providing speciÞc information and does not of this study was to evaluate Þve sampling methods to imply recommendation or endorsement by Oklahoma State Univer- assess efÞcacy for monitoring psocid population levels. sity or the U.S. Department of Agriculture. We wanted to determine whether numbers of psocids 1 Corresponding author: Department of Entomology and Plant Pa- thology, Oklahoma State University, 127 Noble Research Center, in wheat samples (absolute estimates of population Stillwater, OK 74078 (e-mail: [email protected]). density) could be predicted from numbers of psocids 1378 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 3

12 A - grain samples 9

6

3

0 Psocids/Kg of grain 800 B - refuges 600 Hatch 400 Surface 200 0 Psocids/refuge 12000 TM TM 9000 C - Insector counts

6000 Electronic Manual 3000

0 Psocids/Insector Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec 2005 2006 Fig. 1. Psocid densities in (A) grain samples, (B) surface and hatch refuges, and (C) manual and electronic Insector counts in 2005 and 2006. Error bars represent SEM. in corrugated cardboard refuges placed on the under- bin center and in the four cardinal directions (north, side of the bin hatch or the surface of the grain or from south, east, and west). In each cardinal direction, two manual or automated electronic counts from Insector samples each were taken at 0.15 and 0.76 m from the probe traps (OPI Systems, Calgary, Alberta, Canada) bin wall. Each sample was placed in a zip-lock bag and (relative estimates of population density). in the laboratory was divided into three parts, which were sieved separately, for more effective extraction of psocids without killing them. Grain samples were Materials and Methods sieved using a U.S Standard #10 sieve (2-mm open- Storage Situation. Two steel bins at the Grain Mar- ings) to remove psocids, which were identiÞed keting and Production Research Center in Manhattan, (Mockford 1993) and counted. KS, were Þlled in July 2005 with newly harvested hard One week before taking the grain samples, 20 cor- red winter wheat (Triticum aestivum L.) and were rugated cardboard refuges (8.9 by 12.7 by 0.4 cm sampled in 2005 and 2006. Both bins were outdoors in thick) were placed randomly on the surface of the an open area with no shading and no protection from grain in each bin, and three refuges were taped on the ambient air currents. Bin dimensions were 4.72-m di- underside of the hatch. These were removed just be- ameter by 3.35-m high at the eaves, and each bin was fore grain samples were taken. Refuges were placed in Þlled with 32.6 tonnes (1,200 bushels) of wheat to a individual plastic zip-lock bags. Psocids were removed depth of 2.4 m. from the refuges by knocking them out of the card- Sampling Methods. Biweekly sampling was con- board into a white enamel pan with Fluon (polytet- ducted using a 1.2-m open-ended trier, corrugated raßuoroethylene; Northern Products, Woonsocket, cardboard refuges placed on the underside of the bin RI) applied to its walls to prevent psocids from es- hatch or the surface of the grain, and manual or au- caping, and psocids were identiÞed and counted. tomated electronic counts from Insector probe traps. We also placed an Insector in the center of each We collected both manual and automated electronic sampling location (center, north, south, east, and counts from Insector probe traps because we were west). The Insector (originally known as the Elec- trying to determine whether electronic counts (a rel- tronic Grain Probe Counter [EGPIC]) is a atively new technology) are accurate for psocids. Also, modiÞed probe trap equipped with an infrared-beam we wanted to know the suitability of manual probe sensor head to count that passively fall into the trap counts for estimating numbers of psocids in grain trap, thereby minimizing bin entry (Epsky and Shu- samples because manual probe traps are currently man 2001). One week before taking the grain samples, being used in grain storages (e.g., WB Probe Trap II the Þve probes (per bin) were pushed into the grain traps; Tre´ce´, Adair, OK) to monitor insect pests. The with the top of the probe 0.3 m below the grain surface, trier was used to take 480-g samples in the top 0.9 m and the probes were removed just before grain sam- of wheat. Four trier samples each were taken from the ples were taken. Solid collection tips (attached to the June 2009 OPIT ET AL.: EVALUATION OF PSOCID SAMPLING METHODS 1379

10 A 10 B

8 8

6 6

4 4

2 Psocids/Kg of grain 2 2 2 y = 0.25 + 0.31x0.5 (r = 0.50) y = 0.60 + 0.34x0.5 (r = 0.51) 0 0 0 100 200 300 400 0100200300 Psocids/surface refuge Psocids/hatch refuge

C D 10 10

8 8

6 6

4 4

2 2 Psocids/Kg of grain 2 2 y = -0.01 + 0.11x0.5 (r = 0.68) y = -0.20 + 0.11x0.5 (r = 0.62) 0 0 0 1000 2000 3000 0 1000 2000 3000

TM TM Psocids/Insector (manual counts) Psocids/Insector (electronic counts) Fig. 2. Relationships between psocid densities in grain samples and densities in (A) surface refuges, (B) hatch refuges, (C) manual Insector counts, and (D) electronic Insector counts in 2005. For all regressions, P Ͻ 0.01; N ϭ 34, 32, 30, and 21, respectively.

Insector end furthest from the grain surface) Þlled 2005, numbers of psocids found using all the sampling with 1 cm of ethylene glycol (to preserve the insects) methods started to increase in early September but were used with the Insectors for 1 wk, after which the peaked at different times (Fig. 1). The order in which Insectors were pulled out of the grain. The insects in numbers peaked was surface refuges in late Septem- the tips were identiÞed and manually counted: i.e., we ber, followed by manual and electronic Insector obtained both electronic and manual psocid counts. counts in early to late October, grain samples in late In the 2005 sampling study, the steel bins were October, and hatch refuges in early November (Fig. sampled from August 2005 through March 2006. In the 1). No psocids were found in the hatch refuges during 2006 study, the wheat was fumigated using phosphine winter, although low numbers were found throughout in June 2006 and reused for sampling from July winter using the other sampling methods (Fig. 1). through November 2006. The sampling methods were Similarly, in 2006, psocid numbers found using all the same in both years. the sampling methods started to increase in early Sep- Statistical Analysis. Regression analysis was used to tember and peaked at different times (Fig. 1). The determine the relationship between psocid densities order in which numbers peaked was surface refuges in as determined by trier samples (best estimate of ab- early October, followed by grain samples in late Oc- solute population density) and each of the four rela- tober, and hatch refuges and manual and electronic tive sampling methods (i.e., cardboard refuges placed Insector counts in early November (Fig. 1). on the grain surface and on the underside of the hatch, The numbers of psocids found per sample were and manual and electronic Insector counts). Regres- highest in the Insectors, which caught more psocids sion analysis was performed using TableCurve 2D than the other methods (77,502 and 117,201 in 2005 (Systat Software 1996), which Þts a large number of and 2006, respectively). The numbers of psocids per families of curves to data. Residual analysis and the Þt sample were lowest in the grain samples where the of the predicted curve to the observed data were used fewest psocids were found (547 and 408 in 2005 and to select the best model to describe the data. 2006, respectively), and the numbers per refuge were intermediate (psocid numbers found were 33,615 and 7,687 in surface refuges and 3,395 and 4,926 in hatch Results refuges in 2005 and 2006, respectively). Only two psocid species were identiÞed in this Although the densities of psocids in the grain sam- study: L. entomophila in 2005 and L. decolor in 2006. In ples could be estimated from the densities of psocids 1380 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 3

10 10 A B 8 8

6 6

4 4

2 2 Psocids/Kg of grain y = 0.10 + 0.70x0.5 (r2 = 0.56) y = 0.52 + 0.33x0.5 (r2 = 0.69) 0 0 020406080 0 200 400 600 800 Psocids/surface refuge Psocids/hatch refuge

10 10 C D 8 8

6 6

4 4

2 2 Psocids/Kg of grain y = 0.17 + 0.10x0.5 (r2 = 0.88) y = 0.18 + 0.12x0.5 (r2 = 0.66) 0 0 0 2000 4000 6000 8000 0200040006000

TM TM Psocids/Insector (manual counts) Psocids/Insector (electronic counts) Fig. 3. Relationships between psocid densities in grain samples and densities in (A) surface refuges, (B) hatch refuges, (C) manual Insector counts, and (D) electronic Insector counts in 2006. For all regressions, P Ͻ 0.01; N ϭ 20, 20, 18, and 18, respectively. obtained using the cardboard refuges and Insector lower number of insects found in grain samples is that probe traps in both years (Figs. 2 and 3), the density cardboard refuges and Insector probe traps were left of psocids in grain samples was best estimated by the to collect insects for 1 wk, whereas grain samples only densities indicated by the electronic and manual In- recover insects present in a volume of grain at the time sector counts in 2005 and 2006. Cardboard refuge that it is taken (Subramanyam and Hagstrum 1996). densities also gave reasonable estimates of densities of In both 2005 and 2006, psocid numbers started to insects in grain samples. increase in early September, peaked earliest in surface Electronic Insector counts gave a good estimate of refuges, and peaked at nearly the same time in grain actual psocid counts in the probe traps (Fig. 4). In samples and manual and electronic Insector counts. A 2005, electronic counts overestimated actual counts of possible explanation for why psocid numbers peak psocids in the probe traps by a mean percentage error earlier in surface refuges could be that psocids move of 79.9 Ϯ 1.8% (SE) when actual psocid counts were to the surface of the grain because environmental at least 100 per Insector (Fig. 4A). In 2006, electronic conditions at the surface are more favorable than in- counts underestimated actual counts of psocids in the side the grain bulk. Psocid numbers peaked at nearly probe traps by 23.9 Ϯ 2.9% when actual psocid counts the same time in grain samples and manual and elec- were at least 600 per Insector (Fig. 4B). tronic Insector counts probably because we speciÞ- cally took trier samples that corresponded to the same area of the grain mass sampled by Insector probes. Discussion Therefore, numbers of psocids in manual and elec- Only two species of psocids were identiÞed in this tronic Insector counts would be expected to follow the study: L. entomophila in 2005 and L. decolor in 2006. same pattern as those in grain samples. No psocids Mashaya (1999, 2001) and Arbogast et al. (2000) also were found in hatch refuges in December to February, found just one psocid species, L. entomophila, in their most likely because temperatures at the hatch are studies, although Nayak and Daglish (2007) report similar to ambient temperatures, which are very cold that psocid infestations generally comprise more than during this period, whereas the grain is warmer than one Liposcelis sp. in Australia. ambient air during the same period. In both years, psocid numbers were lowest in the Cardboard refuges and Insector probe traps would grain samples. A possible reason for the relatively be suitable for sampling psocids in stored wheat be- June 2009 OPIT ET AL.: EVALUATION OF PSOCID SAMPLING METHODS 1381

in grain samples, but they require entering bins to A - 2005 install and recover the refuges. Both hatch and surface refuges require a moderate level of counting of psocids 2000 and have no equipment costs. Therefore, the hatch and surface refuges provide a low-cost alternative for sampling psocids. Electronic Insector counts matched manual counts 1000 well when numbers of psocids in the traps were low but not as well when numbers of psocids were high. r2 Arbogast et al. (2000) found similar results, which they y = 11.6 + 0.54x ( = 0.87) attributed to several factors, including small psocids 0 not eliciting an electronic count, insects falling in close (manual counts) 0 1000 2000 3000

TM proximity detected as a single count, and dockage particles generating erroneous counts. Despite this, B - 2006 electronic Insector densities provide good estimates of 6000 psocid densities in grain. Calibration of the Insector system can be changed to improve its ability to detect and record psocids in stored grain. 4000 Our results show that cardboard refuges or Insec-

Psocids/Insector tors provide an efÞcient method for sampling psocids in bins of wheat. Choice of a sampling method will 2000 depend on material investment, labor costs, and safety

2 concerns. y = 196.5 + 1.10x (r = 0.76)

0 0 1000 2000 3000 4000 5000 6000 Acknowledgments TM We thank B. Barnett, K. Friesen, A. Prakash, and A. Red- Psocids/Insector (electronic counts) mon for technical support and R. T. Arbogast, H. Melouk, E. Fig. 4. Relationships between manual and electronic In- Mockford, M. Nayak, and M. Reiskind for reviewing an ear- sector psocid counts in (A) 2005 and (B) 2006. For all re- lier version of this manuscript. In addition, we extend our gressions, P Ͻ 0.01. N ϭ 26 and 18, respectively. appreciation to E. Mockford, who conÞrmed the identity of L. entomophila and L. decolor, and the Oklahoma Agricultural Experiment Station for partial support. cause numbers of psocids in the grain samples could be estimated from the numbers of psocids obtained References Cited using cardboard refuges and Insector probe traps. Manual Insector densities gave good estimates of pso- Arbogast, R. T., P. E. Kendra, D. K. Weaver, and D. Shuman. cid densities in grain samples in both years. We expect 2000. Insect infestation of stored oats in Florida and Þeld that manual Insector densities would be similar to evaluation of a device for counting insects electronically. J. Econ. Entomol. 93: 1035Ð1044. densities that would be observed using standard probe Broadhead, E. 1954. Infestation of warehouses and shipsÕ traps for sampling, such as the WB Probe II Trap holds by psocids in Britain. Entomol. Mon. Mag. 90: 103Ð (Tre´ce´). This Þnding is similar to results reported by 105. Roesli and Jones (1994), who also found that the probe Epsky, N. D., and D. Shuman. 2001. Laboratory evaluation trap was the most reliable method for estimating the of an improved electronic grain probe insect counter. J. mean density of psocids in grain compared with the Stored Prod. Res. 37: 187Ð197. other sampling methods they assessed. Although man- Kucˇerova´, Z. 2002. Weight losses of wheat grains caused by psocid infestation (Liposcelis bostrychophila: Liposcelidi- ual Insector counts provided the best estimates of dae: Psocoptera numbers of psocids in grain samples, entering bins to ). Plant Protect. Sci. 38: 103Ð107. Lienhard, C., and C. N. Smithers. 2002. Psocoptera world service the probes and counting large numbers of catalogue and bibliography. Muse´um dÕHistoire Na- psocids is labor intensive, requires moderately expen- turelle, Geneva, Switzerland. sive equipment, and poses worker safety issues. Elec- Mashaya, N. 1999. Population dynamics of Liposcelis ento- tronic Insector counts also provide good estimates of mophila (Enderlein) (Psocoptera: Liposcelidae) in farm numbers of psocids in grain samples, and the process tobacco processing buildings. J. Stored Prod. Res. 35: is automated so no counting or bin entry is required, 355Ð368. but the equipment is relatively expensive. The Insec- Mashaya, N. 2001. Inßuence of ambient temperature and relative humidity on changes in numbers of a natural tor system provides the additional advantage of sam- Liposcelis entomophila pling beetles in the grain automatically, whereas the population of (Enderlein) (Pso- coptera: Liposcelididae). J. Stored Prod. Res. 37: 1Ð12. refuges sample only psocids. Hatch refuges also pro- Mockford, E. L. 1993. North American Psocoptera. Sandhill vide good estimates of numbers of psocids in grain Crane Press, Gainesville, FL. samples but require climbing up to the bin hatch Nayak, M. K. 2006. Psocid and mite pests of stored com- during warmer periods of the year. Similarly, surface modities: small but formidable enemies, pp. 1061Ð1073. In refuges provide good estimates of numbers of psocids I. Lorini, B. Bacaltchuk, H. Beckel, D. Deckers, E. Sund- 1382 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 3

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