Kim A. Hoelmer Christine Dieckhoff

Kathy Tatman Ashley Colavecchio

USDA/ARS, Newark, DE

BMSB Workgroup, Rutgers, NJ – June 16th, 2016

Status of adventive Trissolcus japonicus in the U.S. - 2015

Photo: E. Talamas ARS/SEL

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

Washington

Oregon

Coo

rd. 2

Coord. 1

Principal Coordinates (PCoA)

BARC2014

WINCHESTER

US NATL

VANCOUVER

BIIR 2015

BARC2015

Pop7

Pop8

Pop9

Pop10

Pop11

Pop12

Pop13

Pop14

Pop15

Pop16

Pop17

U.S. adventive populations

Principal coordinate analysis (PCoA) of genetic diversity among 23 microsatellite markers in T. japonicus

Chinese populations

Beijing

East Coast

West Coast

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

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?

Status of Biological Control In North America:

tsp180

tsp181

tsp179

tsp175

tsp174

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

TSP91

TSP93

Tsp52

Tsp41

tsp154

tsp155

tsp167

tsp170

tsp182

TSP144

TSP141

TSP142

TSP143

TSP145

TSP146

TSP147

TSP148

Tsp51

tsp186

Tsp43

tsp161

tsp176

Tsp42

Tsp46

tsp162

Tsp54

TSP127

TSP128

TSp126

TSP96

TSP92

TSP87

TSP86

TSP84

TSP83

TSP82

TSP80

TSP81

TSP85

TSP89

TSP129

TSP131

TSP132

TSP133

TSP134

TSP135

TSP136

TSP137

TSP138

TSP139

TSP140

Tsp40

Tsp58

Tsp59

TSP94

TSP95

TSP152

TSP153

TSP151

TSP150

TSP149

Tsp39

tsp189

tsp184

tsp188

tsp156

tsp177

tsp178

tsp187

tsp190

tsp191

tsp183

Tsp55

Tsp57

tsp192

tsp193

tsp194

tsp159

tsp158

tsp160 100

73

99

100

100

100

100

100

100

100

100

100

100

100

61

61

100

83

62

99

77

100

76

26

41

5

1

22

58

85

100

100

100

99

100

59

69

0.1

Phylogenetic tree based on

Maximum Likelihood, GTR+G+I model

(CO1) T. japonicus

T. sp.

Gryon sp.

T. mitsukurii

T. cultratus

T. plautiae

T. edessae T. spp.

T. spp.

Telenomus spp.

Scelionidae from eggs of Asian

Pentatomidae

M.-C. Bon – ARS/EBCL E. Talamas – ARS/SEL

M. Buffington – ARS/SEL C. Dieckhoff – ARS/BIIR K. Hoelmer – ARS/BIIR

Data from Tim Haye, CABI Bioscience

Trissolcus japonicus is oligophagous - it attacks several (but not all) Asian pentatomid species

Dolycoris baccarum Plautia crossota

Glaucias subpunctatus

Erthesino fullo

Halyomorpha halys

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 non-target attacks likely of some other stink bugs, risk-benefit analysis needed

Ongoing studies: impact on non-target species, including the predatory species Arma chinensis

Summary – In Asia:

NAPPO Guidelines for Petitions for First Release of Arthropod Pest Biological Control Agents

Introducing Asian Parasitoids: Status

0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Trichopepla semivittata (N=)Thyanta pallidovirens (N=16)

Stiretrus anchorago (N=6)Podisus brevispinus (N=9)

Perillus bioculatus (N=7)Oebalus pugnax (N=12)

Murgantia histrionica (N=23)Holcostethus abbreviatus (N=20)

Edessa florida (N=28)Cosmopepla intergressa (N=5)

Coleotichus blackburniae KOA (N=12)Coenus delius (N=12)

Chlorochroa ligata (N=25)Brochymena quadripustulata (N=17)

Bagrada hilaris (N=7)Antheminia remota (N=6)

Amaurochrous sp. (N=8)Agonoscelis puberula (N=12)

live males live females unemerged parasitoids hatched nymphs unhatched nymphs

No-Choice Test Outcome (1)

0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Thyanta custator accerra (MI, N=22)Thyanta custator accerra (DE, N=13)

Thyanta custator (OR, N=23)Thyanta custator (DE, N=23)

Podisus maculiventris (MI, N=19)Podisus maculiventris (DE, N=34)

Holcostethus limbolarius (MI, N=20)Holcostethus limbolarius (DE, N=20)

Euschistus variolarius (DE, N=21)Euschistus variolarius (MI, N=17)

Euschistus tristigmus luridus (MI, N=20)Euschistus tristigmus (DE, N=26)

Euschistus servus euschistoides (MI, N=13)Euschistus servus (DE, N=20)

Cosmopepla lintneriana (OR, N=16)Cosmopepla lintneriana (DE, N=26)

Chlorochroa uhleri (OR, N=8)Chlorochroa uhleri (CA, N=8)

Chinavia hilaris (OR, N=19)Chinavia hilaris (MI, N=17)Banasa dimiata (OR, N=22)Banasa dimiata (MI, N=13)

live males live females unemerged parasitoids hatched nymphs unhatched nymphs

No-Choice Test Outcome (population variability)

Choice Test Outcome (as of 2015, Newark BIIR)

Caveat: Laboratory vs. Field Results

Slide: Courtesy of P. Mason

Observation of parasitoid behavior for

1 hour

Naïve, 24h-old female T. japonicus exposed to

egg masses - 1 hour - 4 hours - 6 hours

- 24 hours

BMSB P. maculiventris

No egg mass

parasitized (N = 8)

53%

Parasitism of BMSB

only (N = 6)

40%

Parasitism P. maculiventris only (N = 1)

7%

Parasitism of both egg

masses (N = 0)

0%

4 hours

No egg mass

parasitized (N = 9)

56%

Parasitism BMSB only

(N = 7) 44%

Parasitism P. maculiventris

only (N = 0)

0%

Parasitism of both

egg masses (N = 0)

0%

6 hours No egg mass

parasitized (N = 1)

7%

Parasitism of BMSB

only (N = 10)

66%

Parasitism P. maculiventris only (N = 0)

0%

Parasitism of both egg

masses (N = 4)

27%

24 hours

No egg mass

parasitized (N = 5)

33% Parasitism of BMSB

only (N = 8)

54%

Parasitism of P.

maculiventris only

(N = 2) 13%

Parasitism

of both egg

masses (N = 0)

0%

1 hour

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

Summary

Photo: E. Talamas ARS/SEL

0%10%20%30%40%50%60%70%80%90%

100%

2007 2008 2009 2010 2011 2012 2013 2014 2015

Naturally laid

Missing Sucking damage Chewing damage

Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped

Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

Fate of BMSB eggs in DE surveys 2007 to 2015

Sentinel Egg Masses

Naturally Laid Egg Masses

Sentinels vs. naturally laid

(wild)

0%10%20%30%40%50%60%70%80%90%

100%

2007 2008 2009 2010 2011 2012 2013 2014 2015

Naturally laid

Missing Sucking damage Chewing damage

Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped

Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

Fate of BMSB eggs in DE surveys 2007 to 2015

Sentinel Egg Masses

Naturally Laid Egg Masses

Missing or apparent predation

0%10%20%30%40%50%60%70%80%90%

100%

2007 2008 2009 2010 2011 2012 2013 2014 2015

Naturally laid

Missing Sucking damage Chewing damage

Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped

Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

Fate of BMSB eggs in DE surveys 2007 to 2015

Sentinel Egg Masses

Naturally Laid Egg Masses

BMSB nymphs (hatched & unhatched)

0%10%20%30%40%50%60%70%80%90%

100%

2007 2008 2009 2010 2011 2012 2013 2014 2015

Naturally laid

Missing Sucking damage Chewing damage

Nymph-Hatched Nymph-Unhatched Nymph-Undeveloped

Parasitoid-Emerged Parasitoid-Unemerged Parasitoid-Undeveloped

Fate of BMSB eggs in DE surveys 2007 to 2015

Sentinel Egg Masses

Naturally Laid Egg Masses

Parasitism (emerged & unemerged)

Compare with parasitism rates on native US pentatomids:

55.46 31.57 47.22 22.93 34.67 46.05 35.44 46.89 64.81 0

10

20

30

40

50

60

70

80

2007 2008 2009 2010 2011 2012 2013 2014 2015Perc

enta

ge p

aras

itize

d eg

gs (m

ean±

SE)

Other

Sentinel BMSB eggs (light grey) & naturally

laid BMSB eggs (dark grey):

% eggs parasitized in each egg mass (± SE)

Naturally laid eggs of other species (blue):

% parasitized per egg mass (± SE)

Note differences in Y-axis scale

0

50

100

150

200

250

300

350

400

450

500

Reject Accept

Tim

e un

til D

etec

tion

of E

gg m

ass

(in

sec

; mea

n ±

SE)

N = 6 N = 27 0

5

10

15

20

25

30

35

40

45

Reject Accept

Tim

e sp

ent a

nten

natin

g/vi

sit (

in

sec/

T sp

ent o

n EM

; mea

n ±

SE)

N = 27 N = 6

Oviposition (mean ± SE): 168.65 ± 11.5 s Marking (mean ± SE): 22.65 ± 2.32 s

F1,29 = 0.0312, P = 0.861 F1,28 = 5.87, P = 0.0224

No Yes