Phenology of Brown Marmorated Stink Bugs and Distribution near California Pear Orchards

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1 Phenology of Brown Mrmorted Stink Bugs nd Distriution ner Cliforni Per Orchrds Chuck Ingels 1, Luci Vrel 2, Rchel Elkins 3, nd Cort Hurley 1 1 UC Coopertive Extension, Scrmento County 2 UC Coopertive Extension, North Cost 3 UC Coopertive Extension, Lke & Mendocino Counties ABSTRACT In the midtown Scrmento BMSB infesttion re, 24 trps were plced nd checked weekly to evlute BMSB phenology. Hlf were stnding 4-ft. pyrmid trps nd hlf were experimentl doule cone trps (Trece) secured to tree of heven rnches. The first trps were plced Fe. 9, nd ecuse Fe. 216 ws unusully wrm, the first dults were found in trps only two dys lter nd every week therefter fr erlier thn in pst yers. The first eggs were found on April 12, erlier thn previous yers nd the erliest in the country. The first nymphs were trpped on My 9, 1 dys erlier thn 215 nd 25 dys erlier thn 214. A typicl pek of nymphs ws seen in trps in June, ut lte July het wve decimted the popultion for month nd the typicl lrge lte summer pek ws fr lower thn in In ll 3 yers, two genertions were found, which grees with the BMSB model. Trps with Rescue lures cught more BMSB thn those with other lures. Trps cught significntly more nymphs thn dults, nd more femles thn mles. Pyrmid trps cught more nymphs thn experimentl doule cone trps. In Mrch, 2 pyrmid trps were plced south of Scrmento to Wlnut Grove nd trps were lso plced in griculturl/urn interfce res in Lke nd Mendocino counties. From mid-june through mid-july, 3 mle dults nd 2 nymphs were found in plum tree ner vineyrd y Clrksurg, nd in lte Sept. nd Oct. 216, three mle dult BMSBs were found in trp in Freeport. No BMSB were found in Lke or Mendocino. INTRODUCTION The rown mrmorted stink ug (Hlyomorph hlys) (BMSB) originted in Est Asi nd ws first identified in the US in Pennsylvni in 21; it hs now spred to 43 sttes ( A lrge popultion ws found in midtown Scrmento in Sept. 213, nd susequent surveys show tht dozens of individuls hve een found in other res of Scrmento County, with t lest eight res of reproducing popultions ( In 21, BMSB cused $37 million in dmge to fruit crops. BMSB hs host rnge of over 17 species, including fruits nd vegetles. Both dult nd nymphl stges cn dmge fruits. Physicl dmge to fruits includes pitting nd deformtion, with pithiness under the stings. This mkes the fruit unmrketle s fresh or cnned product. BMSB usully produce one genertion per yer in cool climtes nd two per yer in

2 wrmer climtes (Lee et l., 213; Nielsen nd Hmilton, 29). Severl trp designs hve een developed, including free-stnding nd trps nd those tht re plced in trees. The AgBio, Inc. (Ded-Inn ) trp consists of n inverted cler plstic continer with n entry cone opening tht is ttched with ungee cord to tll corrugted plstic stnds tht re connected to form pyrmid shpe. The Grower trp type stnds 4 ft. tll. Reserch hs shown tht free-stnding trps on lrger pyrmid stnds ctch more BMSB thn those on smller stnds, nd plcement on the ground is more effective thn in tree cnopy (Leskey et l., 212). However, plcement in on the ground my interfere with orchrd opertions. USDA-ARS reserchers hve lso found the gretest trp cpture using two scents together BMSB ggregtion pheromone scent nd one contining the synergist methyl dectrienote (MDT). These scents cn e seprte lures or comined into single lure. In ddition, incresing mounts of MDT hve een shown to ctch greter numers of BMSB (Leskey et l., 212). An insecticide-lced strip, such s Vportpe II (Hercon), is usully included to kill trpped ugs nd prevent escpe. Trps hve een shown to ctch oth dults nd nymphs, ut will ttrct them from less thn out 1 ft. Field studies showed tht 3rd nd 5th instrs wlked 5-2 meters cross grss field to trps (Leskey, 213). In ddition to the BMSB cught inside trps, lrge numers cn often e found lingering outside of trps in summer. There re numer of ntive nturl enemies of BMSB, oth predtors nd prsitoids, ut they hve hd limited impct on BMSB popultions in other sttes. Prsitoids of BMSB (most notly Trissolcus jponicus) hve een imported nd re now under qurntine in Cliforni nd re undergoing testing t UC Riverside. In 214, wild T. jponicus were found in sentinel egg mss plced in forest in Mrylnd. In 215 nd 216, mny more were found in other res in the mid-atlntic, nd they were found in n egg mss in Vncouver, WA. OBJECTIVES Scrmento County: 1. Determine sesonl phenology of BMSB 2. Compre new Trece lures nd doule cone trp strtegies 3. Monitor trps in per orchrds nd in hevily trveled res ner orchrds. 4. Study effects of nturl enemies on BMSB eggs nd determine sesonl progression of plnt host use Lke & Mendocino Counties: 1. Monitor susceptile host species ner per orchrds nd in urn res. 2. Monitor trps in per orchrds nd in hevily trveled res ner orchrds.

3 PROCEDURES Scrmento County 1. Determine sesonl phenology of BMSB nd compre trp types BMSB popultions were monitored weekly from erly Fe. through lte Oct A totl of 24 trps were plced in lndscpe strips of residences nd usinesses in nd ner the centrl core re of the initil 213 midtown Scrmento infesttion. Of these, 12 were 4-ft.-tll, pyrmid trps (AgBio, Inc.) nd 12 were experimentl Trece doule cone trps plced in the cnopies of tree of heven trees (plstic, 8 in. tll) (Fig. 1). All trps were spced t lest 5 ft. prt. For ech trp type, four trps in ech of three sets were rotted weekly. Ech of the four trps in ech rottion ws ited with one of four lures: Trece, Rescue, AgBio, nd Alph Scents, long with Hercon Vportpe II insecticide strip, ll of which were replced monthly. Adults nd nymphs trpped were counted nd the sex of dults in ech trp ws determined. 2. Compre new Trece lures nd doule cone trp strtegies. Two experimentl BMSB lures y Trece were compred to the stndrd Trece lure. Four Trece experimentl trps (see ove) for ech of the lure types were plced in Chinese pistche trees t lest 5 ft. prt nd rotted weekly from July 25 through Oct. 24. Ech trp hd n insecticide strip to prevent exiting. An dditionl tril ws conducted during the sme time period, using three experimentl Trece trps nd three replictes, ech trp contining Trece lure: 1) n improved version of the trp discussed ove (Fig. 2) with no insecticide strip, 2) the sme trp with n insecticide strip, nd 3) the trp with stickem on the inside nd no insecticide strip. In ech replicte, the three trps were rotted weekly. 3. Determine the spred from the initil infesttion re In Mrch, 2 pyrmid trps with Rescue lures nd n insecticide strip (oth replced monthly) in ech were plced from Freeport Blvd. ner Medowview Rd. south to the Wlnut Grove re. Trps were plced t severl types of loctions, chosen ecuse of their higher risk from people trvelling from midtown/downtown Scrmento. These included frms tht host visitors, per orchrds ner which resident commutes to Scrmento, pcking sheds nd trucking compnies, nd in the Freeport re. Trps were checked every two weeks through Octoer. Folige of nery susceptile hosts ws checked for BMSB with visul serches nd et sheet smples. This monitoring ws in ddition to following the spred within Scrmento nd nery communities sed on reports of BMSB sightings nd verifiction tht the stink ugs were ctully BMSB; the findings in Scrmento hve grown ech yer (Fig. 3). 4. Study effects of nturl enemies on BMSB eggs nd determine sesonl progression

4 of plnt host use (Kent Dne, unfunded) Sentinel egg msses were to e used to determine if incresed numers of egg msses ffect prsitism or predtion compred to single egg mss. Also, feeding vs. reproduction were to e used in cging studies to determine if specific plnt host species sustin BMSB for full genertion or for only prt of genertion. However, chllenges rose in reeding colonies tht resulted in only smll numer of vile egg msses, so this ojective could not e ccomplished. Lke nd Mendocino Counties BMSB were surveyed monthly from mid-mrch through mid-octoer y conducting et try smples erly in the seson nd visul surveys fter fruits or pods developed. Host trees were smpled in urn res in proximity to per orchrds, in riprin corridors, nd ner per orchrds. Five loctions in ech county were selected nd t ech loction the per orchrd nd djcent vegettion were surveyed. Monitoring with pyrmid trps continued in 216. The selected trp loctions re per orchrds per orchrds next to urn res or close to high trffic trnsporttion corridors. Three loctions ech per county were monitored with three trps t ech loction, spced t lest 1 ft. prt from Mrch to Octoer. RESULTS Scrmento County 1. Determine sesonl phenology of BMSB nd compre trp types Well over 5, BMSB were trpped in the 24 trps. Overll, more thn twice s mny nymphs were found thn dults, pyrmid trps cught significntly more BMSB thn doule cone trps, nd significntly more femles were cught thn mles (Fig. 4). Totl sesonl dult trp counts in pyrmid vs. doule cone trps were virtully identicl, wheres pyrmid trps cught significntly more nymphs (Fig. 5). Line grphs for sesonl BMSB trp counts for 214 through 216 re shown in Figs. 6-8, respectively. The 214 grph uses dt from four of the 1 trps tht cught sustntil numer of BMSB, the 215 grph includes eight of the 2 trps tht cught more thn 1 BMSB through the seson, nd the 216 grph uses dt from hlf of the 24 trps the six tht cught the most BMSB of ech of the two trp types. A summry of the BMSB phenology is shown elow: Trps plced 12-Mr. 24-Fe. 9-Fe. First dults (found t first check) 17-Mr. 2-Mr. 11-Fe. First eggs 5-My 17-Apr. 12-Apr. First nymphs 3-Jun. 19-My 9-My

5 In 216, unusully wrm tempertures occurred in Fe., including 1 dys in the upper 6s F nd eight dys t or ove 7 F (Fig. 9); this wrmth rought out overwintering dults very erly. The first eggs nd nymphs were found erlier in 215 thn in 214, nd lso erlier in 216 thn in 215; the 216 dtes re y fr the erliest in the country. As in previous yers, nymph peks were found in June nd erly Septemer. A het wve occurred in lte July 216, with seven dys t or ove 1 F, including two 14 F dys (Fig. 9). Likely due to this het wve, trp counts crshed from lte July through lte Aug. nd the Sept. trp counts were less thn in the two previous yers. In mid-my we noticed lrge numers of (mostly) nymphs outside of trps, so eginning My 23, we counted their numers within 3 ft. rdius of ech trp. Outside the doule cone trps there were nerly 4% of the numer inside the trps, wheres outside the pyrmid trps there were only less thn 2% of the numer inside (Fig. 1). The four lures in ech rottion were compred for sesonl trp ctches. When ll doule cone nd pyrmid trps were comined, trps ited with Rescue lures cught significntly more BMSB through the seson thn those ited with other lures (Fig. 11). The sme ws true with pyrmid trps, wheres in doule cone trps, Trece lures were not significntly different thn Rescue lures (p=.6). 2. Compre new Trece lures nd doule cone trp strtegies. Trps in this study were plced in Chinese pistche trees ecuse tree of heven trees were eing used for the min study discussed ove. Trp counts were likely very low, proly for two resons: 1) the BMSB popultion crshed fter the lte July het wve, nd 2) ecuse BMSB likely don t feed on Chinese pistche fruits until they soften in lte summer. On verge, the two experimentl Trece lures cught virtully the sme numer of BMSB compred to the stndrd Trece lure (Fig. 12). In the trp comprison, those with insecticide strips or dhesive inner wlls cught sustntilly more BMSB thn trps with neither the strip nor dhesive. It is likely tht BMSB could simply wlk ck out through the holes without wy to keep them inside. However, differences mong trps were not significnt due to low trp counts nd high vriility. Severl trps mlfunctioned s result of sun exposure reking down the plstic or wind cusing rnch movement nd rekge. 3. Determine the spred from the initil infesttion re In 216, new infesttion ws discovered in trp plced in flowering plum tree ner vineyrd ner Clrksurg (Fig. 13). A totl of 3 mle dults nd 2 nymphs were found in the trp etween mid-june nd mid-july. None were found in dditionl trps deployed t the site, nd serches of plum nd vineyrd folige turned up no dditionl BMSB. The plum tree ws not spryed. Plum is not on the host list. Monitoring t the site will continue in ernest t the site in 217.

6 Also, in lte Sept. nd erly Oct. 216, totl of 3 mle BMSB were found in trp t the Brtley Cvnugh Golf Course in Freeport (Fig. 13).One mle BMSB ws found t in trp t the site in Oct BMSB popultions often tke up to 5 yers to ecome serious prolem fter the first introduction (Trcy Leskey, personl communiction). A popultion is strting to uild in Freeport nd over the yers the popultion will slowly increse nd egin to spred. Lke nd Mendocino Counties No BMSBs were detected in either the pyrmid trps or during the host plnt surveys in Lke or Mendocino Counties. DISCUSSION Although the midtown Scrmento trp counts hd egun to decline just efore the July het wve egn, it is likely tht extended het set ck the popultion from lte July through lte Aug., s well s the reduced numers in erly Septemer. In order to determine the lethl high temperture extremes of BMSB, Aigner nd Kuhr (216) exposed dults to vrying high tempertures in petri dish contining wter wick. Fifteen minutes of exposure to 122 F killed ll ugs, s did 1 hour exposure to 113 F. Adults exposed to 95, 1, 14, 18, nd 113 F for 4 hours killed 5, 12, 38, 91, nd 1% of the dults, respectively. Mortlity t 18 F nd 113 F ws significntly higher thn it ws t the lower tempertures, nd mortlity t 14 F ws higher thn it ws t either 1 or 95 F. In Scrmento, the temperture on July 24 nd 26 ws 14 F for pprox. 1 hour nd 13 F for pprox. 2 hours. Therefore, it is possile tht perhps 1-25% of dults were killed on ech of those dys, plus more on the other five 1 F+ dys during the hot period. More importntly, nymphs nd eggs re likely fr more het sensitive, nd the het wve hit when the second genertion eggs were eing lid. The greter trp ctches with pyrmid trps grees with previous reserch showing tht lrge pyrmid trps re most effective (Leskey et l., 213). In 215, pyrmid trps cught 14% more BMSB thn 1-gl. doule cone trps plced in rndom trees. In 216, pyrmid trps cught n verge of 34% more thn the doule cone trps (which were smller thn those used on 215), even though the ltter trps were plced in tree of heven, which re highly ttrctive to BMSB. A key fctor in this discrepncy is tht pyrmid trps were significntly more effective in trpping nymphs thn doule cone trps. BMSB nymphs hve een shown to wlk firly long distnces. Most nymph stges hve een shown to wlk on flt ground out 1 ft. in 1 hr. to ited trps, ut third instr nymphs wlked 13 ft. Three yers of monitoring hve confirmed tht two BMSB genertions per yer occur in Scrmento. It lso shows tht dults will ecome ctive in winter when dys re wrm, s tempertures in the upper 6s to mid-7s occurred on 18 dys in Fe A similr ut less extreme phenomenon occurred in 215. Wrmer thn norml tempertures in 216 lso led to the erly discovery of the first egg mss on April 12.

7 However, the timings of the two genertionl peks of 216 were similr to those of 214 nd 215. The proportion of nymphs to dults in three yers hs een 3:1 in 214, 4:1 in 215, nd 2.5:1 in 216. Also, slightly more mles were cught thn femles in 214 nd 215, ut in 216, significntly more femles were trpped. Rescue lures cught fr more BMSB thn the three other lures in the pyrmid trps, ut the differences were fr less in the doule cone trps. The resons for the incresed ttrctiveness of the Rescue lures is unknown, ut it is known tht the higher the lod rte in lures the higher the trp ctches. The greter proportion of nymphs found outside doule cone trps is likely due to greter mount of folige round them compred to the free-stnding pyrmid trps. The finding in 215 of one mle BMSB in trp in Freeport nd three in 216 my indicte tht the BMSB popultion there is slowly estlishing on the northern edge of Delt frmlnd. Also, the finding of three mles nd two nymphs in trp in the flowering plum tree ner Clrksurg indictes potentil popultion lredy estlished. However, four dditionl trps cught none, nd no BMSB were found in the trp fter the lte July het wve. The finding of three mles in the trp in June nd two nymphs in July indictes tht popultion my e estlishing, ut finding none fter mid-july could indicte tht the BMSB did not survive. Not finding BMSB in other griculturl res nd nywhere in the North Cost does not necessrily men tht no BMSB re present in those res. Lure scents re known to ttrct BMSB from only short distnces less thn 1 ft. wy (Leskey et l., 213). Also, it tkes 4-5 yers for BMSB popultions to uild up to mjor pest levels fter the first introduction (T. Leskey, personl communiction). It is possile tht the pest could e present nd popultions eginning to increse somewhere in griculturl res ut not yet detected. LITERATURE CITED Aigner, J.D. nd T.P. Kuhr Lethl high temperture extremes of the rown mrmorted stink ug (Hemipter: Penttomide) nd efficcy of commercil het tretments for control in export shipping crgo. J. Agric. Urn Entomol. 32: 1 6. Lee, D-H., B.D. Short, S.V. Joseph J.C. Bergh, nd T.C. Leskey Review of the iology, ecology, nd mngement of Hlyomorph hlys in Chin, Jpn, nd the Repulic of Kore. Environ. Entomol. 42(4): Leskey, T.C Presenttion t Cumerlnd-Shenndoh Fruit Workers Conf., Dec Leskey, T.C., S.E. Wright, B.D. Short, et. l Development of ehviorlly sed monitoring tools for the rown mrmorted stink ug in commercil tree fruit orchrds. J. Entomol. Sci. 47(1): Nielsen, A. 28. Developmentl rte estimtion nd life tle nlysis for Hlyomorph hlys. Environ. Entomol. 37(2):

8 Figure 1. AgBio pyrmid trp (left) nd 8-inch tll doule cone trp in tree (right), with red insecticide strip nd Trece lure. Twelve of ech trp type were used in the min study. Figure 2. Improved version of the experimentl Trece doule cone trp, with plstic ring fitted to top nd ottom to secure the cone screen on top nd ottom insted of ruer nd nd stples. This trp hs dhesive on the inside to keep BMSB in the trp.

9 Jn. 214 Jn. 215 Jn. 216 Dec. 216 Figure 3. Loctions where BMSB hve een found in the Scrmento region, Jn. 1, 214 (left), Jn. 1, 215 (middle), Jn. 1, 216 nd Dec. 1, 216. Smll dots indicte single finds nd circles indicte reproducing popultions. Approx. 15 new finds were discovered etween Jn. 1 nd Dec. 1, 216.

10 Totl No. of BMSB Totl No. of BMSB ** * ** Adults Nymphs Doule Cone Pyrmid Mle Femle Figure 4. Totl numer of BMSB dults vs. nymphs cught in 24 trps (9-My to 1- Oct.), totl numer of BMSB cught in 12 doule cone vs. 12 pyrmid trps (9-My to 1-Oct.), nd totl numer of dult mle vs. femles cught in 24 trps (18-Apr to 31- Oct.). (* nd ** = significntly different t P.5 nd P.1, respectively, Duncn s MRT.) 25 * 2 15 NS 1 5 Doule Cone Pyrmid Doule Cone Pyrmid Adults Nymphs Figure 5. Totl numer of BMSB dults vs. nymphs cught in 12 doule cone vs. 12 pyrmid trps, 9-My to 1-Oct. (* = significntly different t P.1; NS = not significnt, Duncn s MRT.)

11 2-Mr 16-Mr 3-Mr 13-Apr 27-Apr 11-My 25-My 8-Jun 22-Jun 6-Jul 2-Jul 3-Aug 17-Aug 31-Aug 14-Sep 28-Sep 12-Oct 26-Oct No./Trp/Dy 17-Mr 31-Mr 14-Apr 28-Apr 12-My 26-My 9-Jun 23-Jun 7-Jul 21-Jul 4-Aug 18-Aug 1-Sep 15-Sep 29-Sep No./trp/dy BMSB/Trp/Dy, 214 Averge of 4 trps Adults First eggs: My 5 First nymphs: June 3 1st predicted 2nd gen. eggs: July 11 Nymphs 2 Figure 6. Averge numer of dults nd nymphs per trp per dy found in the 4 Midtown trps tht cught sustntil numers in 214. BMSB/Trp/Dy, 215 Averge of 8 trps with 1+ BMSB Adults First eggs: April 17 First nymphs: My 19 1st predicted 2nd gen. eggs: July 5 Nymphs 2 Figure 7. Averge numer of dults nd nymphs per trp per dy found in the 8 Midtown trps tht cught >1 in 215.

12 1-Fe 15-Fe 29-Fe 14-Mr 28-Mr 11-Apr 25-Apr 9-My 23-My 6-Jun 2-Jun 4-Jul 18-Jul 1-Aug 15-Aug Temperture ( F) 11-Fe 25-Fe 1-Mr 24-Mr 7-Apr 21-Apr 5-My 19-My 2-Jun 16-Jun 3-Jun 14-Jul 28-Jul 11-Aug 25-Aug 8-Sep 22-Sep 6-Oct 2-Oct No./Trp/Dy BMSB/trp/dy, 216 Avg. of 6 pyrmid & 6 doule cone trps with highest counts Four initil trps First eggs: April 12 First nymphs: My 9 1st predicted 2nd gen. eggs: July 3 Extended hot spell Nymphs Adults 2 Figure 8. Averge numer of dults nd nymphs per trp per dy found in the 12 (6 pyrmid nd 6 doule cone) trps tht cught the most BMSB in Midtown in Figure 9. High tempertures t Scrmento Executive Airport, 216. Ferury ws unusully wrm, ringing out dults erly, nd n extended period of extreme het occurred June 23-29, reducing the popultion to ner zero for four weeks.

13 No of BMSB/trp/seson Totl No. of BMSB Inside Outside Inside Outside Figure 1. Totl numer of BMSB nymphs cught inside nd counted outside (within 2 ft.) of doule cone nd pyrmid trps, My 23 to June NS *** *** AgBio Alph Sc. Rescue Trece 1 Doule Cone Pyrmid Comined Figure 11. Sesonl trp counts in rotted trps with four different lures. (*** = significntly different t P.1; NS = not significnt [P=.6], Duncn s MRT.)

14 Std Lure TRE 1295 TRE 1438 Control Ins. Strip Adhesive Avg. No. of BMSB/Trp Lure Study Trp Study Figure 12. Averge trp counts per week in the Trece lure nd trp study. The three lure types cught very similr numers of BMSB (left three rs). Clrksurg re (1 trp ner vineyrd): 6/13/216: 2 mles 6/2/216: 1 mle 7/6/216: 1 nymph 7/11/216: 1 nymph Freeport: 1/23/215: 1 mle 9/2/216: 2 mles 1/4/216: 1 mle Clrksurg Courtlnd Wlnut Grove Figure 13. Loctions of the BMSB trps plced from South Scrmento to Wlnut Grove nd numer nd loctions of BMSB found, 216. Funding for this project ws provided y the (Clif.) Per Pest Mngement Reserch Fund