United States 

Department of 

Agriculture

Marketing and 

Regulatory

Programs

Animal and 

Plant Health 

Inspection 

Service

Field Release of Aphelinus

rhamni (Hymenoptera: 

Aphelinidae) for Biological 

Control of the Soybean 

Aphid, Aphis glycines

(Hemiptera: Aphididae), in 

the Continental United 

States

Environmental Assessment,

August 2013
Field Release of Aphelinus rhamni 

(Hymenoptera: Aphelinidae) for 

Biological Control of the Soybean 

Aphid, Aphis glycines (Hemiptera: 

Aphididae), in the Continental United 

States

Environmental Assessment, 

August 2013

Agency Contact: 

Shirley Wager-Page, Ph.D.

Pest Permitting

Plant Protection and Quarantine

Animal and Plant Health Inspection Service

U.S. Department of Agriculture

4700 River Road, Unit 133

Riverdale, MD 20737–1236

The U.S. Department of Agriculture (USDA) prohibits discrimination in all 

its programs and activities on the basis of race, color, national origin, sex, 

religion, age, disability, political beliefs, sexual orientation, and marital or 

family status. (Not all prohibited bases apply to all programs.) Persons 

with disabilities who require alternative means for communication of 

program information (Braille, large print, audiotape, etc.) should contact 

USDA’s TARGET Center at (202) 720–2600 (voice and TDD).

To file a complaint of discrimination, write USDA, Director, Office of Civil 

Rights, Room 326–W, Whitten Building, 1400 Independence Avenue, SW, 

Washington, DC 20250–9410 or call (202) 720–5964 (voice and TDD). 

USDA is an equal opportunity provider and employer. 

Mention of companies or commercial products in this report does not imply 

recommendation or endorsement by the U.S. Department of Agriculture 

(USDA) over others not mentioned. USDA neither guarantees or warrants 

the standard of any product mentioned. Product names are mentioned 

solely to report factually on available data and to provide specific information.

This publication reports research involving pesticides. All uses of pesticides

must be registered by appropriate State and/or Federal agencies before they 

can be recommended.

CAUTION: Pesticides can be injurious to humans, domestic animals, 

desirable plants, and fish or other wildlife–if they are not handled or applied 

properly. Use all pesticides selectively and carefully. Follow recommended 

practices for the disposal of surplus pesticides and pesticide containers.
Table of Contents

I. Purpose and Need for the Proposed Action............................ 1

II. Alternatives................................................................................ 2

III. Affected Environment.............................................................. 5

IV. Environmental Consequences ............................................... 7

V. Other Issues............................................................................ 12

 

VI. Agencies, Organizations, and Individuals Consulted ........ 13

 

VII. References ............................................................................ 15

Appendix A .................................................................................. 23

Appendix B .................................................................................. 25
1

I. Purpose and Need for the Proposed 

Action

The U.S. Department of Agriculture (USDA), Animal and Plant Health 

Inspection Service (APHIS), Plant Protection and Quarantine (PPQ), Pest 

Permitting Branch is proposing to issue permits for release of the insect

Aphelinus rhamni (Hymenoptera: Aphelinidae). This organism would be 

used by the applicant for biological control of soybean aphid, Aphis 

glycines (Hemiptera: Aphididae), in the continental United States. Before 

issuing permits for release of Aphelinus rhamni, APHIS–PPQ needs to

analyze the potential impacts of the release of this organism into the 

continental United States.

This environmental assessment1(EA) was prepared to be consistent with 

USDA–APHIS' National Environmental Policy Act of 1969 (NEPA) 

implementing procedures (Title 7 of the Code of Federal Regulations 

(CFR), part 372). It examines the potential effects on the quality of the 

human environment that may be associated with the release of the 

parasitoid wasp, A. rhamni, to control soybean aphid in the continental 

United States. A parasitoid is an insect whose immature stages (larvae and 

pupae) live as parasites that eventually kill their hosts (typically other 

insects). This EA considers a “no action” alternative and the potential 

effects of the proposed action.

The applicant’s purpose for releasing A. rhamni is to reduce the severity of 

damage to soybean (Glycine max) from infestations of soybean aphid in 

the continental United States. In 2000, the soybean aphid (native to Asia), 

was found in North America, and is now a major soybean pest infesting 42 

million acres in 2003 which resulted in decreased soybean yields and 

greatly increased control costs (Ragsdale et al., 2011; Landis et al., 2008;

Song and Swinton, 2009). The soybean aphid invaded most soybean 

production regions in North America, including 21 states and three 

Canadian provinces since originally reported in North America in 2000 

(Ragsdale et al., 2004).

The applicant identified several purposes for releasing this particular 

insect species for biological control of soybean aphid. First, impacts to

non-target species are expected to be low. Second, this parasitic wasp may

exhibit utility as a biological control agent on the soybean aphid’s 

alternate buckthorn host, Rhamnus species. Lastly, the distribution of A. 

rhamni in the United States may differ from the expected distribution of A. 

glycinis, a related biological control agent of soybean aphid recently 

 

1

Regulations implementing the National Environmental Policy Act of 1969 (42 

United States Code 4321 et seq.) provide that an environmental assessment “[shall include brief 

discussions of the need for the proposal, of alternatives as required by section 102(2)(E), of the 

environmental impacts of the proposed action and alternatives, and a listing of agencies and persons 

consulted” (40 CFR § 1508.9). 
2

approved for release in the United States. Deployment of both insect 

species has the potential to provide enhanced control of soybean aphid 

over a broader area in the United States than A. glycinis alone. These 

parasitic wasps are insects whose immature stages (larvae and pupae) live 

as parasites that eventually kill their hosts (typically other insects).

Most of the existing soybean aphid management options (discussed 

below) are expensive, temporary, and/or include non-target impacts. For 

these reasons, there is a need to identify and release a complement of

effective, host-specific biological control organisms against soybean aphid

in the continental United States. 

II. Alternatives

This section will explain the two alternatives available to APHIS–PPQ: no 

action (no issuance of permits) and issuance of permits for environmental 

release of A. rhamni in the continental United States. Although APHIS’ 

alternatives are limited to a decision of whether to issue permits for release 

of A. rhamni, we describe other methods currently used to control soybean 

aphid by soybean producers in the United States. Use of these control 

methods is not an APHIS decision, and their use is likely to continue 

whether or not APHIS-PPQ issued permits for environmental release of A. 

rhamni. 

APHIS–PPQ considered a third alternative but will not analyze it further. 

Under this third alternative, APHIS–PPQ would issue permits for the field 

release of A. rhamni. The permits, however, would contain special 

provisions or requirements concerning release procedures or mitigating 

measures, such as limited releases of A. rhamni in the United States. There 

are no issues raised indicating that special provisions or requirements are 

necessary.

A. No Action 

Under the no action alternative, APHIS–PPQ would not issue permits for 

the field release of A. rhamni for the control of soybean aphid — the 

release of this biological control agent would not occur, and current 

methods to control soybean aphid in the United States will continue. Use 

of these methods is likely to continue even if APHIS–PPQ issues permits

for release of A. rhamni. Presently, control of soybean aphid in the United 

States is limited to chemical control, plant resistance, and biological

control methods.

Insecticide treatments are the most effective method to manage soybean 

aphids in North America. Foliar sprays of insecticides provide temporary

suppression (7 to 14 days) of soybean aphid populations. Insecticides 

1. Chemical 

Control
3

including esfenvalerate, dimethoate, chlorpyrifos, zeta-cypermethrin, 

methyl parathion, permethrin, and lambda cyhalothrin are or have been 

labeled for foliar application against soybean aphid (Ostlie, 2002). 

Soybean seed treatments using the neonicotinoid insecticides imidacloprid 

and thiamethoxam for systemic control of soybean aphids also can be used 

(Pedersen and Lang, 2006; Magalhaes et al., 2009).

Aphid-resistant soybean plants were bred to support reduced aphid 

populations. Host plant resistance works by inhibiting aphid growth and 

development and increasing plant tolerance to aphid feeding.

 

Aphelinus certus is a parasitoid native to Asia, accidentally introduced into 

the United States when the soybean aphid invaded (Heimpel et al., 2010).

A. certus has a broad host range (Heimpel et al., 2010; Frewin et al., 

2010), and was not considered for purposeful introduction against soybean 

aphid. In the long term, introduction of another parasitoid is unlikely to 

affect the abundance of A. certus because these insects coexist in Asia. 

Another Asian parasitoid, Binodoxys communis (Hymenoptera: 

Braconidae), was released in the United States beginning in 2007; 

unfortunately, it did not establish in the environment (Ragsdale et al., 

2011). In 2002, a previously introduced strain of the European parasitoid 

Aphelinus atriplicis was released against soybean aphid. This strain was

first released in the western United States against the Russian wheat aphid 

(Hopper et al., 1998; Prokrym, 1998; Heraty et al., 2007), but it also 

attacks the soybean aphid (Wu et al., 2004). Although this strain of 

Aphelinus atriplicis was released in nine Minnesota sites in 2002 (Heimpel 

et al., 2004), it was not recovered since that time.

Most recently, APHIS–PPQ approved the parasitoid Aphelinus glycinis for 

environmental release into the United States (Hopper, 2010; USDAAPHIS, 2012). This related species originated from Xiyuan, Liaoning 

Province, Peoples Republic of China. The climate in this area closely 

matches the climate in the northern Midwest United States where soybean 

aphid is a major pest. It is expected that A. glycinis will become limited to 

this region, but may extend its range into Ontario and Quebec provinces in 

Canada. Establishment is expected to occur primarily in soybean fields

infested with soybean aphid during the growing season.

 

B. Issue Permits for Environmental Release of 

A. rhamni.

Under this alternative, APHIS–PPQ would issue permits upon request and 

after evaluation of each application for the field release of A. rhamni for 

the control of soybean aphid in the continental United States. These

permits would contain no special provisions or requirements concerning 

release procedures or mitigating measures.

3. Biological 

Control

2. Host Plant 

Resistance
4

Insect Taxonomy

Order: Hymenoptera

Family: Aphelinidae 

Genus: Aphelinus

Species: rhamni Woolley and Hopper

Common name: none

The species description of A. rhamni was published in 2012 (Hopper et al., 

2012). Voucher specimens of A. rhamni are held at three locations. These 

include (1) the Beneficial Insect Introductions Research Unit, Agricultural 

Research Service (ARS), United States Department of Agriculture,

Newark, Delaware, (2) Texas A&M University, Department of 

Entomology, and (3) the Smithsonian in the Systematic Entomology

Laboratory, USDA−ARS. 

Aphelinus species are tiny (about 1 millimeter (mm) in length), stingless 

parasitic wasps. The immature stages develop as internal parasitoids of 

arthropods where, in this case, feeding of the wasp larva inside the host 

aphid eventually kills the host aphid. Many species of Aphelinus have 

demonstrated their importance in the biological control of aphids

(Hemiptera: Aphididae).

Aphelinus rhamni females prefer second to fourth instar (an immature 

developmental stage) aphid hosts for oviposition (egg laying), but will lay

eggs in all stages, including winged adults. Females use an egg laying 

organ called an ovipositor to insert an egg into the aphid. The inserted egg 

hatches and the wasp larva feeds on the internal organs of the aphid host.

At 20oC, the wasps develop from egg to pupa in about 14 days; third instar 

wasps kill their hosts leaving intact the aphid host external skeleton 

(exoskeleton) hardened and black, in a process called mummification.

Adult A. rhamni wasps emerge from the mummified aphid about one week 

after pupation by chewing a hole through the host exoskeleton to escape. 

Adult wasps eat plant nectar and honeydew (a sugary liquid secreted by

aphids and other sap-feeding insects). Adult females also feed on aphids to 

obtain nutrients for egg production by piercing or “stinging” the aphids 

with their ovipositor and drinking the hemolymph (insect blood) from the 

wound, killing about two aphids per day by such feeding. Females emerge 

as adults with five to 15 mature eggs, but produce more eggs throughout 

their lives, maturing about 10 eggs per day. In the laboratory, adult wasps 

live for two to three weeks, but they are unlikely to survive this long in the 

field (Hopper, 2011).

Aphelinus species are weak fliers, searching primarily by walking

(Fauvergue et al., 1995; Mason and Hopper, 1997). Another related 

parasitoid, Aphelinus asychis, dispersed an average of 13 feet in one 

generation and 26 feet in three generations in fields with abundant hosts

1. Aphelinus 

rhamni

Taxonomic 

Information 

2. Description 

and 

Biology of

Aphelinis

rhamni
5

(Fauvergue and Hopper, 2009). Insects would have to disperse much 

further at the end of the growing season to track their hosts.

Aphelinus rhamni was collected from parasitized soybean aphids on 

Rhamnus species in 2005 near Daxing (Beijing, Hebei Province) Peoples 

Republic of China, and is not known to occur elsewhere (Hopper et al., 

2012). The present distribution of soybean aphid in the United States 

matched fairly well with a climate-based expected distribution of A. 

rhamni (Dymex Simulator Application software, version 2.01.025, (c) 

CSIRO, 2004). It is expected that A. rhamni may not establish in the full 

southern range of the soybean aphid because this pest is found further 

south than the climate match for Beijing. Aphelinus rhamni is expected to 

establish primarily in the northern half of the United States east of the 

Rocky Mountains (Hopper, 2011).

In the laboratory, an individual female A. rhamni wasp parasitizes or kills 

by host feeding over 200 aphids during a lifetime of three weeks, but long 

lifetimes in the field are unlikely. If females lived one week in the field,

each is expected to parasitize and host feed on 70 aphids, if aphids are

sufficiently abundant (Hopper, 2011). 

III. Affected Environment

A. Soybean Aphid

The soybean aphid is a host alternating species, which means it must 

disperse between two different types of host plants between summer and 

winter. Females reproduce asexually on soybean from June to September, 

producing winged and wingless forms. In September, winged males and 

parthenogenetic (a form of reproduction in which an unfertilized egg 

develops into a new individual) females migrate to their primary host 

plants, Rhamnus species, and the migratory females bear sexual, flightless 

females, which mate with the migratory males and lay overwintering eggs. 

In the spring, parthenogenetic females hatch from these eggs, and several 

generations of females reproduce asexually on Rhamnus species before 

winged aphids move to soybean plants. Although soybean aphids are weak 

fliers, the rapid rate of spread of soybean aphid indicates a high rate of 

windborn dispersal. In the laboratory, soybean aphid has a high rate of 

population increase at 25oC, with a steep decline to a negative rate when 

temperatures are higher than 30oC (McCornack et al., 2004). This can 

explain why it has not moved further south in the United States where 

temperatures are warmer. At 25oC, females can produce 73 offspring

during their lifetime, with a generation time of 10 days. The combination 

of high dispersal rate and high reproductive rate mean that soybean aphid 

can rapidly reach damaging levels over wide regions, if not properly 

managed (Hopper, 2011).

3. Geographic

Range of

Aphelinis

rhamni

4. Impact of 

Aphelinus

rhamni

on Soybean 

Aphid
6

B. Areas Affected by Soybean Aphid

The soybean aphid is native to East Asia, found in eastern Russia, China, 

Japan, and Southeast Asia (Vietnam, Thailand, Indonesia, Malaysia, and 

the Philippines). There are reports in Kenya, and it invaded Australia in 

2000. 

In North America, it is currently known from Ontario and Quebec in 

Canada, and from the following 29 U.S. states: Arkansas, Connecticut, 

Delaware, Georgia, Indiana, Iowa, Illinois, Kansas, Kentucky, Louisiana, 

Maine, Maryland, Massachusetts, Michigan, Minnesota, Mississippi, 

Missouri, Nebraska, New Jersey, New York, North Dakota, Ohio, 

Oklahoma, Pennsylvania, South Dakota, Tennessee, Virginia, West 

Virginia, and Wisconsin (Ragsdale et al., 2011). 

Soybean (Glycine max) is the summer host of soybean aphid while various 

buckthorn species (Rhamnus species) are the winter hosts. Several native 

and a few introduced species of Rhamnus occur in the United States. 

C. Insects Related to Soybean Aphid and A. rhamni

in the United States

Information regarding insects taxonomically related to soybean aphid is 

included because closely related insect species have the greatest potential 

for attack by A. rhamni. 

Of the 497 species of Aphis with distributions listed in Blackman and 

Eastop (2006), 119 are reported from North America. Of these species 

found in North America, 33 are widely distributed throughout the world, 

and many of these are invasive exotic pests. Only 86 species of Aphis were 

described from collections in North America, and consequently may be 

considered native species. Fortunately, most native Aphis species are not 

closely related to soybean aphid (Aphis glycines). The soybean aphid is 

closely related to the cotton aphid, Aphis gossypii, which is also native to 

Asia and a major agricultural pest, and to the buckthorn-potato aphid, 

Aphis nasturtii, which shares its overwintering host (Rhamnus species).

Aphis nasturtii is a pest of potatoes in North America, and believed to be 

native to Asia (Hopper, 2011). 

Thirty-one species of Aphelinus are reported from North America, 

however, only about half of these species (14) were described from North 

America (listed in Appendix A with their authors and species complex 

membership, as well as reported distributions and hosts). These 14 

Aphelinus species are reported exclusively or almost exclusively from 

North America, and likely are native. 

The remaining Aphelinus species reported from North America were 

2. Present 

Distribution in 

North America

1. Native and 

Worldwide 

Distribution

3. Soybean 

Aphid

Hosts

1. Insects 

Related 

to 

Soybean 

Aphid

2. Insects 

Related to 

Aphelinus 

rhamni
7

described elsewhere, are reported from one to several other continents, and 

therefore are unlikely to be native to North America. Several have been 

introduced for biological control of pest aphids (Hopper et al., 1998; 

Jackson et al., 1971; van den Bosch et al., 1959). Three native Aphelinus

species were reported from Aphis species, A. marlatti, A. nigritis, and A. 

semiflavus, but only A. semiflavus parasitizes a species closely related to 

the soybean aphid, being reported from the cotton aphid in the Midwestern 

United States. The native parasitoid species appear unlikely to switch to 

attack the soybean aphid, because these types of switches have not been 

observed (Lin and Ives, 2003; Rutledge et al., 2004; Kaiser et al., 2007; 

Costamagna and Landis, 2007; Noma and Brewer, 2008; Noma et al., 

2010). Five native Aphelinus species (A. lapisligni, A. mali, A. prociphili, 

A. sanborniae, and A. siphonophorae) are in the mali complex to which A. 

rhamni belongs. These species are more closely related to A. rhamni than 

other native Aphelinus species, yet their hosts are different from those 

parasitized by A. rhamni (see Appendix A). Therefore, A. rhamni is not 

expected to compete with native species of Aphelinus.

Climate projections suggest both A. rhamni and A. glycinis are likely to 

establish in the northern Midwest of the United States (Hopper, 2010; 

Hopper, 2011; Hopper, 2012). Establishment of A. glycinis may

preferentially occur on the soybean host, while A. rhamni is expected to 

establish on the buckthorn hosts. 

IV. Environmental Consequences 

A. No Action

a. Effect of soybean aphid on host plants

Soybean aphids suck sap from plants. When aphid infestations are large,

infested leaves are wilted or curled. Direct feeding damage from aphids 

may include plant stunting, reduced pod and seed counts, and yellowing of 

leaves. Soybean aphids also transmit plant viruses such as alfalfa mosaic, 

soybean mosaic, and bean yellow mosaic; these diseases cause yield 

reduction in soybeans. 

For soybean growers in the north central United States, the soybean aphid 

is the first insect pest to consistently cause important losses over wide 

areas (Ragsdale et al., 2004), with yield decreases of up to 40 percent

(Ragsdale et al., 2007). Invasion of the soybean aphid led to dramatic 

changes in the pest management practices of soybean producers. In 2000, 

less than one-tenth of one percent of soybeans in the north central states 

were treated with insecticides. By 2006, over 13 percent of soybeans in 

these states were treated with insecticides. This indicates soybean aphid 

was responsible for a 130-fold increase in the use of insecticides 

(Ragsdale et al., 2011). Control of the soybean aphid currently relies on 

1. Impact of 

Soybean 

Aphid on the 

Environment
8

insecticide use, and millions of acres of soybeans have been sprayed since 

the invasion of this pest. This is a major disruption in the 70 million acres 

of soybean production within the country. 

The continued use of chemical control, plant resistance, and biological 

control at current levels would result if the “no action” alternative is 

chosen, and may continue even if permits are issued for environmental 

release of A. rhamni.

a. Chemical Control

Foliar applications may not sufficiently control soybean aphids and 

prevent yield loss, especially if large quantities of soybean aphids are 

surviving on lower leaves. Foliar sprays may pose a threat to bees and 

aphid natural enemies, such as lady beetle larvae and predatory bugs. In a 

screening assay, both λ-cyhalothrin and dimethoate were harmful to A. 

certus (Frewin et al., 2012). This suggests chemical pest controls may

limit the effectiveness of various parasitoid wasps released as potential 

biocontrol organisms.

Seed treatments of systemic insecticides such as imidacloprid do not last 

the entire growing season. In addition, seed treatment insecticides are 

applied at the beginning of the growing season before it is known if 

treatment for soybean aphid is even necessary. This creates a financial loss 

to growers if aphid populations would not have been high enough to 

trigger economic damage requiring pest treatments. 

b. Plant Resistance

Although plant resistance inhibits aphid growth and development and 

increases plant tolerance to aphid feeding, plant resistance in certain cases has 

been overcome by soybean aphids.

c. Biological Control

Two biological control organisms, Aphelinus atriplicis and Binodoxys 

communis were released against soybean aphid, however, neither

organism established in the environment and provides control of the

soybean aphid. The related A. glycinis recently was approved for 

environmental release in the continental United States (Hopper, 2010; 

USDA-APHIS, 2012). This organism is expected to establish primarily on 

the soybean host. 

These impacts from the use of other control methods may have 

environmental consequences even with the implementation of the 

biological control alternative, depending on the efficacy of A. rhamni to 

reduce soybean aphid infestations in the continental United States.

2. Impact from 

the Use of 

Other Control

Methods
9

B. Issue Permits for Environmental Release of A. 

rhamni

a. Scientific Literature

Published literature on the host range of A. rhamni includes only the 

information in the species description. In the field, Aphis glycines is the 

only known host, but in laboratory experiments, Aphelinus rhamni

parasitizes Aphis glycines, closely related species in this genus, and rarely 

Rhopalosiphum padi L. and Schizaphis graminum (Hopper et al., 2012). 

Other species in the mali complex tend to have narrow host ranges; a 

notable exception is A. mali itself which reportedly has a broad host range.

On the other hand, literature reports of broad host ranges may reflect

confounding effects from cryptic species within this genus (Heraty et al., 

2007). 

b. Host Specificity Testing

Host specificity testing of A. rhamni in containment examined three ways 

that aphids were killed: oviposition leading to mummification, stinging the 

aphid to death without mummification, and host feeding (Hopper, 2011). 

Parasitism of 13 aphid species in five genera in two tribes on 10 plant 

species in nine families was measured (Table 1). These aphids covered a 

range of closely related aphids reported as hosts of the A. mali complex 

(see Appendix A), of which A. rhamni is a member. Furthermore, the 

aphid-plant combinations provided contrasts of aphids in the same versus 

different genera, on the same versus different plants (see Appendix B). 

Based on the aphid distributions in Blackman and Eastop (2006), most of 

these aphid species occur within the native geographic range of A. rhamni, 

so these aphids and this parasitoid are likely to have been in contact for at 

least 10,000 years. The exceptions are Diuraphis noxia, which is native to 

central to western Asia and Europe, and Aphis oestlundi and Aphis 

monardae, which are native to North America.

1. Impact of 

A. rhamni on 

Non-target 

Insects
10

Table 1. Aphid and host plant species used to test Aphelinus

rhamni host specificity.

Aphid species Plant species Plant family

Aphis glycines Glycine max Fabaceae

Aphis gossypii Gossypium hirsutum Malvaceae

Aphis gossypii Asclepias syriaca Apocynaceae

Aphis monardae Monarda fistulosa Laminacea

Aphis oestlundi Oenothera biennis Onagraceae

Aphis nerii Asclepias syriaca Apocynaceae

Aphis asclepiadis Asclepias syriaca Apocynaceae

Aphis craccivora Vigna unguiculata Fabaceae

Aphis rumicis Rumex altissimus Polygonaceae

Rhopalosiphum maidis Hordeum vulgare Poaceae

Rhopalosiphum padi Hordeum vulgare Poaceae

Schizaphis graminum Hordeum vulgare Poaceae

Diuraphis noxia Hordeum vulgare Poaceae

Myzus persicae Raphanus sativus Brassicaceae

Tests of parasitism in 24-hour exposures of aphids to A. rhamni consisted 

of A. rhamni females being placed in cages with 100 aphids of a single 

species on plant foliage. In this study, A. rhamni rarely or never 

parasitized aphids outside of the genus Aphis. Within the genus Aphis, A. 

rhamni produced mummified aphids on species closely related to the 

target aphid, A. glycines (e.g., A. gossypii, A. monardae, and A. oestlundi),

but not on more distantly related Aphis species. 

Direct observation of the behavior of A. rhamni and aphids determined

host use patterns. Continuous microscopic observation of each female 

parasitoid (and the aphids to which she was exposed) for 25 minutes under 

magnification showed A. glycines is the most suitable species for A. 

rhamni development, by producing an adult parasitoid per oviposition. In 

most other species in the genus Aphis, there were less than half as many A. 

rhamni adults per oviposition produced. 

In summary, laboratory experiments showed oviposition and host feeding 

by A. rhamni was restricted almost completely to species in the genus 

Aphis closely related to the target. Furthermore, parasitoid stinging that 

did not lead to mummification or host feeding did not increase mortality of 

any aphid species. Handling times of aphids by A. rhamni were long, so 

ant-fended native aphids, such as A. monardae and A. oestlundi, should 

not be at risk in the field. The target pest, soybean aphid, was the most 

suitable aphid species for A. rhamni development (Hopper, 2011). See 

Appendix B for details on the host specificity study.

Additional studies determined if A. rhamni might be likely to shift to nontarget aphid hosts under certain conditions. In these studies, it was found 
11

that stresses decreasing the length of life of A. rhamni did not increase its 

acceptance of low quality aphid host species. Specificity appears to be 

stable, and low-quality, non-target species should not have increased risk 

of attack when A. rhamni is stressed from starvation or age.

Once a biological control agent such as A. rhamni is released into the 

environment and becomes established, there is a possibility it could move 

from the target insect (soybean aphid) to attack nontarget insects, such as 

native aphid species. Native species that are closely related to the target 

species are the most likely to be attacked (Louda et al., 2003). If other 

aphid species were to be attacked by A. rhamni, the resulting effects could 

be environmental impacts that may not be easily reversed. Biological 

control agents such as A. rhamni generally spread without intervention by

man. In principle, therefore, release of these parasitoids at even one site 

should be considered equivalent to release over the entire area in which 

potential hosts occur and in which the climate is suitable for reproduction 

and survival. 

In addition, these agents may not be successful in reducing soybean aphid

populations in the continental United States. Approximately 12 percent of 

all parasitoid introductions have led to significant sustained control of the 

target pests, but the majority of introductions have failed to provide 

control of the pest (Greathead and Greathead, 1992) either because 

introduction did not lead to establishment or establishment did not lead to 

control (Lane et al., 1999). 

Actual impacts on soybean aphid populations by A. rhamni will not be 

known until after release and establishment occurs. Actual impacts on the 

establishment of A. glycinis, including potential competitive interactions

will not be known until after release and establishment of A. rhamni

occurs. The environmental consequences discussed under the no action

alternative may occur even with the implementation of the action

alternative, depending on the efficacy of A. rhamni to reduce soybean 

aphid in the continental United States.

“Cumulative impacts are defined as the impacts on the environment which 

results from the incremental impact of the action when added to other past, 

present and reasonably foreseeable future actions regardless of what 

agencies or person undertakes such other actions” (40 CFR 1508.7).

To date, other soybean aphid biological control organisms released in the 

United States have not successfully established. Therefore, competitive 

interactions would not occur among any organisms previously released. 

The release of A. glycinis is not expected to produce competitive 

interactions with A. rhamni because habitat partitioning of the two 

parasitoids between soybean aphids on the two alternate plant hosts

(soybean and Rhamnus species) is anticipated (K. Hopper, pers. comm.).

2. Uncertainties 

Regarding the 

Environmental 

Release of 

Aphelinus

rhamni.

 Cumulative 

Impacts

3. Cumulative 

Impacts
12

The two species also have different predicted geographical distributions 

based on climate matching, with the distribution of A. glycinis extending 

further north and A. rhamni further south (Hopper, 2010). As discussed 

previously, A. rhamni is not expected to compete with native species of

Aphelinus. 

The non-native parasitoid Aphelinus certus Yasnosh accidentally 

established in North America (Heimpel et al., 2010, Frewin et al., 2010). It 

was found over a wide geographic range in the eastern United States and 

Canada since 2005. In laboratory experiments, it has a host range of at 

least four genera in two subfamilies of aphids, and on at least four host 

plant species (Heimpel et al., 2010). The abundance of A. certus in the 

United States is unlikely to be affected by introduction of A. rhamni

because this parasitoid’s host range is narrower than for A. certus.

Aphelinus certus might interfere with establishment of A. rhamni, but the 

coexistence of these parasitoid species in Asia suggests any interference is 

likely to be short-lived. 

Release of A. rhamni is not expected to have any negative cumulative 

impacts in the continental United States because of its host specificity to 

soybean aphids. Effective biological control of soybean aphid will have 

beneficial effects for soybean growers in the United States, may result in a 

long-term, non-damaging method to assist in the control of soybean aphid, 

and may reduce the use of insecticides on soybean.

Section 7 of the Endangered Species Act (ESA) and ESA’s implementing 

regulations require Federal agencies to ensure that their actions are not 

likely to jeopardize the continued existence of federally listed threatened 

and endangered species, or result in the destruction or adverse 

modification of critical habitat.

APHIS has determined that, based on the host specificity of A. rhamni, 

there will be no effect on any listed insect species or designated critical 

habitat in the continental United States. In host specificity testing, A. 

rhamni only attacked species of aphids. There are no federally listed 

threatened or endangered insects belong to the aphid family, Aphididae

(USFWS, 2012). There are no federally listed species are known to 

depend on or utilize soybean aphid. 

V. Other Issues

Consistent with Executive Order (EO) 12898, “Federal Actions to Address 

Environmental Justice in Minority Populations and Low-income 

Populations,” APHIS considered the potential for disproportionately high 

and adverse human health or environmental effects on any minority 

populations and low-income populations. There are no adverse 

environmental or human health effects anticipated from the field release of 

4. Endangered 

Species Act
13

A. rhamni and its release will not have disproportionate adverse effects to 

any minority or low-income populations. 

Consistent with EO 13045, “Protection of Children From Environmental 

Health Risks and Safety Risks,” APHIS considered the potential for 

disproportionately high and adverse environmental health and safety risks 

to children. There are no circumstances that would trigger the need for 

special environmental reviews involved in implementing the preferred 

alternative. Therefore, there are no disproportionate effects on children 

anticipated because of the field release of A. rhamni.

EO 13175, “Consultation and Coordination with Indian Tribal 

Governments”, was issued to ensure that there would be “meaningful 

consultation and collaboration with tribal officials in the development of 

Federal policies that have tribal implications....” Consistent with EO 

13175, APHIS sent letters of notification and requests for comment and 

consultation on the proposed action to tribes in areas where the soybean 

aphid occurs. APHIS will continue to consult and collaborate with Indian 

tribal officials to ensure that they are well-informed and represented in 

policy and program decisions that may impact their agricultural interests, 

in accordance with EO 13175.

VI. Agencies, Organizations, and 

Individuals Consulted

This EA was prepared and reviewed by APHIS and ARS. The addresses 

of participating APHIS units and any applicable cooperators are provided.

U.S. Department of Agriculture

Animal and Plant Health Inspection Service

Policy and Program Development 

Environmental and Risk Analysis Services

4700 River Road, Unit 149

Riverdale, MD 20737

U.S. Department of Agriculture

Animal and Plant Health Inspection Service

Plant Protection and Quarantine 

Registrations, Identification, Permits, and Plant Safeguarding

4700 River Road, Unit 133

Riverdale, MD 20737

U.S. Department of Agriculture

Agricultural Research Service

Beneficial Insect Introductions Research Unit

501 South Chapel Street
14

Newark, DE 19713
15

VII. References

Archer, T.L., Cate, R.H. and Eikenbary, R.D. 1974. Parasitoids collected 

from greenbugs and corn leaf aphids in Oklahoma in 1972. Annals of the 

Entomological Society of America. 67: 11−14.

Ashmead, W.H. 1888a. Descriptions of some new North American 

Chalcididae. III: Euderinae (Hymenoptera: Chalcidoidea). Canadian 

Entomologist. 20: 101−107.

Ashmead, W.H. 1888b. Descriptions of some unknown parasitic 

Hymenoptera in the collection of the Kansas State Agricultural College, 

received from Prof. E.A. Popenoe. Bulletin of Kansas Agricultural 

Experiment Station, Manhattan. No. 3 (appendix):v.

Becker, G.G. 1918. Notes on the woolly aphis. Bulletin of the Arkansas 

Agricultural Experiment Station. 11: 245−255.

Blackman, R.L. and Eastop, V.F. 2006. Aphids of the world's herbaceous 

plants and shrubs. Volume 2: the aphids. Wiley and Sons, Ltd., West 

Sussex, U.K.

Bruner, L. 1894. Insect enemies of the apple tree and its fruit. Annual 

Report of the Nebraska State Horticultural Society. 2: 154−223.

Bueno, R., Jr. and Stone, J.D. 1983. Phenology of a parasite of the 

blackmargined aphid in West Texas. Southwestern Entomologist. 8:

73−79.

Carver, M. 1980. A new species of Aphelinus Dalman (Hymenoptera: 

Chalcidoidea: Encyrtidae). Proceedings of the Entomological Society of 

Washington. 82: 536−540.

Costamagna, A.C. and Landis, D.A. 2007. Predators exert top-down 

control of soybean aphid across a gradient of agricultural management 

systems. Ecological Applications. 17: 639−639.

Cresson, E.T. 1862. Catalogue of the described species of North American 

Hymenoptera. (Continued.) Proceedings of the Entomological Society of 

Philadelphia. 1: 227−238.

Delong, D.M., and Jones, M.P. 1926. Control measures for the Houghton 

gooseberry aphis with special reference to plant resistance. Journal of 

Economic Entomology. 19: 40−43.

Edelson, J.V. and Estes, P.M. 1987. Seasonal abundance and distribution 

of predators and parasites associated with Monelliopsis pecanis Bissell 
16

and Monellia caryella (Fitch) (Homoptera: Aphidae). Journal of 

Entomological Science. 22: 336−347.

Exec. Order No. 13175, 65 Fed. Reg. 67249 (2000).

Exec. Order No. 13045, 62 Fed. Reg. 5137 (1997), amended in EO 12961 

(1995).

Exec. Order No. 12898, 59 Fed. Reg. 7629 (1994).

Fauvergue, X. and Hopper, K.R. 2009. French wasps in the New World: 

experimental biological control introductions reveal a demographic Allee 

effect. Population Ecology. 51: 385−397.

Fauvergue, X., Hopper, K.R. and Antolin, M.F. 1995. Mate finding via a 

trail sex-pheromone by a parasitoid wasp. Proceedings of the National 

Academy of Sciences of the United States of America. 92: 900−904.

Frewin, A.J., Schaafsma, A.W. and Hallett, R.H. 2012. Susceptibility of 

Aphelinus certus to foliar-applied insecticides currently or potentially 

registered for soybean aphid control. Pest Management Science 68(2): 

202-208.

Frewin, A.J., Xue, Y.E., Welsman, J.A., Broadbent, A.B., Schaafsma, 

A.W. and Hallett, R.H. 2010. Development and parasitism by Aphelinus 

certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines

(Hemiptera: Aphididae). Environmental Entomology. 39: 1570−1578.

Gahan, A.B. 1924. Some new parasitic Hymenoptera with notes on several 

described forms. Proceedings of the United States National Museum. 65:

9.

Gillette, C.P. and Taylor, E.P. 1908. A few orchard plant lice. Colorado 

Agricultural Experiment Station Bulletin. 133: 1−48.

Girault, A.A. 1911. A new aphid-infesting Aphelinus which is not black. 

Entomologist. 44: 178.

Girault, A.A. 1916. Descriptions Hymenopterorum Chalcidiocorum 

variorum cum observationibus, ii. Entomological News. 27: 405.

Girault, A.A. 1917. Descriptiones stellarum novarum. Private publication:

1−18.

Greathead, D., and Greathead, A.H. 1992. Biological control of insect 

pests by parasitoids and predators: the BIOCAT database. Biocontrol 

News and Information. 13: 61N−68N.
17

Griswold, G.H. 1926. Notes on some feeding habits of two chalcid 

parasites. Annals of the Entomological Society of America. 19: 331.

Griswold, G.H. 1927. Observations on the biology of a new geranium 

aphid (Macrosiphum cornelli Patch). Journal of Economic Entomology.

20: 91−94.

Haldeman, S.S. 1859. Eriophilus. Proceedings of the Boston Society of 

Natural History. 6: 402−403.

Hartley, E.A. 1922. Some bionomics of Aphelinus semiflavus (Howard) 

chalcid parasite of aphids. Ohio Journal of Science. 22: 209−237.

Heimpel, G.E., Frelich, L.E., Landis, D.A., Hopper, K.R., Hoelmer, K.A., 

Sezen, Z., Asplen, M.K. and Wu, K.M. 2010. European buckthorn and 

Asian soybean aphid as components of an extensive invasional meltdown 

in North America. Biological Invasions. 12: 2913−2931.

Heimpel, G.E., Lee, J.C., Wu, Z.S., Weiser, L., Wackers, F. and Jervis, 

M.A. 2004. Gut sugar analysis in field-caught parasitoids: adapting 

methods originally developed for biting flies. International Journal of Pest 

Management. 50: 193−198.

Heraty, J.M., Woolley, J.B., Hopper, K.R., Hawks, D.L., Kim, J.W. and

Buffington, M. 2007. Molecular phylogenetics and reproductive 

incompatibility in a complex of cryptic species of aphid parasitoids. 

Molecular Phylogenetics and Evolution. 45: 480−493.

Herting, B. 1972. Homoptera. A catalogue of parasites and predators of 

terrestrial arthropods. Section A. Host or Prey/Enemy. Commonwealth 

Agricultural Bureaux, Slough, England.

Hopper, K.R. 2012. Supplement to Petition for the Release of Aphelinus 

rhamni (Hymenoptera: Aphelinidae) for the Biological Control of the 

Soybean Aphid, Aphis glycines (Hemiptera: Aphididae). 14 pp. 

Hopper, K.R. 2011. Petition for the Release of Aphelinus rhamni

(Hymenoptera: Aphelinidae) for the Biological Control of the Soybean 

Aphid, Aphis glycines (Hemiptera: Aphididae). 35 pp.

Hopper, K.R. 2010. Petition for the Release of Aphelinus glycinis

(Hymenoptera: Aphelinidae) for the Biological Control of the Soybean 

Aphid, Aphis glycines (Hemiptera: Aphididae). 32 pp.

Hopper, K., Woolley, J., Hoelmer, K., Wu, K., Qiao, G. and Lee, S. 2012. 

An identification key to species in the mali complex of Aphelinus
18

(Hymenoptera: Chalcidoidea) with descriptions of three new species. 

Journal of Hymenoptera Research 26:73-96.

Hopper, K.R., Coutinot, D., Chen, K., Mercadier, G., Halbert, S.E., 

Kazmer, D.J., Miller, R.H., Pike, K.S. and Tanigoshi, L.K. 1998.

Exploration for natural enemies to control Diuraphis noxia in the United 

States. In: A response model for an introduced pest - The Russian wheat 

aphid, (Quissenbery, S.S. and Peairs, F.B., eds.). pp. 166−182. Thomas 

Say Publications in Entomology: Proceedings. Entomological Society of 

America, Lanham, MD.

Howard, L.O. 1881. Report of the parasites of Coccidae in the collections 

of the U.S. Department of Agriculture Part III. . In: Report of the 

entomologist for 1880, (Comstock, J.H., ed.). pp. 350−372, plates 23,24.

United States Department of Agriculture, Washington.

Howard, L.O. 1895. Revision of the Aphelininae of North America a 

subfamily of hymenopterous parasites of the family Chalcididae. 

Technical Series, Bureau of Entomology, United States Department of 

Agriculture. 1: 25.

Howard, L.O. 1908. Upon the aphis feeding species of Aphelinus. 

Entomological News. 19: 365−367.

Howard, L.O. 1914. Concerning some Aphelininae. Proceedings of the

Entomological Society of Washington. 16: 80 

Howard, L.O. 1917. A new aphis-feeding Aphelinus. Proceedings of the 

Biological Society of Washington. 30: 77.

Jackson, H.B., Rogers, C.E. and Eikenbary, R.D. 1971. Colonization and 

Release of Aphelinus asychis, an imported parasite of greenbug. Journal of 

Economic Entomology. 64: 1435−1438.

Kaiser, M.E., Noma, T., Brewer, M.J., Pike, K.S., Vockeroth, J.R. and

Gaimari, S.D. 2007. Hymenopteran parasitoids and dipteran predators 

found using soybean aphid after its midwestern United States invasion. 

Annals of the Entomological Society of America. 100: 196−205.

Kelly, E.O.G. 1917. The green-bug (Toxoptera graminum Rond.) 

outbreak of 1916. Journal of Economic Entomology. 10: 233–248.

Kuhlmann, U., Schaffner, U., and Mason, P.G. 2005. Selection of nontarget species for host specificity testing of entomophagous biological 

control agents. In: International Symposium on Biological Control of 

Arthropods, September 12–16, 2005. Complied by Hoddle, M.S., United 

States Department of Agriculture, Forest Service, FHTET-2005–08, 
19

Morgantown, WV, USA, 566–583.

Landis, D.A., Gardiner, M.M., van der Werf, W. and Swinton, S.M. 2008. 

Increasing corn for biofuel production reduces biocontrol services in 

agricultural landscapes. Proceedings of the National Academy of Sciences 

of the United States of America. 105: 20552–20557.

Lane, S.D., Mills, N.J., and Getz, W.M. 1999. The effects of parasitoid 

fecundity and host taxon on the biological control of insect pests: the 

relationship between theory and data. Ecological Entomology. 

24:181−190.

Lin, L.A. and Ives, A.R. 2003. The effect of parasitoid host-size 

preference on host population growth rates: an example of Aphidius 

colemani and Aphis glycines. Ecological Entomology. 28: 542–550.

Lohrenz, H.W. 1911. The woolly aphis, Schizoneura lanigera. Journal of 

Economic Entomology. 4: 162–170.

Louda, S.M., Pemberton, R.W., Johnson, M.T., and Follett, P.A. 2003. 

Nontarget effects—the Achilles’ heel of biological control. Retrospective 

analyses to reduce risk associated with biological control introductions. 

Annual Review of Entomology. 48: 365–396.

Magalhaes, L.C., Hunt, T.E., and Siegfried, B.D. 2009. Efficacy of 

neonicotinoid seed treatments to reduce soybean aphid populations under 

field and controlled conditions in Nebraska. J. Econ. Entomol. 102:

187−195.

Mason, P.G. and Hopper, K.R. 1997. Temperature dependence in 

locomotion of the parasitoid Aphelinus asychis (Hymenoptera: 

Aphelinidae) from geographical regions with different climates. 

Environmental Entomology. 26: 1416−1423.

Mizell, R.F., III and Schiffhauer, D.E. 1990. Effects of pesticides on 

pecan aphid predators Chrysoperla rufilabris (Neuroptera: Chrysopidae), 

Hippodamia convergens, Cycloneda sanguinea (L.), Olla v-nigrum

(Coleoptera: Coccinellidae), and Aphelinus perpallidus (Hymenoptera: 

Encyrtidae). Journal of Economic Entomology. 83: 1806−1812.

Noma, T. and Brewer, M. J. 2008. Seasonal abundance of resident 

parasitoids and predatory flies and corresponding soybean aphid densities, 

with comments on classical biological control of soybean aphid in the 

Midwest. Journal of Economic Entomology. 101: 278−287.

Noma, T., Gratton, C., Colunca-Garcia, M., Brewer, M.J., Mueller, E.E., 

Wyckhuys, K.A.G., Heimpel, G.E. and O'Neal, M.E. 2010. Relationship 
20

of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, 

landscape structure, and natural enemies. Environmental Entomology. 39: 

31−41.

Peck, O. 1963. A catalogue of the Nearctic Chalcidoidea (Insecta; 

Hymenoptera). Canadian Entomologist (Supplement). 30: 267.

Pedersen, P. and Lang, B. 2006. Use of insecticide seed treatments for 

managing soybean aphids. Integrated Crop Management. IC-496. 

http://www.ipm.iastate.edu/ipm/icm/2006/1-23/seedtreat.html last 

accessed January 30, 2012. 

Prokrym, D.A. 1998. Biological control of Diuraphis noxia (Homoptera: 

Aphididae): implementation and evaluation of natural enemies. In: A 

response model for an introduced pest - The Russian wheat aphid.

(Quissenberry, S.S. and Peairs, F.B., eds.). pp. 183−208. Entomological 

Society of America, Lanham, MD.

Ragsdale, D.W., Landis, D.A., Brodeur, J., Heimpel, G.E. and Desneux, 

N. 2011. Ecology and management of soybean aphid in North America. 

Annual Review of Entomology. 56: 375–99.

Ragsdale, D.W., McCornack, B P., Venette, R.C., Potter, B.D., Macrae, 

I.V., Hodgson, E.W., O'Neal, M.E., Johnson, K.D., O'Neil, R.J., Difonzo, 

C.D., Hunt, T.E., Glogoza, P.A. and Cullen, E.M. 2007. Economic 

threshold for soybean aphid (Hemiptera : Aphididae). Journal of 

Economic Entomology. 100: 1258−1267.

Ragsdale, D.W., Voegtlin, D.J. and O'Neil, R.J. 2004. Soybean aphid 

biology in North America. Annals of the Entomological Society of 

America. 97: 204−208.

Rogers, C.E., Starks, K.J., Jackson, H.B., Eikenbarry, R. and Starks, K.J. 

1972. Host-parasitoid interaction of Aphis helianthi on sunflowers with 

introduced Aphelinus asychis, Ephedrus plagiator, and Praon gallicum, 

and native Aphelinus nigritus and Lysiphlebus testaceipes. Annals of the 

Entomological Society of America. 65: 38−41.

Rutledge, C.E., O'Neil, R.J., Fox, T.B. and Landis, D.A. 2004. Soybean 

aphid predators and their use in integrated pest management. Annals of the 

Entomological Society of America. 97: 240−248.

Smith, 1923. Research Bulletin of the Idaho Agricultural Experiment 

Station. 2: 55−57.

Song, F. and Swinton, S.M. 2009. Returns to integrated pest management 

research and outreach for soybean aphid. Journal of Economic 
21

Entomology. 102: 2116−2125.

Sullivan, D.J. and van den Bosch, S. J. 1971. Field ecology of the 

primary parasites and hyperparasites of the potato aphid, Macrosiphum 

euphorbiae, in the east San Francisco Bay area. Annals of the 

Entomological Society of America. 64: 389−394.

USDA-APHIS. 2012. Field Release of Aphelinus glycinis (Hymenoptera: 

Aphelinidae) for Biological Control of the Soybean Aphid, Aphis glycines

(Hemiptera: Aphididae), in the Continental United States; Draft 

Environmental Assessment, Riverdale, MD, 32pp. Fed. Reg. Docket No. 

APHIS-2012-0061.

U.S. Fish and Wildlife Service. 2012. Environmental Online 

Conservation System. http://ecos.fws.gov/tess_public/ last accessed

January 31, 2012.

USFWS—see U.S. Fish and Wildlife Service

van Alphen, J.J.M. and Vet, L.E.M. 1986. An evolutionary approach to 

host finding and selection. In: Insect Parasitoids (Waage, J. and

Greathead, D., eds.). pp. 23−61. Academic Press, London.

van den Bosch, R., Schlinger, E.I., Dietrick, E.J., Hagen, K.S. and

Holloway, J.K. 1959. The colonization and establishment of imported 

parasites of the spotted alfalfa aphid in California. Journal of Economic 

Entomology. 52: 136−41.

Watterson, G.P. and Stone, J.D. 1982. Parasites of blackmargined aphids 

and their effect on aphid populations in far-West Texas. Environmental 

Entomology. 11: 667−669.

Webster, F.M. 1909. Investigations of Toxoptera graminum and its 

parasites. Annals of the Entomological Society of America. 2: 67−87.

Webster, F.M. and Phillips, W.J. 1912. The spring grain-aphis or 

"greenbug". In: USDA Bureau of Entomology Bulletin, Vol. 110

(Agriculture, ed.). 153 pp.

Wu, Z.S., Hopper, K.R., O'Neil, R.J., Voegtlin, D.J., Prokrym, D.R. and

Heimpel, G.E. 2004. Reproductive compatibility and genetic variation 

between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), 

a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae). 

Biological Control. 31: 311−319.

Yasnosh, V.A. 1963. New species of the genus Aphelinus Dalm. 

(Hymenoptera, Chalcidoidea) in the fauna of the USSR. 
22

Entomologicheskoe Obozrenie 42(1): 178-185 as cited in

http://zipcodezoo.com/Animals/A/Aphelinus_certus.

Zuparko, R.L. and Dahlsten, D.L. 1993. Survey of the parasitoids of the 

tuliptree aphid, Illinoia liriodendri (Hom: Aphididae), in northern 

California. Entomophaga. 38: 31−40.

Zuparko, R.L. and Dahlsten, D.L. 1995. Parasitoid complex of 

Eucallipterus tiliae (Homoptera: Drepanosiphidae) in northern California. 

Environmental Entomology. 24: 730−737.
23

Appendix A. Aphelinus species described from North America and their species complexes, distributions, and reported hosts

Species Author

Species 

complex Reported distribution Reported hosts

howardii Dalla Torre, 

1898

abdominalis California (Howard, 1895) Acyrthosiphon pisum (Herting, 1972); Macrosiphum euphorbiae 

(Sullivan and van den Bosch, 1971); Illinoia liriodendri (Zuparko and

Dahlsten, 1993)

jucundus Gahan, 1924 abdominalis California (Gahan, 1924); New York (Griswold, 

1926)

Acyrthosiphon malvae (Griswold, 1926); Acyrthosiphon

pseudodirhodum (Griswold, 1927); Aulacorthum solani (Herting, 

1972); Macrosiphum euphorbiae (Gahan, 1924); Myzus persicae 

(Griswold, 1927)

semiflavus Howard, 1908 asychis Colorado (Howard, 1908); Indiana (Hartley, 1922);

Kansas, Oklahoma (Kelly, 1917); Minnesota, New 

Mexico (Webster and Phillips, 1912); New York

(Griswold, 1927); Ohio (Girault, 1917)

Acyrthosiphon pisum, Aphis gossypii, Cerusaphis viburnicola,

Rhopalosiphum maidis, Macrosiphoniella sanborni, Macrosiphum 

avenae (Hartley, 1922); Aphis rumicis, Brevicoryne brassicae, 

Lipaphis pseudobrassicae, Sitobion avenae (Peck, 1963);Chaitophorus 

viminalis, Schizaphis graminum (Webster and Phillips, 1912); Myzus 

persicae (Howard, 1908); Myzaphis rosarum (Peck, 1963)

marlatti Ashmead, 

1888

asychis Kansas (Ashmead, 1888b); Ontario; Quebec (Peck, 

1963)

Aphis sp. (Ashmead, 1888b); Myzus persicae (Herting, 1972)

lapisligni Howard, 1917 mali Oregon (Howard, 1917); Idaho (Smith, 1923);

Washington (Smith, 1923)

Brachycaudus helichrysi (Peck, 1963); Nearctaphis bakeri (Howard, 

1917)

mali Haldeman, 

1851

mali Arkansas (Becker, 1918); Colorado (Gillette and

Taylor, 1908); District of Columbia, Illinois,

Missouri (Howard, 1881); Kansas (Lohrenz, 1911);

Nebraska (Bruner, 1894); Pennsylvania (Cresson, 

1862)

Eriosoma americanum (Girault, 1909); Eriosoma crataegi (Howard, 

1881); Eriosoma lanigerum (Haldeman, 1859)

prociphili Carver, 1980 mali Iowa (Carver, 1980) Prociphilus fraxinifolii (Carver, 1980)

sanborniae Gahan, 1924 mali Pennsylvania (Gahan, 1924); Ohio (Delong and

Jones, 1926)

Sanbornia juniperi (Gahan, 1924); Nasonovia houghtonensis (Delong 

and Jones, 1926)

siphonophorae Ashmead, 

1888

mali Florida (Ashmead, 1888a); New Jersey (Peck, 

1963)

Macrosiphum sp. (Ashmead, 1888a)

nigritus Howard, 1908 varipes South Carolina (Howard, 1908); Kansas, Minnesota

(Webster and Phillips, 1912); New Mexico

(Webster, 1909); Oklahoma (Jackson et al., 1970);

Texas (Archer et al., 1974)

Schizaphis graminum (Howard, 1908); Hysteroneura setariae 

(Webster and Phillips, 1912); Aphis helianthi (Rogers et al., 1972);

Rhopalosiphum maidi (Jackson et al., 1970)

aureus Gahan, 1924 subgenus 

Mesidia 

California (Gahan, 1924) Chaitophorus nigrae (Gahan, 1924)

automatus Girault, 1911 subgenus 

Mesidia 

Illinois (Girault, 1911); Virginia (Girault, 1916);

California (Zuparko and Dahlsten, 1995)

Chaitophorus sp. (Girault, 1911); Hysteroneura setariae (Girault, 

1916); Eucallipterus tiliae (Zuparko and Dahlsten, 1995)
24

gillettei Howard, 1914 subgenus 

Mesidia 

Colorado (Howard, 1914) Diuraphis tritici (Howard, 1914)

perpallidus Gahan, 1924 subgenus 

Mesidia 

Iowa (Gahan, 1924); Alabama (Edelson and Estes, 

1987); California (Peck, 1963); Florida (Mizell and

Schiffhauer, 1990); Texas (Watterson and Stone, 

1982)

Chromaphis juglandicola (Peck, 1963); Melanocallis fumipennellus, 

Monellia costalis (Peck, 1963); Monellia caryella (Bueno and Stone, 

1983); Monelliopsis pecanis (Edelson and Estes, 1987)
25

Appendix B. Host specificity tests for Aphelinus 

rhamni (Hopper 2011; 2012).

Parasitism in 24-hour exposure of aphids on plant. Individual female parasitoids were exposed 

to one of 12 aphid species. One to five day old females were used that had been with males and 

aphids since emergence and thus had the opportunity to mate, host-feed, and oviposit. Females

were isolated from males and aphids for 24 hours before using them in experiments to insure that 

the females had a full egg load. Each female parasitoid was placed in a cage (10 centimeters (cm) 

diameter by 22 cm tall) enclosing the foliage of a potted plant of the appropriate species with 100 

aphids of mixed instars of a single species. Female parasitoids were removed after 24 hours and 

were used only once.

Because these parasitoids can parasitize a maximum of 20 aphids in 24 hours, this abundance of 

aphids and period of exposure allowed parasitoids to use their full egg complement. 

Furthermore, the density of aphids, amount of plant material, and cage size meant that 

parasitoids were not limited by search rate. Parasitism scoring occurred after larval parasitoids 

killed and mummified their hosts. Therefore, a combination of acceptance of hosts for 

oviposition and suitability of hosts for parasitoid development were measured.

Female parasitoids had the choice to oviposit or not to oviposit in a particular host species. This 

is frequently the choice parasitoids make in the field. The purpose of this study was to measure

parasitism in an environment that appears to harbor only one aphid species on only one plant

species and where female parasitoids re-encounter this combination repeatedly starting with a

full egg complement.

Ten days after exposure of aphids to parasitoids, any mummified aphids were collected and held 

for adult parasitoid emergence. After the adults emerged, the number of mummified aphids and 

the number and sex of adult parasitoids were recorded. Eight to 32 females on each of 12 aphid 

species were tested.

After 24 hours exposure, the number of aphids mummified by A. rhamni varied with aphid 

species (F = 13.1; df = 12, 213; P < 0.0001; Fig. 3).Female parasitoids rarely or never parasitized 

aphids outside the genus Aphis; within the genus Aphis, female parasitoids produced

mummified aphids on species phylogenetically close to A. glycines, e.g. A. gossypii, A.

monardae, and A. oestlundi, but not on aphids that are more phylogenetically distant, e.g. A. nerii

and A. rumicis. The low numbers of mummified aphids for A. nerii may have resulted from

their host plant, A. syriaca, which is known to produce toxic secondary chemicals which aphids

could sequester for their defense (Mooney et al., 2008, Warashina and Noro, 2000). This effect is

supported by many fewer mummies for A. gossypii on A. syriaca than on G. hirsutum (Fig. 3).

The proportion of mummies from which parasitoid adults emerged was generally high 

(0.93±0.01) but varied among species (F = 4.6; df = 8, 67; P = 0.0002) because A. oestlundi had

a lower adult emergence rate (0.64±0.01) than the other aphids. Sex ratio of parasitoid progeny
26

did not differ from equality (0.52±0.02) and did not differ among aphid species.

Direct observations of behavior in experiments on the stresses of starvation and age, egg load, 

and experience affecting acceptance of low versus high quality host species for oviposition by 

Aphelinus rhamni found female parasitoids may behave differently after encountering low versus 

high quality hosts for longer periods. Starved Aphelinus rhamni females persisted in ovipositing 

more in high-quality aphid species than in low quality aphid species. Females oviposited about 

twice as often in Aphis glycines than in A. craccivora or R. padi (F = 5.8; df = 2,128; P = 0.004).

Starved and fed females laid about the same numbers of eggs (1.0 ± 0.2 versus 1.1 ± 0.2, 

respectively), and there was no interaction between nutrition and aphid species in their effect on 

oviposition. Aphid species and egg load did interact in their effect on oviposition (F =

5.9; df = 3,124; P = 0.0009).Honey-fed parasitoids exposed to A. glycines oviposited more when 

they carried more eggs, but oviposition in the other aphid species did not increase with egg load, 

and increased only slightly in water-fed females exposed to A. glycines. This pattern is the 

opposite of what one would expect if female parasitoids became choosier as eggs became more 

limiting. The higher oviposition in A. glycines did not result from stinging this species more 

often. Indeed, female parasitoids stung A. craccivora more often than A. glycines, which was 

stung at the about the same rate as R. padi (6.3±0.4, 4.1±0.3, and 3.7±0.3 aphids, respectively; F 
27

= 17.3; df = 2,156; P < 0.0001), although A. glycines was oviposited in twice as often as the 

other aphid species. The lack of correlation between stinging and oviposition, probably results

because Aphelinus females usually do not directly contact aphids before ovipositor insertion, and 

thus are may not assess host quality until aphids are stung. On encountering a potential host, 

Aphelinus rhamni females stop at about half their body length away from the aphid. Without

touching the aphid, females sway from side to side several times with antennae extended (an 

approach). Stinging did not vary with nutrition, egg load, nor did these factors interact with aphid

species in its effect on numbers of aphids stung.

Effect of age on oviposition in low versus high quality hosts. Ten-day old Aphelinus

rhamni females persisted in ovipositing more in a high quality aphid species than in a low quality

aphid species. Females oviposited over twice as often in A. glycines than in R. padi (F

= 13.0; df = 1,76; P = 0.0006). Young and old females laid about the same number of eggs (1.1

± 0.2 versus 0.9 ± 0.2 eggs, respectively), and there was no interaction between parasitoid age

and aphid species.

As in the nutrition experiment, there was a strong interaction between aphid species and

egg load in their effect on oviposition (F = 6.6; df = 3,125; P = 0.0002). Young parasitoids

exposed to A. glycines oviposited more when they carried more eggs, but oviposition did not

increase significantly with egg load in parasitoids exposed to R. padi or in older parasitoids

exposed to A. glycines. As in the nutrition experiment, the preference for high quality

hosts persisted in the face of low versus high egg load. At the start of observations, young

females carried about 3 more eggs than older females (9.5 ± 0.9 versus 6.2 ± 0.6, respectively; F 

= 453.3; df = 2,77; P < 0.0001), and by the end of observations, both young and old females still 

had eggs they had not oviposited (8.0 ± 0.8 and 5.3±0.6, respectively).

The higher oviposition in A. glycines was partly a result of stinging this aphid species more

often. Unlike the starvation experiment, where A. glycines and R. padi where stung equally often,

female parasitoids in this experiment stung A. glycines slightly more often than R. padi.

Effect of age on oviposition in low versus high quality hosts. Ten-day old Aphelinus rhamni 

females persisted in ovipositing more in a high quality aphid species than in a low quality

aphid species. Females oviposited over more than twice as often in A. glycines than in R. padi 

(F= 13.0; df = 1,76; P = 0.0006). Young and old females laid about the same number of eggs 

(1.1± 0.2 versus 0.9 ± 0.2 eggs, respectively), and there was no interaction between parasitoid 

age and aphid species.

As in the nutrition experiment, there was a strong interaction between aphid species and

egg load in their effect on oviposition (F = 6.6; df = 3,125; P = 0.0002). Young parasitoids

exposed to A. glycines oviposited more when they carried more eggs, but oviposition did not

increase significantly with egg load in parasitoids exposed to R. padi or in older parasitoids

exposed to A. glycines. As in the nutrition experiment, the preference for high quality

hosts persisted in the face of low versus high egg load. At the start of observations, young

females carried about 3 more eggs than older females (9.5 ± 0.9 versus 6.2 ± 0.6, respectively; F 

= 453.3; df = 2,77; P < 0.0001), and by the end of observations, both young and old females still 
28

had eggs they had not oviposited (8.0 ± 0.8 and 5.3±0.6, respectively). The higher oviposition in 

A. glycines was partly a result of stinging this aphid species more often. 

Unlike the starvation experiment, where A. glycines and R. padi where stung equally often,

female parasitoids in this experiment stung A. glycines slightly more often than R. padi (5.6±0.4 

versus 4.4±0.3, respectively; F = 5.3; df = 1,77; P = 0.02).However, this difference was only 1.3 

fold more stings in A. glycines than R. padi, whereas oviposition was 2.5 fold greater in A. 

glycines than in R. padi. Stinging did not vary with age, egg load, nor did these factors interact 

with aphid species in its effect on numbers of aphids stung. The frequency of host feeding did 

not vary with age, but parasitoids fed on A. glycines more frequently than on R. padi (32 percent 

versus 6 percent of parasitoids fed on each species; likelihood ratio χ2 = 8.2; n = 74; P = 0.003), 

and this difference was similar to that for honey-fed parasitoids in the nutrition experiment of the 

same age. Host feeding did not vary with egg load for either aphid species, age, or their

combinations.

Differences in aphid defense cannot explain differences in oviposition between species because 

A. glycines defended itself as much as R. padi (2.3 ± 0.3 versus 2.1±0.3 defensive behaviors per 

approach), but received over twice as many eggs. Amount of aphid defense behavior did not vary

with aphid species, age, or their interaction.

Both young and old Aphelinus rhamni females produced more progeny on high quality host 

species than on low quality host species when exposed to the aphids for 24 hours.

Conclusions. Stresses that decreased life expectancy did not increase acceptance of low quality

host species by Aphelinus rhamni. Egg load was also lower in stressed females, which resorbed 

eggs in response to starvation and aging, so changes in life expectancy and egg load may have 

counterbalanced one another. However, the decrease in egg load was small relative to the 

decrease in life expectancy, particularly for starved females, which carried about three-quarters

of the egg load of honey-fed females, but would die the day following the assays.

Furthermore, although oviposition increased with egg load for females exposed to A. glycines,

oviposition did not vary with egg load for females exposed to low quality aphid species. The

outcome of this pattern was that females became less choosy as egg load decreased, rather than

becoming choosier, as theory predicts. Besides having lower life expectancy, older females were 

kept without aphids as they aged so they experienced a more aphid-poor environment than did 

young parasitoids. It was expected this would make parasitism of low quality aphids by older 

females more frequent, yet it did not. These results demonstrate that A. rhamni specificity is 

behaviorally stable rather than dynamic, and low-quality non-target species should not have 

increased risk of attack when parasitoids are stressed from starvation or age or when they

accumulate eggs.