BMSB Workgroup, Rutgers, NJ June 16th, Kim A. Hoelmer Christine Dieckhoff Kathy Tatman Ashley Colavecchio USDA/ARS, Newark, DE

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1 BMSB Workgroup, Rutgers, NJ June 16th, 2016 Kim A. Hoelmer Christine Dieckhoff Kathy Tatman Ashley Colavecchio USDA/ARS, Newark, DE

2 Status of adventive Trissolcus japonicus in the U.S Photo: E. Talamas ARS/SEL

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4 T. japonicus now found in: MD, D.C., VA, DE (east coast) and WA (west coast) Recoveries were made from BMSB (sentinel & wild), Podisus and Thyanta

5 Washington Oregon

6 Principal coordinate Principal analysis Coordinates (PCoA) of genetic diversity among 23 microsatellite markers in T. japonicus Coord. 2 West Coast U.S. adventive populations Chinese populations East Coast BARC2014 WINCHESTER US NATL VANCOUVER BIIR 2015 BARC2015 Pop7 Pop8 Pop9 Pop10 Pop11 Pop12 Pop13 Pop14 Pop15 Pop16 Pop17 Beijing Coord. 1

7 Wider regional surveys needed to monitor their spread Determine their impact on BMSB & non-targets in the field Continue work on a Petition to release Beijing T. japonicus APHIS requires a Petition for each state Field recovery/impact data may help to fast-track a Petition to Release in other regions (if it is still needed) or redistribute the adventive populations

8 Status of Biological Control In North America: Regional surveys (ongoing) to document the occurrence & impact of natural enemies: Overall low levels of parasitism Impact varies according to habitat Predation is often more important than parasitism Studies in conservation biological control to increase impact of native predators and parasitoids Border plantings, trap crops, insectary plants Will native natural enemies adapt to BMSB over time? Why are native parasitoids poorly adapted to BMSB? Can adaptation be enhanced via laboratory selection?

9 tsp180 tsp181 tsp179 tsp175 tsp174 Phylogenetic tree based on Maximum Likelihood, GTR+G+I model (CO1) tsp173 tsp172 tsp171 tsp169 tsp168 tsp166 tsp165 tsp164 tsp163 tsp157 TSP130 TSp125 TSp118 TSP115 TSp110 Tsp53 TSP98 TSp102 TSp106 Tsp50 Tsp49 Tsp48 Tsp45 Tsp44 tsp185 TSP77 TSP78 TSP79 TSP88 TSP90 T. japonicus Scelionidae from eggs of Asian Pentatomidae TSP91 TSP93 Tsp52 Tsp41 tsp154 tsp155 tsp167 tsp170 tsp TSP TSP141 TSP142 TSP143 TSP145 TSP146 TSP147 T. sp. 22 Tsp51 tsp186 Tsp42 TSP148 Tsp43 tsp161 tsp176 T. plautiae Tsp46 tsp162 Tsp54 TSP127 TSP128 TSp126 TSP96 TSP TSP87 TSP86 TSP84 TSP83 TSP82 TSP80 TSP81 T. cultratus TSP85 TSP89 TSP TSP131 TSP132 TSP133 TSP134 TSP135 TSP136 TSP137 Tsp58 TSP138 TSP139 TSP140 Tsp40 T. spp. 41 Tsp59 TSP94 T. edessae tsp TSP152 TSP153 TSP151 TSP150 TSP149 Tsp TSP95 T. mitsukurii 99 tsp184 tsp188 tsp156 tsp177 tsp190 tsp191 tsp183 Tsp55 Tsp57 tsp192 tsp tsp187 tsp193 tsp194 tsp159 tsp158 tsp160 T. spp. Telenomus spp. Gryon sp. M.-C. Bon ARS/EBCL E. Talamas ARS/SEL M. Buffington ARS/SEL C. Dieckhoff ARS/BIIR K. Hoelmer ARS/BIIR 0.1

10 Data from Tim Haye, CABI Bioscience

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12 Trissolcus japonicus is oligophagous - it attacks several (but not all) Asian pentatomid species Halyomorpha halys Glaucias subpunctatus Plautia crossota Dolycoris baccarum Erthesino fullo

13 Summary In Asia: T. japonicus is the dominant species throughout the season on different host plants Other species (e.g., Anastatus, Telenomus, tachinid flies) are of minor importance in controlling BMSB Ecological host range of T. japonicus contains other species in these habitats, e.g. Plautia and Dolycoris T. japonicus is an oligophagous species, thus nontarget attacks likely of some other stink bugs, riskbenefit analysis needed Ongoing studies: impact on non-target species, including the predatory species Arma chinensis

14 Introducing Asian Parasitoids: Status NAPPO Guidelines for Petitions for First Release of Arthropod Pest Biological Control Agents

15 No-Choice Test Outcome (1) Agonoscelis puberula (N=12) Amaurochrous sp. (N=8) Antheminia remota (N=6) Bagrada hilaris (N=7) Brochymena quadripustulata (N=17) Chlorochroa ligata (N=25) Coenus delius (N=12) Coleotichus blackburniae KOA (N=12) Cosmopepla intergressa (N=5) Edessa florida (N=28) Holcostethus abbreviatus (N=20) Murgantia histrionica (N=23) Oebalus pugnax (N=12) Perillus bioculatus (N=7) Podisus brevispinus (N=9) Stiretrus anchorago (N=6) Thyanta pallidovirens (N=16) Trichopepla semivittata (N=) 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% % live males live females unemerged parasitoids hatched nymphs unhatched nymphs

16 No-Choice Test Outcome (population variability) Banasa dimiata (MI, N=13) Banasa dimiata (OR, N=22) Chinavia hilaris (MI, N=17) Chinavia hilaris (OR, N=19) Chlorochroa uhleri (CA, N=8) Chlorochroa uhleri (OR, N=8) Cosmopepla lintneriana (DE, N=26) Cosmopepla lintneriana (OR, N=16) Euschistus servus (DE, N=20) Euschistus servus euschistoides (MI, N=13) Euschistus tristigmus (DE, N=26) Euschistus tristigmus luridus (MI, N=20) Euschistus variolarius (MI, N=17) Euschistus variolarius (DE, N=21) Holcostethus limbolarius (DE, N=20) Holcostethus limbolarius (MI, N=20) Podisus maculiventris (DE, N=34) Podisus maculiventris (MI, N=19) Thyanta custator (DE, N=23) Thyanta custator (OR, N=23) Thyanta custator accerra (DE, N=13) Thyanta custator accerra (MI, N=22) 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% % live males live females unemerged parasitoids hatched nymphs unhatched nymphs

17 Choice Test Outcome (as of 2015, Newark BIIR)

18 Caveat: Laboratory vs. Field Results Slide: Courtesy of P. Mason

19 BMSB P. maculiventris Naïve, 24h-old female T. japonicus exposed to egg masses - 1 hour - 4 hours - 6 hours - 24 hours Observation of parasitoid behavior for 1 hour

20 1 hour Parasitism of P. maculiventris only (N = 2) 13% Parasitism of BMSB only (N = 8) 54% No egg mass parasitized (N = 5) 33% Parasitism of both egg masses (N = 0) 0% Parasitism P. maculiventris only (N = 1) 7% Parasitism of BMSB only (N = 6) 40% 4 hours No egg mass parasitized (N = 8) 53% Parasitism of both egg masses (N = 0) 0% Parasitism of both egg masses (N = 0) 0% 6 hours 24 hours No egg Parasitism BMSB only (N = 7) 44% No egg mass parasitized (N = 9) 56% Parasitism P. maculiventris only (N = 0) 0% Parasitism P. maculiventris only (N = 0) 0% Parasitism of both egg masses (N = 4) 27% Parasitism of BMSB only (N = 10) 66% mass parasitized (N = 1) 7%

21 Summary Native parasitoids have low impact in landscape reservoirs but may be important in certain crops/situations (e.g., Anastatus, Telenomus) T. japonicus is established and spreading in the U.S. in arboreal landscape habitats (important as population reservoirs) Physiological host range of T. japonicus includes other stink bug species in the U.S. (in laboratory tests) Ongoing studies: ecological impact on non-target pentatomids, including Podisus maculiventris Impact of both native & introduced natural enemies should increase over time

22 Photo: E. Talamas ARS/SEL

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24 Sentinel Egg Masses Fate of BMSB eggs in DE surveys 2007 to 2015 Sentinels vs. naturally laid (wild) % 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Naturally Naturally Laid Egg laid Masses Missing Sucking damage Chewing damage Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

25 Sentinel Egg Masses Fate of BMSB eggs in DE surveys 2007 to 2015 Missing or apparent predation % 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Naturally Naturally Laid Egg laid Masses Missing Sucking damage Chewing damage Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

26 Sentinel Egg Masses Fate of BMSB eggs in DE surveys 2007 to 2015 BMSB nymphs (hatched & unhatched) % 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Naturally Naturally Laid Egg laid Masses Missing Sucking damage Chewing damage Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

27 Sentinel Egg Masses Fate of BMSB eggs in DE surveys 2007 to 2015 Parasitism (emerged & unemerged) % 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Naturally Naturally Laid Egg laid Masses Missing Sucking damage Chewing damage Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

28 Compare with parasitism rates on native US pentatomids:

29 Note differences in Y-axis scale Sentinel BMSB eggs (light grey) & naturally laid BMSB eggs (dark grey): % eggs parasitized in each egg mass (± SE) Other 80 Naturally laid eggs of other species (blue): % parasitized per egg mass (± SE) Percentage parasitized eggs (mean±se)

30 Time until Detection of Egg mass (in sec; mean ± SE) Reject No N = 6 N = 27 Accept Time spent antennating/visit (in sec/t spent on EM; mean ± SE) N = 6 Reject Oviposition (mean ± SE): ± 11.5 s Marking (mean ± SE): ± 2.32 s Yes N = 27 Accept F 1,29 = , P = F 1,28 = 5.87, P =