Causes and consequences of the host range expansion of in North America

Don Cipollini Department of Biological Sciences Wright State University Dayton, OH

Emerald ash borer (Agrilus planipennis)

June – July: Adults mate, females lay eggs on surface or in cracks of bark Late May – July: Adults emerge from D-shaped exit holes, feed on

July – Sept: Larvae feed on inner bark, grow and develop. May – June:: Pupation Oct – April: Larvae overwinter as pre-pupa

Host range in insects

• The host range is the number of species utilized by an insect species; narrow range=specialist, broad range=generalist

•A host range expansion is an increase in the number of host species utilized by an insect species

•A host shift is the addition of a new host to the diet of a species, with a concomitant reduction in the ability to use its ancestral host(s) Ecological fitting

• When organisms encounter novel environmental conditions - a new habitat, a changed climate, novel hosts - they survive and persist where and if they "fit" by means of characteristics they already possess.

• Host shifts are often initiated because the pest is “preadapted” to the novel host. The novel host might share important characteristics with the ancestral host or it might have been used in the past.

• (Agosta et al. 2010) Soapberry Bug Jadera haematoloma

Specializes on members of the Sapindaceae in the New World Tropics Taiwanese Rain Koelreuteria elegans

Balloon Vine Cardiospermum corindum (Carroll et al. 1992) Wallander and Albert 2000 White fringetree, virginicus L. ()

Yellow Springs, Ohio May 15, 2016 “Grancy Greybeard” “Old Man’s Beard”

Yellow Springs, Ohio Little Miami River Bike Trail August 17, 2014

Yellow Springs, Ohio Dayton, Ohio Private Residence Cox Arboretum August 29, 2014 September 20, 2014

Springfield, Ohio Ferncliff Cemetery and Arboretum October 8, 2014 Emerald ash borer specimen used to certify white fringetree as a new host record by the USDA Systematic Entomology Laboratory on October 13, 2014 • 4 of 20 (now 10) white fringetrees had either one or more EAB exit holes or galleries • One debarked tree produced ~10 live larvae and a dead adult confirmed to be EAB

Top pest report of the last two years; Greenhouse Grower magazine (2015) In what sorts of landscapes have attacks occurred and what factors are associated with attack? Spring Grove Cemetery and Arboretum

Cincinnati, Ohio: 733 acres, 30 white fringetrees

Exit holes on Ohio state champion white fringetree 108th and Central Park Ave., Chicago, IL

Courtesy of Jim Tresouthick, Urban forester, Homewood, IL

North Park, Pittsburgh

• First non-managed population found to be infested

• 31 of 60 infested

• Infested trees had lower canopy ratings than uninfested trees

OARDC

Core Arboretum, WVU

University of Kentucky

Guilford County, NC Characteristics of attacked trees

Variable Infested Uninfested P-value trees trees

Basal stem diameter (cm) 10.1 (±0.8) 6.3 (±0.4) <0.001

Percent of trees with 68.1 29.0 <0.001 dieback (%)

Epicormic branching (%) 65.9 20.8 <0.001 Sex ratio (M:F) 1.47 2.19 0.283 Ash adjacency (m) 57.4 (±9.5) 100.6 (±8.7) 0.007 White fringetree adjacency 76.6 (±14) 57.6 (±7.5) 0.219 (m)

Peterson and Cipollini 2016 How long have attacks occurred and how successful have they been? Dayton, Ohio Cox Arboretum September 20, 2014

Vanessa Lopez Annie Ray Scott Gula Emerald ash borer reared from white fringetree stems collected at Spring Grove Cemetery and Arboretum

Emerged on April 8, 2015 from stems placed in laboratory on February 3, 2015 Thiemann et al. 2016 ABGallery 2014, Exit hole 2015 Gallery 2011

C Gallery 2013 D Gallery 2013

Thiemann et al. 2016 Yellow Springs

Springfield

Dayton

Cincinnati 1

Cincinnati 2 Tree

Cincinnati 3

Cincinnati 4

Cincinnati 5

Cincinnati 6

0 102030405060708090

Number of Galleries per Square Meter

Thiemann et al, 2016

Can adults complete maturation feeding on white fringetree leaves? Adult feeding bioassays White fringetree Green ash

Peterson and Cipollini, in prep

Why have attacks occurred and what else is at risk? Is this white fringetree drought stressed? octane 5.00 4-hydroxy-4-methyl-2-pentanone (Z)-3-hexenol

α-pinene 3-methyl nonane sabinene myrcene

10.00 decane (Z)-3-hexenyl acetate

(E)-β-ocimene Canopy VolatileOrganicCarbons Black Ashvs.WhiteFringeTree

linalool nonatriene 15.00

methyl salicylate 20.00

nonyl acetate (standard) 25.00 α-copaene

(E)-caryophyllene α-trans-bergamotene α-humulene

30.00 germacrene D δ-cadinene (E)-(E)-α-farnesene (Z)-3-hexenyl benzoate Black Ash White Fringe

green ash white fringetree pennsylvanica

Chinese fringetree devilwood Chionanthus retusus Osmanthus americanus

Cipollini and Rigsby 2015 Pygmy fringetree, Sandhills Preserve, Orange County, 5-cm diameter pygmy Emerald ash borer gallery fringetree stem and exit hole in 1 cm diameter stem of white fringetree EAB feeding gallery lengths on white and pygmy fringetree

Species 2 weeks 3 weeks

White Fringetree 10.5 cm 23 cm

Pygmy fringetree 9.5 cm 21.7 cm

PFT stems provided by staff of Archbold Biological Station Florida swampprivet Forestiera segregata Cultivated olive, Olea europaea Cultivated olive in Melbourne, FL Olive Stem Bioassay February-October 2016

• Large stem from olive, cv. Manzanilla (18 cm diameter at base, ~50 yrs old) • Field grown near Lemon Cove, California under standard olive cultivation First emerald ash borer recorded emerging from an olive stem

“Oliver” emerged on August 31, 2016

Cipollini et al, in revision Summary • ~30% of ornamental white fringetrees examined had exit holes or galleries characteristic of EAB; higher rates observed in a high density unmanaged populations

• Attack found across U.S. (OH, IN, IL, PA, KY, WV, NC); attacks concurrent with attack on ash and likely due to shared signals

• Attack rate increases with tree size and adjacency to ash; attacked trees have lower canopy ratings

• Trees in urban landscapes have regularly supported EAB through adult emergence for several years; currently evaluating adult maturation feeding on leaves

• EAB may threaten other hosts, but may need ash trees to be a real problem Acknowledgements

• Yellow Springs Tree Committee • Juliane Chaney, Stanley Spitler, Rich Pearson, Kevin Bradbury, Brian Heinz, Dave Gressley, Dave Apsley, Paul Van Ausdal, Patrick Kelsch, Rich Larson, Lloyd Kennedy, Robert Gage, Tom Tiddens • Cox Arboretum, Ferncliff Cemetery and Arboretum, Spring Grove Cemetery and Arboretum, Morton Arboretum, Dawes Arboretum, Chicago Botanic Garden • John Stireman, Matt Duncan, Sam Davis, Chad Rigsby, Dani Thiemann, Donnie Peterson; Wright State • Dan Herms; Ohio State • Jim Zablotny; USDA-APHIS • Lourdes Chamorro; USDA-ARS • Vanessa Lopez, Annie Ray; Xavier University

• USDA-APHIS 15-8130-0539-CA