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Cold tolerance of two potential biological control agents of the brown marmorated stink bug
Erica Nystrom1, Robert Venette2, Christine Dieckhoff3, Kim Hoelmer3 and Robert L. Koch1
1Department of Entomology, University of Minnesota, Saint Paul, MN2USDA-FS, Saint Paul, MN 55108
3USDA-ARS-BIIRU, Newark, DE 1971
© Christopher Hedstrom
© Brandon Woo© Pierre Bornand
Photo by Stephen Ausmus
Halyomorpha halys (Stål) (Pentatomidae)The brown marmorated stink bug (BMSB)
BMSB detected
Nuisance problems only
Agricultural and nuisance problems
Severe agricultural and nuisance problems
Stopbmsb.org 2016
Minnesota Department of Agriculture 2016
Instar 1
Eggs
Adult
5
4
3
2
Diagram adapted from Oregon State University Extension Service
Halyomorpha halys life cycle
150+ diverse plant species are at risk,
and the value of susceptible crops exceeds $21 billion
Hoebeke and Carter 2003; Leskey et al. 2012 Photos by Ric Bessin, Doug Pfeiffer, David Wright, and Eric Day
Photo by StopBMSB.orgInkley 2012; Lee 2014
Photo from istockphoto.comLeskey et al. 2012
Hamilton et al. 2014; Herlihy et al. 2015; Ogburn et al. 2016 Photo by University of Maryland Extension
Classical biological control: “The regulation of a pest population
(insect, mite, mammal, weed, pathogen) by exotic natural enemies (parasites, predators, pathogens) that are importedfor this purpose.”
Caltagirone 1981
Natural enemy survey locations in Asia
Hymenoptera: Scelionidae• Trissolcus mitsukurii• Trissolcus itoi• Trissolcus cultratus• Trissolcus japonicus
Natural enemy survey locations in Asia
Hymenoptera: Scelionidae
Trissolcus japonicus
Trissolcus cultratus
Photos by Chris Hedstrom and Pierre Bornand
© Chris Hedstrom
© Pierre Bornand
Trissolcus spp. life cycle
Diagram adapted from Hoffman and Frodsham 1993
Larva develops in host egg
Pupa in blackened host egg
Adult emerges
Female lays egg in host egg
Photo by Mark JohnsonLee 2010
Carillo et al. 2004; Stephens et al. 2015
Carillo et al. 2004; Stephens et al. 2015
Carillo et al. 2004; Stephens et al. 2015
Supercooling point (freezing)
Time
Tem
per
atu
re °
C0°C
Temperature °C 0 °C
Pro
po
rtio
n f
reez
ing
-30 °C
100
0
Cumulative freezing curve
Lower lethal temperature (mortality)
Time
Tem
per
atu
re °
C0°C
Time
Tem
per
atu
re °
C0°C
Temperature °C 0 °C
Pro
po
rtio
n m
ort
alit
y
-30 °C
100
0
Cumulative mortality curve
How are freezing and
mortality related?
Renault et al. 2002
Temperature °C 0 °C
Pro
po
rtio
n m
ort
alit
y
-30 °C
100
0
Mortality occurs after freezing
Temperature °C 0 °C
Pro
po
rtio
n m
ort
alit
y
-30 °C
100
0
Mortality = freezing
Temperature °C 0 °C
Pro
po
rtio
n m
ort
alit
y
-30 °C
100
0
Mortality occurs before freezing
Ecological relevance of cold tolerance measurements
Renault et al. 2002
At what temperatures do T. japonicus and T. cultratus
experience freezing and mortality?
Renault et al. 2002
Trissolcus cultratusTrissolcus japonicus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Tsukuba 1, Japan
Tsukuba 2, Japan
T. cultratus
Cold tolerance assays
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
Proportion freezing Proportion mortality
Beijing, China
Tsukuba, Japan
Pucheon, S. Korea
Nanjing, China
T. japonicus T. japonicus
Tsukuba 1, Japan
Tsukuba 2, Japan
T. cultratus
a
a
ab
b
Supercooling point results±
SE
Population: df = 3, χ²= 9.59, p = 0.02
Freezing results (T. japonicus)
a
a
ab
b
±SE
50% of populations of T. japonicus freeze at -21 °C
Population: df = 3, χ²= 9.59, p = 0.02
a
a
a
a
< >±
SEMortality results (T. japonicus)
Population: df = 3, χ²= 0.12, p = 0.99
a
a
a
a
< >±
SE50% of populations of T. japonicus die at -19 °C
Population: df = 3, χ²= 0.12, p = 0.99
< >Comparing mortality and freezing (T. japonicus)±
SE
Assay: df = 1, Z = 6.74,p < 0.001
Assay: df = 1, Z = 3.44,p < 0.001
Assay: df = 1, Z = 2.29,p = 0.02
Assay: df = 1, Z = 6.46,p < 0.001
< >All populations of T. japonicus die before freezing±
SE
Assay: df = 1, Z = 6.74,p < 0.001
Assay: df = 1, Z = 3.44,p < 0.001
Assay: df = 1, Z = 2.29,p = 0.02
Assay: df = 1, Z = 6.46,p < 0.001
Mortality results (T. cultratus)±
SE a
a
Population: df = 1, χ²= 0.01, p = 0.98
Mortality results (T. cultratus)±
SE50% of populations of T. cultratus die at -19 °C
a
a
Population: df = 1, χ²= 0.01, p = 0.98
Conclusions?
Conclusions?
The ecologically relevant measure of cold tolerance for T. japonicus is lower lethal temperature.
Conclusions?
The ecologically relevant measure of cold tolerance for T. japonicus is lower lethal temperature.
50% of populations from both species die at -19 °C, which is below lethal temperatures for H. halys.
Conclusions?
The ecologically relevant measure of cold tolerance for T. japonicus is lower lethal temperature.
50% of populations from both species die at -19 °C, which is below lethal temperatures for H. halys.
From a cold tolerance standpoint, all populations of both species are equally suitable for introduction.
How do our laboratorymeasurements compare to
field conditions?
Plant Hardiness Zone MapAverage Annual Extreme Minimum
Temperature (1976-2005)
T. japonicus
Plant Hardiness Zone MapAverage Annual Extreme Minimum
Temperature (1976-2005)
T. japonicus
Plant Hardiness Zone MapAverage Annual Extreme Minimum
Temperature (1976-2005)
T. japonicus
T. japonicusH. halys
Plant Hardiness Zone MapAverage Annual Extreme Minimum
Temperature (1976-2005)
T. japonicusH. halys
Plant Hardiness Zone MapAverage Annual Extreme Minimum
Temperature (1976-2005)
Photo by Chuck Ingels
What about additionalmeasurements of cold
tolerance?
Longevity
Longevity
Acclimation
Longevity
Acclimation
Lower lethal time
AcknowledgementsMany people helped make this project possible through financial, technical, and moral support:
USDA-ARS-BIIRU: Kathleen TatmanMDA-MAES: Stephanie Dahl, Nik Prenevost, and Jeanne CiborowskiUMN support: The Salt Journal Group; Koch, Venette, Hutchison, and Aukema lab members. Especially Amy Morey, Theresa Cira, Lindsey Christianson, James Menger-Anderson, and Jaana Iverson.Michigan State: Paul Botch and Patricia Samota
Funding for this project was provided by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative‐Citizen Commission on Minnesota Resources
(LCCMR), and the Minnesota Soybean Research and Promotion Council.
Photo by Elijah Talamas
Questions?
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