BIOLOGICAL CONTROL OF INVASIVE APHIDS IN HAWAII

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: TERMINATED
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 0201739
• Project No.: HAW00970-H
• Project Start Date: Oct 1, 2004
• Project End Date: Sep 30, 2009

Project Director
Messing, R. H.

Recipient Organization
UNIV OF HAWAII
3190 MAILE WAY
HONOLULU,HI 96822

Performing Department
PLANT & ENVIRONMENTAL PROTECTION SCIENCES

Non Technical Summary
Invasive species of arthropods in Hawaii pose a continuous, serious, and growing threat to the well-being of virtually all agricultural and natural ecosystems in the state. Historically, Hawaii has responded to invasive pests with strong efforts at classical biological control. This method of importing and establishing self-replicating predators, parasitoids, and pathogens of invasives has resulted in complete control of 38 species of insect pests and 7 species of weeds, plus substantial suppression of another 13 insect species and 3 weeds. In recent years biological control in Hawaii has become much more restricted, and the rate of natural enemy introductions has plummeted. More than any other state in the nation, Hawaii has come to have formidable regulatory obstacles to the practice of biological pest control. As the number of invasive arthropods increases, and the number of natural enemy introductions decreases, Hawaii faces an increasingly critical biotic gap in pest control, with severe consequences for both agriculture and native ecosystems. Aphids comprise one taxon of invasive pests in Hawaii that can confidently be targeted for classical and augmentative biological control with little risk of non-target impacts. This project will identify extant aphid species throughout the Hawaiian isands and seek to import effective natural enemies to increase biological control of aphid pests of agriculture.

Animal Health Component

(N/A)

Research Effort Categories

Basic

20%

Applied

80%

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
215	3110	1130	100%

Knowledge Area
215 - Biological Control of Pests Affecting Plants;

Subject Of Investigation
3110 - Insects;

Field Of Science
1130 - Entomology and acarology;

Keywords

biological control (insects)

aphididae

hawaii

invasive species

insect surveys

insect distribution

abundance

insect population

population dynamics

natural enemies

insect ecology

insect identification

insect predators

parasitoids

quarantines

insect release

entomopathogens

Goals / Objectives
1) Conduct a broad and intensive survey throughout the state to determine distribution, relative abundance, and host associations of extant aphid species, as well as their natural enemies, in agricultural, weedy, and native habitats. 2) Prepare a comprehensive database and simple but accurate diagnostic materials for identification of extant aphids as well as those associated with regularly incoming commodities to the Hawaiian Islands. 3) Introduce, quarantine, release, and evaluate parasitoids (and possibly predators) of aphids into Hawaii to improve biological control and build up biotic resistance to this group of invasives. 4) Determine the occurrence and efficacy of indigenous Hawaiian entomopathogens that infect aphids, and ways in which their effect as biological control agents may be enhanced.

Project Methods
1) Using protocols similar to Pike et al. (2000), we will regularly sample a diversity of agricultural, weedy, and native habitats to collect, curate and identify all aphid species on the major islands in Hawaii. Alates and other adult aphids will be collected directly in he field if available; in other cases plant material will be returned to the laboratory in coolers and earlier instar aphids reared in cages until the adult stage (necessary for taxonomic work). We will document distribution, abundance, and host associations of extant species, and provide all information to the State Dept. of Agriculture on a regular basis to update KTO lists. 2) Combining historical and current interception data from the HDOA, previously published keys, and any new species we find during our surveys, we will prepare a database of all aphid species in Hawaii and those which are most likely to invade in the near future, based on their association with agricultural and ornamental commodities regularly imported into the state. Along with this database, we will take digital macro-photographs of all species as well as key morphological characteristics necessary to distinguish among them. Information will be combined into simplified keys that can be used with minimal training of agricultural inspectors, and a website, CDs and hard copy booklet will be prepared that contains the digital photographs, keys, and most relevant abstracts of the database. 3) A matrix of extant Hawaiian aphids and parasitoids that are documented to attack them in different parts of the world is currently being elaborated. We will focus in on host-parasitoid relationships that are known to be effective in other regions. Initial importations will be from pure colonies of parasitoids being reared in insectaries, or those readily available in the field. (For example, Lipolexis scutellaris is known to be abundant on citrus aphids (Toxoptera spp.) in Guam). 4) Aphid populations will be sampled from a variety of diverse habitats, and screened for the presence of entomopathogens. Sampled aphids will be examined for signs of mycosis, and placed on water agar media to allow fungi to grow. Entomopathogens that grow on the water agar will be subsampled and grown on corn meal agar. Fungi that are isolated will be grown in pure cultures, and identified. Laboratory bioassays will be conducted to demonstrate that the fungi are responsible for mortality of aphids.

Progress 10/01/04 to 09/30/09

Outputs
OUTPUTS: We surveyed aphid species on all major Hawaiian islands, analyzed and described geographic and host relationships. We also analyzed the morphological and ecological factors contributing to invasiveness in these species. Experiments were performed on deliberately introduced biological control agents of aphids; and on fortuitous biocontrol agents (that arrived by unknown means) to Hawaii. We presented the first description and gave life history information on a new species of aphid parasitoid, Endaphis fugitiva, found to parasitize the banana aphid, Pentalonia nigronervosa Coquerel, the vector of banana bunchy top virus We published several papers in peer-reviewed scientific journals, and gave multiple talks, seminars, and presentations about our results at scientific symposia; and provided testimony and published a Draft Environmental Assessment for the introduction of new aphid parasitoids in Hawaii. PARTICIPANTS: Dr. Ed Mondor worked as a Junior Entomologist and obtained advanced research training that helped him obtain a full-time tenure track faculty position at Georgia Southern University. Dr. Frederic Muratori worked as a Junior Entomologist and obtained advanced research training that helped him obtain a position at the University Catholique de Louvain in Belgium. Drs. Keith Pike (Washington State University) and Robert Foottit (Agriculture Canada) collaborated on a book describing the overall invasive aphid fauna of the islands. TARGET AUDIENCES: Farmers, consumers, and rural citizens who can appreciate reduced pesticide inputs as we come to rely more on biological means of pest control. Scientists who study invasive species and in particular aphid biology. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
We documented the occurrence and host plants of over a dozen new invasive aphid species not previously known to occur in Hawaii. We documented a large number of endemic Hawaiian plants, some of which are threatened or endangered, that are attacked by these invasive aphid species. We defined the host range for a newly imported aphid parasitoid in Hawaii (Aphidius transcaspicus). We provided life history data on a newly discovered aphid parasitoid in Hawaii (Endaphis fugitiva). We successfully obtained State and Federal permits for the introduction of a new aphid parasitoid into Hawaii (Binodoxys communis).

Publications

• Mondor, E. B., M. N. Tremblay & R. H. Messing. 2006. Extrafloral nectary production in Vicia faba is both damage and resource-dependent. Biology Letters 2: 583-585.
• Muratori F. B., R. J. Gagne & R. H. Messing. 2009. Ecological traits of a new aphid parasitoid, Endaphis fugitiva (Diptera: Cecidomyiidae), and its potential for biological control of the banana aphid, Pentalonia nigronervosa (Hemiptera: Aphididae). Biological Control 50: 185-193.
• Wang, X. G. & R. H. Messing. 2006. Potential host range of the newly introduced aphid parasitoid Aphidius transcaspicus (Hymenoptera: Braconidae) in Hawaii. Proc. Haw. Entomol. Soc. 38: 81-86.

Progress 10/01/07 to 09/30/08

Outputs
OUTPUTS: We have presented the first description and have given life history information on a new species of aphid parasitoid, Endaphis fugitiva, found to parasitize the banana aphid, Pentalonia nigronervosa Coquerel, the vector of banana bunchy top virus. Field and laboratory observations showed that fly eggs are laid on the leaves near an aphid colony, the newly hatched fly larvae search for hosts while crawling on the leaf, and they penetrate the aphid between the legs and thorax, develop as koinobiont endoparasitoids, and eventually emerge from the aphid's anus and fall to the ground to pupate in the soil. We provided parameters for the rearing of Endaphis fugitiva, and discussed the potential of this new species to contribute to the control of banana aphid in Hawaii. A paper has been submitted and is in review in the journal Biological Control. We also submitted an Environmental Assessment for the Chinese aphid parasitoid Binodoxys communis to the state Office of Environmental Quality Control. PARTICIPANTS: Russell Messing (PI) developed the project, surveyed for aphids statewide, documented new (native plant) hosts. Dr. Frederic Muratori (University Catholique de Louvain, Belgium) was a post-doc who worked extensively on the description and experiments with the new aphid parasitoid Endaphis fugitiva. He has professionally developed in his research skills and secured employment back in Belgium, where he continues to work with Endaphis. Dr. Ray Gagne, USDA-ARS; Dr. Keith Pike (Washington State University); and Dr. Bob Foottit (Canadian National Collection of Insects) all provided valuable taxonomic assistance with aphids and aphid parasitoids. TARGET AUDIENCES: Farmers (who grow crops infested by aphids); consumers (who eat crops that may have pesticide residues); and conservationists (who try to conserve aphid infested plants) all benefit from the efforts to establish better aphid biological control. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
We have gained additional knowledge about the extant parasitoid guild attacking the banana aphid and other aphids in Hawaii's crops. This knowledge will be critical to incorporate into future Integrated Pest Management Programs for both banana and for ornamental host plants that serve as aphid hosts. We have also gained knowledge about the infestation of native Hawaiian plants by invasive aphids; this can be useful in assessing threats to endangered species, and in providing additional impetus to island wide sustainable control strategies for these invasive species that infest both agricultural and native plants. Knowledge of the factors that contribute to invasiveness of aphids can help mitigate future invasions of new pest species.

Publications

• Messing, R. H. M. N. Tremblay Mondor, E. B., Foottit R. G. & Pike K. S. 2007. Invasive aphids attack native Hawaiian plants. Biological Invasions 9: 601 to 607.
• Mondor, E. B., M. N. Tremblay & R. H. Messing. 2007. Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands. Biological Invasions 9: 87-100.

Progress 10/01/06 to 09/30/07

Outputs
OUTPUTS: Experiments were performed on deliberately introduced biological control agents of aphids; and on fortuitous biocontrol agents (that arrived by unknown means) to Hawaii. PARTICIPANTS: Dr. Russell Messing (PI): University of Hawaii, Kauai Agricultural Research Center Dr. Xin-geng Wang: currently at University of California at Riverside, Kearney Research Center. Dr. Frederic Muratori: Laboratoire d'ecologie et biogeographie Departement de biologie, Universite catholique de Louvain (Dr. Muratori is currently doing post-doctoral training in Dr. Messing's lab). Both Dr. Wang and Dr. Muratori took advantage of the opportunity for professional development by advancing their research skills and training. TARGET AUDIENCES: Farmers, consumers, and rural citizens who can appreciate reduced pesticide inputs as we come to rely more on biological means of pest control.

Impacts
We have obtained new knowledge about the existing guild of biological control agents that is extant in Hawaii, and is currently contributing to the control of aphid populations.

Publications

• Wang, X. G. & R. H. Messing. 2006. Potential host range of the newly introduced aphid parasitoid Aphidius transcaspicus (Hymenoptera: Braconidae) in Hawaii. Proc. Haw. Entomol. Soc. 38: 81-86.

Progress 10/01/05 to 09/30/06

Outputs
Aphidius transcaspicus Telenga, a mealy plum aphid (Hyalopterus pruni Geoffroy) parasitoid from the Mediterranean, was introduced into Hawaii for control of invasive aphids. Under laboratory conditions the parasitoid successfully attacked several important aphid pests in Hawaii, including the melon aphid (Aphis gossypii Glover), the banana aphid (Pentalonia nigronervosa (Coquerel)), the green peach aphid (Myzus persicae (Sulzer)), the corn leaf aphid (Rhopolosiphum maidis (Fitch)), and the cowpea aphid (Aphis craccivora Koch). It could not successfully parasitize the turnip aphid (Lipaphis erysimi Kalt.) or the black citrus aphid (Toxoptera aurantii (Boyer de Fonscolombe)). Field cage tests with P. nigronervosa and M. persicae also showed that A. transcaspicus successfully attacked both host species under semi-natural conditions, and preferred M. persicae over P. nigronervosa.

Impacts
The introduction and establishment of new natural enemies of aphids will reduce pesticide use and contribute to more sustainable pest management.

Publications

• No publications reported this period

Progress 10/01/04 to 09/30/05

Outputs
We identified two potential parasitoids of aphids that are available for importation to Hawaii: Bindoxys communis (Braconidae) originated in China and is currently being reared in Minnesota on the soybean aphid, and also is reported to attack the melon aphid (Aphis gossypii), the major aphid pest species in Hawaii. Lipolexis oregmae (Braconidae) also originated in Asia and is available via colleagues in Guam where it parasitizes several species of citrus aphids. We are currently evaluating population levels of target aphids so as to have a baseline against which to measure impact of the introduced parasitoids.

Impacts
Importation of new natural enemies of aphids will increase natural mortality and reduce reliance on chemical pesticides.

Publications

• No publications reported this period