Potato psyllids and associated pathogens: A diagnostic aid - Susan Halbert Joseph E Munyaneza
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Potato psyllids and associated
pathogens:
A diagnostic aid
Susan Halbert
Florida Department of Agriculture & Consumer Services, Division of
Plant Industry
Joseph E Munyaneza
USDA-ARS, Yakima Agricultural Research Laboratory, Wapato, WA
World species of potato psyllids
• Bactericera cockerelli (Šulc, 1909)
– North America Photo: Joe Munyaneza
• Russelliana solanicola Tuthill, 1959
– South America
• Bactericera nigricornis (Förster, 1848)
– Eurasia
• Acizzia solanicola Kent & Taylor, 2010
– Additional species known from eggplant
in Australia Photo: Deborah Kent
Bactericera cockerelli,
the North American potato psyllid
• Most studied of the group
• Known to transmit at least one Candidatus
Liberibacter sp.
Photo: Joe Munyaneza, USDA/ARS
Adults of Bactericera cockerelli
Photos: Joe Munyaneza, USDA/ARS
Nymphs of Bactericera cockerelli
Photos: Joe Munyaneza, USDA/ARS
Eggs of Bactericera cockerelli
Photos: Joe Munyaneza, USDA/ARS
Systematics • Original description: Šulc, K. 1909. Trioza cockerelli. n. sp., novinka ze Severní Ameriky, Mající I hospodářský význam. Acta Societatis Entomologicae Bohemiae 4: 102-109. Pages 107-109 are an English translation of the paper. • To genus Paratrioza (Crawford, 1911) • To genus Bactericera (Burckhardt & Lauterer, 1997)
Systematics, cont. • Described from pepper (Capsicum) in the garden of Professor T.D.A. Cockerell, University of Colorado, Boulder. Photo: Thomson Paris, FDACS/DPI
How to recognize Bactericera cockerelli
• Found on Solanaceous crops
• Look for trifurcating wing
veins
• Look for very short genal
cones
• Dark psyllid with light
patterns, especially a light
raised rim around the dorsal
part of the head (see below)
• There is at least one similar
species in the same genus on
native Lycium (Solanaceae),
but it does not colonize crops B. Cockerelli wing, ventral aspect
(see below). of head
Photos: Thomson Paris, FDACS/DPI
Other North American Bactericera • Bactericera is a large and difficult genus. • If psyllids are found on plants outside Solanaceae, microscopic analysis by a taxonomist is required to determine if they are B. cockerelli. • There is at least one species of Bactericera on N. American Solanaceae: Bactericera dorsalis (Crawford, 1914) on Lycium carolinianum. • Photo of Lycium: http://www.florida.plantatlas.usf.edu/Plant.aspx? id=3149
Bactericera cockerelli and
Bactericera dorsalis
• B. dorsalis lacks genal cones (present in B.
cockerelli)
• B. dorsalis lacks well-defined white ridge around
the dorsal aspect of the head
B. cockerelli B. dorsalis
Photos: Susan Halbert, FDACS/DPIBactericera cockerelli Above: Head, showing genae Right: Male genitalia, showing male capsule and detail of the tip of the aedeagus Photos: Thomson Paris and Susan Halbert, FDACS/DPI
Bactericera dorsalis
Body, male genitalia
Photos: Thomson Paris, FDACS/DPIBactericera nymphs
Bactericera cockerelli Bactericera dorsalis
Photos: Thomson Paris, FDACS/DPIDistribution of B. cockerelli • Mexico, north to southern Canada • Species is migratory, overwintering in Mexico and Texas, and maybe in Central California. Other areas are colonized each year. In some years, populations do not reach the northern areas such as Canada, Washington, and Idaho. • Present in Honduras (FSCA specimens), but not recorded in Brown and Hodkinson’s (1988) book on psyllids of Panama
Distribution, continued • Two biotypes are known (Liu et al. 2005). One is the historical population in Mexico and the central states. A new one is found in the far western USA. • Bactericera cockerelli apparently does not occur in the eastern states of the USA. Liu, D.-g., Trumble, J.T., and Stouthamer, R. 2006. Genetic differentiation between eastern populations and recent introductions of potato psyllid (Bactericera cockerelli) into western North America. Entomologia Experiemntalis et Applicata 118: 177-183.
Distribution map of Bactericera
cockerelli in the Americas
• Lighter blue areas are colonized intermittently.
Map: Scott Burton
FDACS/ Div. Plant IndustryInterceptions and regulatory issues
• Bactericera cockerelli was introduced into New
Zealand, where it is causing major damage.
• Florida has intercepted this species on
poblano peppers from Mexico.
Psyllid nymphs hide
under the calyx of
the peppers
Photo: Susan Halbert, FDACS/DPIHost plants
• Species has a strong preference for
Solanaceae, including important crops: potato,
pepper, tomato, eggplant.
• Also known from plants outside the
Solanaceae. The species appears polyphagous
in comparison with most psyllids. See New
Zealand’s illustrated list for examples:
– http://www.potatoesnz.co.nz/users/Image/Graphi
cs/PDFS/Psyllid_fact_sheets_-_hosts_lr.pdfRegulatory issues, continued • 19 interceptions of Triozidae from Mexico on peppers in the USDA interception database • 1 interception of Bactericera from eggplant from Mexico • Insects were on fruit or stem (one instance) • Infested fruit was in baggage or permit cargo
Associated pathogens and damage due
to Bactericera cockerelli
• Damage to potato crops from potato psyllids
has been recorded in North America since the
1930s. It has been called “Psyllid yellows.”
• Damage might result from:
– Toxins secreted by the insects (no pathogens)
– Candidatus Liberibacter spp. transmitted by the
insects
– Candidatus Phytoplasma spp. transmitted by the
insectsStatus of damage possibilities • Toxin alone: Some damage is possible, but it does not occur in all cultivars. • Candidatus Liberibacter spp.: Damage confirmed and severe. Disease known as Zebra Chip (please see below) • Candidatus Phytoplasma spp.: Probably not transmitted by B. cockerelli (Munyaneza et al. 2007 a, b) •Munyaneza, J.E., Crosslin, J.M., and Upton, J.E. 2007. Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip,” a new potato disease in southwestern United States and Mexico. J. Econ. Entomol. 100: 656-663. •Munyaneza, J.E., Goolsby, J.A., Crosslin, J.M., and Upton, J.E. 2007. Further evidence that zebra chip potato disease in the lower Rio Grande Valley of Texas is associated with Bactericera cockerelli. Subtropical Plant Sci. 59: 30-37.
Liberibacter-free
psyllids:
Psyllid yellows
(in cv. Atlantic)
Liberibacter-infective psyllids
Zebra Chip symptoms
Photos: Joe Munyaneza, USDA/ARSZebra Chip (ZC) disease • Range of foliar symptoms Early disease symptoms (Similar to Potato leafroll virus) Photos: Joe Munyaneza, USDA/ARS Severe foliar symptoms of zebra chip disease
Photo: Gary Secor, N. Dakota State University
Photos (except top left): Joe Munyaneza, USDA/ARSChiligatoro, Intibucá, Honduras (2009)
Photo: Jose Melgar, FHIA, HondurasZC symptoms, continued
• ZC symptoms in tubers and chips
• Final diagnosis depends on observing the fried
chips, and molecular confirmation of the pathogen.
Photos: Joe Munyaneza, USDA/ARSBrown to pinkish
(collapsed) stolons
Healthy Tuber
Photos: Joe Munyaneza, USDA/ARSPhotos: Joe Munyaneza, USDA/ARS
Secor
Papa manchada Papa rayada
Secor
Photos: Joe Munyaneza, USDA/ARSPhotos: Joe Munyaneza
Photos: Joe Munyaneza
Zebra
ChipPhotos: Joe Munyaneza
Photo: Joe Munyaneza, USDA/ARS
Russelliana solanicola
The South American potato psyllid
• Not much information about biology of this insect
• Possibly associated with a vectored pathogen
thought to be a virus (SB 26/29) (Chavez et al.
2003, Salazar 2006)
– http://aridaterra.uta.cl/scielo.php?script=sci_arttext&pid=S0073-46752003000100001&lng=en&nrm=iso&tlng=es
– http://www.springerlink.com/content/7803113640r88015/
Photos: Verónica Cañeda, International Potato Center (CIP)Systematics
• Described as Russelliana solanicola Tuthill
– Tuthill, L.D. 1959. Los Psyllidae del Perú Central (Insecta:
Homoptera). Revista Peruana de Entomologia Agricola 2:
1-27. (description with illustration on p. 12)
http://rameau.snv.jussieu.fr/psyllespdf/76.pdf
• Revision that includes most of the genus (including all
on Solanaceae) can be found in Burckhardt 1987.
– Burckhardt, D. 1987. Jumping plant lice (Homoptera:
Psylloidea) of the temperate neo tropical region Part 1:
Psyllidae (subfamilies Aphalarinae, Rhinocolinae, and
Aphaloidinae). Zoological Journal of the Linnean Society
89: 299-392. (Russelliana on pages 365-end)Systematics, continued • An obscure species, Bactericera solani Ruebsaamen 1908 also may occur on S. American Solanaceae. • Bactericera solani was described from Solanum sp. from Rio de Janeiro, Brazil. • Species description based on nymphs pressed in botanical specimens. Apparently the edges of the leaves were rolled. • Original description on page 59 (45-46 of free pdf): – http://rameau.snv.jussieu.fr/psyllespdf/216.pdf
How to recognize Russelliana
solanicola
• Note bifurcating wing veins
• Male genitalia characteristic of genus (bird-like
structure on the aedeagus)
• Other species of Russelliana not known from
potato (but see Burckhardt 1987 if unsure)
Russelliana solanicola wing
(about 2.5 or more times as long as wide
Russelliana solanicola male genitalia
Photos: Thomson Paris, FDACS/DPIRusselliana solanicola Photos: Natasha Wright, FDACS/DPI/CAPS
Russelliana solanicola
Head, showing relative length of
genal cones
Close-ups of wing, showing spinules.
Russelliana solanicola wings do not have a
break in the spinule pattern along the veins.
No spines on metatarsus
Photos: Thomson Paris, FDACS/DPIDistribution
• Not known to occur outside of South America
• Reported from Argentina, Chile, Peru
http://rameau.snv.jussieu.fr/psyllespdf/76.pdf
• Specimens from Brazil in Florida State Collection of
Arthropods
• Not known if ranges of North and South American
potato psyllids overlap, but unlikely, as neither is
reported in an extensive work on psyllids of Panama
– Brown, R.G. and I.D. Hodkinson. 1988. Taxonomy and
ecology of the jumping plant-lice of Panama (Homoptera:
Psylloidea). Entomonograph 9. E.J. Brill/Scandinavian
Science Press Ltd. Leiden, New York København, Köln. 304
pp.Distribution map for
Russelliana solanicola
Map: Scott Burton, FDACS/DPIRegulatory issues • This pest is a quarantine pest for the USA and for the State of Florida • Interceptions are not known • Not known if R. solanicola infests fruit of peppers and tomatoes (unlikely on potato tubers)
Hosts of Russelliana solanicola • Described from Datura (Solanaceae) – http://rameau.snv.jussieu.fr/psyllespdf/76.pdf • Pest of potato and possibly other solanaceous crops • Chávez et al. 2003 have a more extensive list, including several plants in the Compositae – http://aridaterra.uta.cl/scielo.php?script=sci_arttext&pid=S0073-46752003000100001&lng=en&nrm=iso&tlng=es
Hosts, continued • Crops reported as hosts: – Potato – Tomato – Pepper • Hosts reported in Compositae (Chávez et al. 2003): – Marigold – Flaveria bidentis • Source: Chávez et al. 2003 (see previous slide)
Pathogens associated with
Russelliana solanicola
• Severe damage to potato, thought to be caused
by a virus, SB 26/29
– http://www.pestalert.org/newsAlertDocs/EPPO%2020
06%20No.11.pdf
– http://aridaterra.uta.cl/scielo.php?script=sci_arttext&
pid=S0073-
46752003000100001&lng=en&nrm=iso&tlng=es
– http://www.springerlink.com/content/7803113640r8
8015/
– http://www.crawfordfund.org/assets/files/awards/Pot
ato_Viruses_after_the_20th_Century.pdfPathogens, continued
Information from Salazar1
• Purified virus contained isometric particles.
• Two bands at 7.5 and 6.2 Kb
• Mechanically transmissible with difficulty to Nicotiana
occidentalis, Nicotiana benthamiana, and Physalis
floridana
• Some torrado viruses have these characteristics and do
infect potatoes (Personal communication, Dr. Carlye
Baker, FDACS, Division of Plant Industry). Known
torrado viruses are transmitted by whiteflies.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2880234/
(see illustration of gel, which shows bands of similar weights).
1. 16th Triennial Conference of the European Association of Potato Research, 2005, Bilboa, Spain.SB 26/29 • Severe tuber and foliar symptoms • Illustration from Salazar 2003 – http://www.crawfordfund.org/assets/files/awards/Potato_Viruses_after_the_20th_Century.pdf
Pathogens, continued
• Disease can cause up to 80% yield loss
– http://www.springerlink.com/content/780311364
0r88015/
• Neither the diseased potato plants nor the
psyllids have been tested for fastidious
prokaryotes, to our knowledge
• More research is needed to determine the
nature of this disease and its pathogens.Bactericera nigricornis
Old World potato psyllid
• Ranges from Europe into Central Asia, south
to the Middle East and North Africa
• Host range confusing due to taxonomic
problems
• Recent problems in Iran (Fathi 2011, see
below) suggest that this species might
transmit plant pathogens
• No photographs available at the present timeSystematics
• Described by Förster from Frankfurt, Germany
in 1848 as Trioza nigricornis
• Became Bactericera nigricornis
– Ossiannilsson, F. 1992. The Psylloidea (Homoptera) of Fennoscandia and Denmark.
Fauna Entomologica Scandinavica 36: 346 pp. E.J. Brill, Leiden (Netherlands).
• Synonym: Trioza brassicae Vasil’ev 19221
– Burckhardt, D. and P. Lauterer. 1993. The jumping plant-lice of Iran (Homoptera,
Psylloidea). Revue Suisse de Zoologie 100(4): 829-898.
Note: The B. brassicae form might have a pale antennal segment 3, whereas the
original B. nigricornis has a dark antennal segment 3. (Please see below.)Taxonomic treatment of Bactericera
nigricornis and closely related species
• Hodkinson, I.D. Status and taxonomy of the Trioza
(Bactericera) nigricornis Förster complex (Hemiptera:
Triozidae)
– Three species with overlapping host ranges
– T. (B.) brassicae, included as fourth species, later
synonymized with B. nigricornis (see previous slide)
– Paper deals with host plants and distribution
– Key to species in the complex, including B. nigricornis,
Bactericera trembayi (Wagner), Bactericera trigonica
Hodkinson (described in the paper), and the now
synonymized B. brassicae. Color of antennal segment 3 is
discussed.
– http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=2378204Closely related species, continued
• Burckhardt, D. and J. Freuler. 2000. Jumping
plant-lice (Hemiptera, Psylloidea) from sticky
traps in carrot fields in Valais, Switzerland.
Mitteilungen der Schweizerischen
Entomologishchen Gesellschaft 73: 191-209.
– Keys to adult and nymphal triozids on carrots,
including Bactericera nigricornis
– http://www.cabdirect.org/abstracts/20013010426.html;jsessionid=0C56E50D1B4F796FBE1C8A9BB7DE65A5How to recognize
Bactericera nigricornis
• Use above two references to separate
Eurasian triozids on carrots and potatoesHow to separate Bactericera
nigricornis from Bactericera cockerelli
• According to Burckhardt & Lauterer (1993),
antennal segments 4-7 of B. nigricornis and
Bactericera trigonica are dark. Bactericera
cockerelli has striped ones.
Right: antennae of Bactericera
cockerelli. Note the stripes.
Bactericera nigricornis has dark
antennal segments 4-7.
Bactericera nigricornis can have
light or dark antennal segment
three.
Burckhardt, D. and P. Lauterer. 1993. The jumping plant-lice of Iran (Homoptera,
Psylloidea). Revue Suisse de Zoologie 100(4) 829-898.
Photo: Thomson Paris, FDACS/DPIHow to separate Bactericera
nigricornis from Bactericera cockerelli
• Bactericera cockerelli with wing spinules will key to
Bactericera femoralis (Förster 1848) in Burckhardt &
Freuler 2000. Bactericera cockerelli sometimes has
spinules on the surface of the wing, whereas B.
nigricornis does not. Bactericera femoralis is not on
Solanaceae.
• Bactericera cockerelli without wing spinules will key to
Bactericera trigonica. The antennae should separate
these species (distal segments dark for B. trigonica and
striped for B. cockerelli).
Right: Wing spinules that
occur on some B. cockerelli
Photo: Susan Halbert, FDACS/DPIOther Old World psyllids on
Solanaceae
• We could not find any other Old World psyllids
listed as feeding on potatoes, other than the ones
in the B. nigricornis complex.
• Several obscure species of Diaphorina feed on
other plants in the family Solanaceae. They are
not known from potatoes.
– Diaphorina solani Capener 1970, South Africa
– Diaphorina luteola Loginova 1978, Arabian peninsula
and surrounding areas.
• Burckhardt, D. and D. Mifsud. 1998. Psylloidea (Insecta:
Hemiptera) of the Arabian Peninsula. Fauna of Arabia 17-7-
49. (good key to Arabian species of Diaphorina)Distribution of Bactericera nigricornis Map: Scott Burton, FDACS/DPI
Regulatory issues • No quarantines known • 7 interceptions of Bactericera sp. on dill from the Middle East listed in the USDA database • 1 interception of Triozidae from Brassica from Italy in USDA database • 15 interceptions of Bactericera spp. on coriander from the Middle East in USDA database • 7 interceptions of Bactericera spp. on parsley from the Middle East in USDA database
Hosts • Host range is very uncertain as a result of taxonomic confusion due to several closely related polyphagous species with overlapping host ranges (see above). • Crops include potatoes, various cole crops, carrots, and maybe onions. Status of other Umbelliferae not known. • Go to the following website and type Bactericera nigricornis into the search line for host information: http://rameau.snv.jussieu.fr/cgi- bin/psyllesexplorer.pl?lang=en • More host information can be found in Hodkinson 1981 and Burckhardt & Freuler 2000
Associated pathogens
• No proven associated pathogens
• Trioza apicalis and species in the B. nigricornis
complex may transmit Candidatus Liberibacter
solanacearum in carrots1
– Overlapping host ranges would provide ample
opportunity for B. nigricornis (which can feed on
carrot) to acquire these pathogens.
1. Source for Liberibacter in carrots: Munyaneza, J.E., T.W. Fisher, V.G. Sengoda,
S.F. Garczynski, A. Nissinen, and A. Lemmetty. 2010. Association of “Candidatus
Liberibacter solanacearum” with the psyllid, Trioza apicalis (Hemiptera: Triozidae)
in Europe. J. Econ. Entomol. 103: 1060-1070.Associated pathogens, continued
• Potato plants in Iran that are infested with B.
nigricornis develop “a striped pattern of
necrosis in the tuber cross-section,” suggestive
of zebra chip disease.
– Fathi, S.A.A. 2011. Population density and life-
history parameters of the psyllid Bactericera
nigricornis (Forster) on four commercial cultivars
of potato. Crop Protection 30: 844-848.
http://www.citeulike.org/article/9188175Acizzia solanicola
Australian eggplant psyllid
• Recently discovered pest of eggplant
Female Acizzia solanicola (teneral specimen)
Photo: Deborah Kent, University of Adelaide, Australia. Used by permission.Systematics • Described from eggplant in Australia • Kent, D. and G. Taylor. 2010. Two new species of Acizzia Crawford (Hemiptera: Psyllidae) from the Solanaceae with a potential new economic pest of eggplant, Solanum melongena. Australian Journal of Entomology 49: 73-81. • Description available free: http://onlinelibrary.wiley.com/doi/10.1111/j.144 0-6055.2009.00739.x/pdf
Male Acizzia solanicola Photo: Deborah Kent, University of Adelaide, Australia. Used by permission.
How to recognize Acizzia solanicola
• Bifurcating wing veins (similar to Russelliana)
• No dorsal pattern on the thorax
• Lacks ornate male genitalia of Russelliana
Head, wing, and male genitalia drawing, taken
from Kent & Taylor 2010. Used by permission.How to recognize Acizzia solanicola
• Nymph covered with long setae
• Honeydew excreted in bags of various sizes
Color photo: Deborah Kent, University of Adelaide, Australia. Used by permission.
Black & white photo: from Kent & Taylor 2010. Used by permission.Distribution • Known only from coastal New South Wales (north of Sydney), and from Adelaide, Australia (see map below) • The origin of this insect is not known. Either it has been introduced into Australia, or it made a host switch to cultivated eggplant. Source: Kent & Taylor 2010
Regulatory issues • None known.
Hosts • Eggplant (Solanum melongena) • Solanum mauritanum (wild tobacco bush) • Will not feed on tomato or pepper Source: Kent & Taylor 2010
Damage and associated pathogens • Feeding by nymphs deforms leaves and causes wilting and premature senescence of new leaves and flowers. • Loss of flowers causes crop loss, which can be severe. • No pathogen transmission is known. Source: Kent & Taylor 2010
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