General comments about biological control

Aphid advantages:

Rapid colonization (winged forms) followed by rapid reproduction (wingless forms)

The aphid’s best defense is its reproductive rate Results in a ‘threshold effect’: Replacement rate > rate = biocontrol failure Effective biological control requires the timely recruitment of multiple natural enemy

New aphid invasions normally have 3 phases: Epidemic phase, Attenuation phase, Endemic phase

Eventually (5 – 30 years?), natural biological control evolves and the aphid becomes a sporadic problem associated with BC disruption How (partially) resistant varieties reduce losses to 1

Susceptible 0.8 plant Resistant plant 0.6 No. aphids No. 0.4 Economic Injury Threshold

0.2

0

Time Resistant varieties require the support of biological control Natural Enemies Groups Important in Aphid Biocontrol

Primary groups

Coccinellidae (lady ) Syrphidae (hover )

Chrysopidae (green lacewings) Braconidae (aphidiine wasps)

Secondary groups

Chamaemyiidae (aphid flies) Aphelinus spp. (aphelinid wasps)

Hemiptera: (predatory bugs) Hemerobidae (brown lacewings) Anthocoridae (flower bugs) Nabidae (damsel bugs)

Entomopathogens (humid conditions only) : Hippodamia convergens

• High aphid consumption / reproductive rate • Drought tolerant • Capable of extended summer diapause (survives aphid scarcity) • Uses a wide range of plant resources as supplementary food • Good overwintering survival in severe winter conditions • Lab research shows M. sacchari is as suitable as greenbug for both development and reproduction of H. convergens Numerical response of H. convergens to M. sacchari Coccinellidae: Coccinella septempunctata (C7)

• A true aphid specialist (larvae develop ONLY on aphid food) • A large and voracious species • Not a native species – introduced from Europe • Widely distributed in NA • Second most abundant species on the High Plains (after Hcon) Coccinellidae: Harmonia axyridis (Asian multicolored LB)

• Another exotic invader – from Asia • A large, voracious species with a broad diet range • status (fruit crops and house invasions) • Also a strong competitor and intraguild predator • Normally arboreal - prefers trees to herbaceous plants • Has played an integral role in controlling • Relatively rare on the High Plains compared to other invaded habitats Coccinellidae: sanguinea (Blood-red LB)

• A subtropical species, largely arboreal • Not capable of hibernation or surviving hard freezes • Valuable in for controlling aphids and psyllids • Related species, Cycloneda munda, has more northern distribution • However, C. munda has become increasing rare • Neither species of Cycloneda will contribute much to SCA control Coccinellidae: Olla v-nigrum (Ash gray ladybeetle) stigma

• Another arboreal, largely subtropical species • Widely distributed in the lower 48 states and into Canada • Valuable in citrus for controlling aphids and psyllids • Not likely to contribute much to SCA control Melanic form Olla v-nigrum

C. septempunctata Coccinellidae: Coleomegilla maculata (12 spot ladybeetle)

• A common species with a very wide range of prey • Very omnivorous - an complete development on pollen only • Widely distributed across all • Has a very high water demand in both adult and larval stages • Not very abundant in arid regions of the High Plains • Lab studies show SCA is highly suitable prey • Could contribute to SCA control in wetter regions Coccinellidae: Scymnus sp. (no common name)

• Several small species, all with waxy larvae • Not very voracious, but able to forage on ant-tended aphids • Widely distributed across all North America • Not very abundant in arid regions of the High Plains • Will not contribute much to SCA control Chrysopidae: Chrysoperla carnea (green lacewing)

• An important aphid predator in cereal crops throughout North America • Preys on many soft bodied • Strong intraguild predator • Lab studies show SCA is suitable prey, Although not as good as greenbug • Will be a key player in SCA biocontrol throughout the High Plains No. of natural enemy -days, by life stage Cohort 1 Cohort 2 Natural enemies Life stage GB SCA GB SCA

Aphelinus sp. adults 0 4 8 4 mummies 22 41 771 319

Chamaemyiidae larvae 0 24 0 0 Chrysoperla carnea adults 3 12 10 34 eggs 194 609 204 401 larvae 3 19 35 97

Coccinellidae adults 0 3 58 64 egg masses 0 8 2 97 larvae 0 77 2 24

Erythraeus sp. (mite) nymphs 12 5 0 0 Hemerobiidae adults 0 0 0 1 eggs 0 181 0 0

C. carnea was the only dominant species equally present in both cohorts Chrysopidae: Ceraeochrysa sp. (trash bug)

• Most trash-carrying lacewings are arboreal and subtropical or tropical • Important in controlling aphids and psyllids in citrus • Not likely to contribute much to SCA biocontrol Hemerobiidae: Hemerobius sp. (brown lacewing)

• Most brown lacewings are primarily arboreal • Larvae have very cryptic behavior • Eggs are NOT laid on stalks • Not likely to contribute much to SCA biocontrol although recruitment has been observed near trees Syrphidae

• Highly specialized aphid predators • Hover flies use both olfactory and visual cues to find aphids • Often the first predators to oviposit on aphid colonies (while they are small) • Adults require flowers sources of POLLEN and NECTAR • Impact is limited in large-scale monocultures with aggressive weed control Pseudodorus clavatus

• A common subtropical species • Larvae are bristled, almost transparent, variable in color Syrphidae: obliqua

• Widely distributed in North America • Contributes to control of citrus psyllids • Larvae are smooth, lime green, with two longitudinal white stripes Allograpta obliqua and M. sacchari No. of natural enemy arthropod-days, by life stage

Cohort 1 Cohort 2 Life stage GB SCA GB SCA

Lysiphlebus sp. adults 2 5 0 0 mummies 47 0 771 0

Orius insidiosus adults 0 0 39 11 nymphs 0 0 104 22

Syrphidae adults 5 9 0 0 eggs 1308 1626 13 37 larvae 631 1278 33 60 pupae 0 5 0 1 Conclusion: There were greater differences between cohorts than between aphid species Syrphidae: Other spp.

Helophilus fasciatus Syrphus opinator (female) (male)

Larva of Syrphus sp.

Various large, voracious species, widely distributed in North America Aphelinidae: Aphelinus spp.

• Aphid specialists • Small, slow-moving wasps kill aphids by host-feeding and parasitism • Only small instar aphids are attacked • Synovigenic, low fecundity, but long-lived (able to resorb eggs) • Can be important against certain aphid species (e.g. wooly apple aphid) • Not likely to contribute much to SCA control • BUT – unaffected by aphid secondary symbionts that protect against Braconids Braconidae: Lysiphlebus testaceipes

• Tribe Aphidiinae: all aphid specialists, but L. testaceipes has broad host range • Most significant parasitoid of cereal aphids on the High Plains • Can attack 1st-4th instar aphids, 2nd instars preferred • Moderately proovigenic, high fecundity, but short-lived • Does not overwinter north of OK / KS border on the High Plains • Could be significant factor in SCA control in overwintering areas • BUT – some SCA clones are infected with secondary symbionts Hamiltonella defensa, that protect them against parasitism DNA tests revealed our clone of M. sacchari was infected with Hamiltonella defensa, a secondary endosymbiont of aphids

Hamiltonella defensa is known to protect various aphid species from parasitism by braconid (Aphidiinae) parasitoids

Laboratory trials suggested ca. 100% protection from L. testacipes

How widespread are H. defensa infections in SCA populations?

Infections could affect levels of biocontrol obtained in overwintering sites in the south

Are there physiological costs of infection ? What is the heritability of the symbiont ? What is the frequency of transmission ? Chamaemyiidae: sp. (aphid flies)

• Feed on aphids and scale insects • Prefer edge habitats • Not strong fliers Anthocoridae: Orius insidiosus (insidious flower bug)

• Generalist, omnivorus predators of small soft-bodied insects • Eggs laid into plant stems, nymphs consume plant tissues + prey • Feed readily on aphids, but prefer thrips • Lab studies reveal SCA is suitable prey for O. insidiosus, if not optimal • O. insidiosus seems to be abundant in Sorghum fields • Could contribute significant SCA – has been significant against soybean aphid No. of natural enemy arthropod-days, by life stage

Cohort 1 Cohort 2 Life stage GB SCA GB SCA

Lysiphlebus sp. adults 2 5 0 0 mummies 47 0 771 0

Orius insidiosus adults 0 0 39 11 nymphs 0 0 104 22

Syrphidae adults 5 9 0 0 eggs 1308 1626 13 37 larvae 631 1278 33 60 pupae 0 5 0 1 Conclusion: There were greater differences between cohorts than between aphid species Verticillium (Lecanicillium) (entomopathogens)

Whiteflies killed by V. lecanii Aphids killed by V. lecanii

• Requires high humidity and prolonged periods of leaf wetness to produce epizootics • Require high aphid populations to spread • Can result in rapid collapse of aphid colonies under suitable conditions • Most of the High plains is far too dry for aphid entomopathogens