News 51N research focusing on parasitoid wasps as model tions did not reach the levels recorded prior to 1997 organisms. and were brought under control by the weevil.

Conclusion A full cost:benefit analysis was performed on the A. filiculoides biological control programme. This We wish to provoke action from both ‘pure’ and showed that the economic returns would increase ‘applied’ parasitoid biologists, preferably in the form from 2.5:1 in 2000 to 13:1 in 2005, and are predicted of collaboration. The most obvious benefits of such to increase to 15:1 by 2010. Based on the field evi- cross-disciplinary research are, however, already on dence, there is no reason to suggest that this offer: simple and practicable manipulations of para- prediction is an underestimate. sitoid rearing conditions can greatly enhance efficiency by promoting female bias. Practitioners Ten years on, S. rufinasus is now widely established who are trained more in ‘applied entomology’ than in throughout South Africa and there is no need to fur- ‘evolutionary ecology’ may take solace in the fact that ther distribute the agent. No parasitism of the weevil there should be no need to delve very deeply into the has been recorded in the field and it is envisaged that fascinating, yet huge and dauntingly complex, litera- there will be no need for additional biocontrol agents. ture on sex ratio evolution: the essential Azolla filiculoides is now under complete control in assumptions and predictions of the theory, as out- South Africa, but with the decline of these infesta- 1 lined above (and given in more detail in ref. ), are tions of red water fern, other aquatic plant taxa relatively straightforward. (Lemna sp., Wolffia sp., Spirodela sp. as well as algae) have taken the vacated niche. The successful 1 Ode, P.J. & Hardy, I.C.W. (2008) Parasitoid sex control of these three species will rely on a commit- ratios and biological control. In: Wajnberg, E., Bern- ment to reducing eutrophication in aquatic stein, C. & van Alphen, J.J.M. (eds) Behavioral ecosystems – something that needs to be addressed ecology of insect parasitoids: from theoretical in the many tropical countries of the world that are approaches to field applications. Blackwell, Oxford, battling successive invasions by aquatic weeds. UK. pp. 253–291. [In press] By: Andrew McConnachiea and Martin Hillb By: Ian C. W. Hardya & Paul J. Odeb aARC-PPRI, Weeds Division, Private Bag X6006, aSchool of Biosciences, University of Nottingham, Hilton, 3245, South Africa. Sutton Bonington Campus, Loughborough, Leices- Email: [email protected] tershire LE12 5RD, UK. Fax: +27 33 355 9423 Email: [email protected] Fax: +44 115 9516060 bDepartment of Zoology and Entomology, Rhodes University, Grahamstown, 6140, South Africa. bDepartment of Entomology, North Dakota State Email: [email protected] University, 270 Hultz Hall, 1300 Albrecht Blvd., Fax: + 27 46 622 8959 Fargo ND 58105, USA. Email: [email protected] Fax: +1 701 231 8557 Progress on Biological Control of the Emerald Ash Borer in North America 51N Weevil, Weevil Rock You: Ten Years of Azolla In 2002, the emerald ash borer (EAB), Agrilus Biocontrol in South Africa planipennis, a buprestid beetle native to Northeast Asia, was discovered as the cause of extensive ash The biological control programme launched against tree (Fraxinus spp.) mortality in southern Michigan Azolla filiculoides (red water fern) in South Africa and Ontario. It is believed that EAB was introduced was first reported on in the March 2001 issue of BNI. into Michigan from solid-wood packing materials After the first release of the curculionid weevil Sten- during the 1990s and became established in the opelmus rufinasus in December 1997, further abundant ash resources throughout urban areas, releases were made at 111 sites throughout the parks, forests, and riparian ecosystems1. In an effort republic, covering a wide variety of water body types to protect ash resources in North America, regula- and climatic zones. Quantitative post-release evalu- tory agencies imposed quarantines and developed ations revealed that the weevil caused a dramatic programmes to eradicate and contain EAB. Although reduction in the populations of the weed with local these efforts may have slowed the rate of spread, extinctions occurring at the majority of sites within eradication was abandoned in the ‘core infestation’ the space of a year. due to the size of the infestation, the lack of effective methods to detect and control EAB, and the chal- The weevil has shown a wide thermal tolerance in lenges associated with quarantine compliance and the field, as predicted from pre-release studies, and enforcement. Although researchers estimate EAB an ability to disperse unaided over long distances (up can spread 10 to 20 miles (16–24 km) per year, to 300 km). Despite local extinctions of the host humans are responsible for its long-range dispersal plant, the weevil has been able to persist by moving through the illegal transport of infested ash nursery between infestations of the weed. In the last ten stock, firewood, and logs. Regulatory agencies have years, the weevil has been recorded from 42 new determined that EAB is established throughout Azolla sites and where the weed has reoccurred (at Lower Michigan and areas of the neighbouring 22 of the original 112 release sites) these re-infesta- states of Ohio and Indiana; separate infestations are 52N Biocontrol News and Information 28(3) also known in Michigan’s Upper Peninsula, Illinois, The lack of natural enemies capable of suppressing Maryland, and Pennsylvania. This invasive EAB populations below a density threshold tolerable buprestid is expected to continue spreading for survival of native ash trees is especially trou- throughout North America due to the widespread bling, and supports the need to introduce parasitoids use of ash as a landscape tree and the prevalence of that coevolved with EAB in Asia for biological control ash trees throughout forested and riparian ecosys- of this buprestid in North America. tems. Land managers and the public are now seeking sustainable management methods to reduce EAB Natural Enemies of EAB in China population densities and to slow its rate of spread. Foreign exploration for EAB in its native range in When EAB was discovered in North America, only China resulted in the discovery of three hymenop- scant information on its biology was available in the teran parasitoids considered suitable for use as literature from Asia where it is considered only a biocontrol agents in North America: a gregarious 2,3,4 minor and periodic pest of indigenous ash species. To larval braconid ectoparasitoid Spathius agrili , a develop biological and microbial controls for EAB in gregarious larval eulophid endoparasitoid Tetras- 3,5,6 North America, we began studying this beetle in tichus planipennisi , and a solitary, Michigan and China in 2002. EAB completes its life parthenogenic encyrtid egg parasitoid Oobius 6,7 cycle in one or two years depending on the age of the agrili . We have found T. planipennisi overlaps in 3 6 infestation, tree health, and other biotic and abiotic distribution with S. agrili and O. agrili , although factors. Emergence of EAB adults typically begins in additional survey work is needed to identify their late May and peaks during June. Adults chew D- distributions and interactions in China. shaped exit holes in the tree bark to emerge and begin maturation feeding on ash foliage followed by Oobius agrili was discovered in 2004 in Jilin Prov- 7 mating; after about three weeks, females start to ovi- ince, China although it may be more widely posit in bark crevices and between bark layers. distributed. In China, O. agrili is a solitary egg par- Although egg-laying peaks toward the end of June, asitoid with at least two generations per year. It eggs are laid throughout the summer and into the spends the winter and spring as a mature larva in fall due to a prolonged adult emergence period and EAB eggs, and adult emergence is synchronized with long adult longevity. After egg hatch, EAB neonates the EAB oviposition period during July and August tunnel through the tree bark until reaching the in the field. Parasitism rates of O. agrili in EAB eggs phloem where they continue feeding through four peak at 61.5% in August. Its distribution overlaps larval stages. When mature, EAB larvae chew pupa- with that of T. planipennisi at one of our study sites tion cells in the outer sapwood or bark; pupation in China, and the combined mortality of EAB by 6 occurs during the spring or summer. Early in an these two parasitoids is ca. 75% . Oobius agrili is infestation, EAB attacks the upper crown of large parthenogenic, thus females produce females ash trees, and as populations increase, the trees without mating; its sex ratio from field-collected EAB become weaker. Tree mortality is caused by larval eggs in China is 15:1 (female:male). Much of the girdling of the main trunk, when EAB populations knowledge of this parasitoid’s biology is based on lab- reach lethal density thresholds for ash. This occurs oratory studies in our quarantine laboratory. We over a period of several years depending on initial have found that O. agrili females prefer to oviposit in tree health, species, site, rainfall, and other factors. 0- to 6-day-old EAB eggs, live ca. three weeks, and Current management strategies are being developed complete a generation every three weeks. The with the goals of containing isolated EAB infesta- average lifetime fecundity of each female is ca. 24 tions, slowing its spread, and suppressing population progeny, with a range of five to 62. densities below a tolerance threshold for survival of North America’s ash trees. In Michigan, we developed methods to rear O. agrili in the laboratory from eggs produced by EAB adults, Lack of Natural Enemies in North America which are reared from EAB-infested ash logs cut in winter and held in cold-storage. After emergence We conducted natural enemy studies in Michigan from infested logs held at room temperature in the from 2002 to 2004, and found 0.7% parasitism for laboratory, EAB adults are fed greenhouse-grown EAB larvae; no egg parasitoids were found. The Fraxinus uhdei foliage and allowed to oviposit on larval parasitoids reared from EAB larvae in Mich- small ash sticks; sticks with EAB eggs are removed igan included hymenopteran parasitoids that attack and exposed to O. agrili for parasitism in a plastic native Agrilus spp: two native braconids (Atanycolus cup with a streak of honey and moist cotton ball. In sp. and Spathius floridanus), one native chalcid the laboratory, we performed no-choice assays with (Phasgonophora sulcata), and one exotic eupelmid eggs of six Agrilus spp., two cerambycid beetles, and (Balcha indica). This rate of parasitism detected for four lepidopterans. Overlap in physiological host EAB in the USA is low compared to EAB parasitism range was found for three native Agrilus spp. with rates found in China and those reported in the liter- eggs of similar size to EAB. For these three species, ature for native Agrilus spp. Other biological factors paired choice assays revealed O. agrili strongly pre- causing EAB mortality include entomopathogenic ferred to oviposit in EAB eggs laid on ash than in fungi, three predatory beetle species (Enoclerus sp., eggs of other Agrilus spp. on their respective host Tenebroides sp. and Catogenus rufus), and wood- plants. This confirms that O. agrili is attracted to ash peckers, but rates of attack were relatively low and for host location. constant at different EAB population densities. Some mortality resulted from larval starvation, Tetrastichus planipennisi was discovered in 2003 dehydration, and cannibalism in over-infested trees. in Jilin and Liaoning Provinces of China3 and later News 53N in Heilongjiang Province5. The results of our labora- parasitoids were collected and identified. Because tory and field studies show that T. planipennisi this early testing showed no parasitism of species oviposits through the tree bark and oviposits into the outside the genus Agrilus, even species attacking haemocoel of actively-feeding third- and fourth- ash, further testing concentrated on Agrilus spp. In instar EAB larvae. It completes at least four genera- China, no S. agrili were reared from six species of tions per year and overwinters as a mature larva field-collected Agrilus larvae (n = 2074). However, inside the host gallery. In the spring, the parasitoid no-choice laboratory assays of some Chinese and larva pupates, ecloses as an adult, chews a round 1- North America Agrilus larvae showed some overlap mm diameter hole in the bark, and the wasp brood in the physiological host range of S. agrili, although exits the tree. An average of 35 parasitoids (range successful parasitism was lower in non-hosts than in five to 122) emerges from a single EAB larva. During EAB. Therefore, we evaluated the ecological host 2005, the results of EAB field research in Jilin Prov- range of S. agrili using an olfactometer to determine ince, China revealed T. planipennisi parasitism rates the attractiveness of certain host plants: naïve mated increased from 8% in June to 40% in August6. S. agrili females were placed in vertical Y-tube olfac- tometers and given a choice of leaves and twigs from In Michigan, we developed methods to rear T. 14 tree species or clean air. We found S. agrili was planipennisi in the laboratory by exposing groups of only attracted to Fraxinus pennsylvanica, F. velu- parasitoids to fourth-instar EAB larvae inserted into tina, and the willow Salix babylonica. In nature, if small ash branches. Adult parasitoids are main- parasitoids are not attracted to the host tree they will tained during the exposure period with a streak of be unlikely to encounter and parasitize the non- honey and a moistened cotton ball. T. planipennisi target larvae. Given the combination of evidence completes one generation every three weeks and from no-choice tests (lower parasitism rates or no females live about 24 days, twice as long as males. attack on non-target species), olfactometer tests EAB larvae are acquired for parasitoid production by (only attracted to ash and willow), the lack of S. removal from EAB-infested ash logs or after rearing agrili reared from other Agrilus spp. in China, and on an ash-based artificial diet. Using our laboratory that native Spathius rarely find and parasitize EAB, rearing methods, we evaluated the host specificity of we predict incidental parasitism by S. agrili in non- T. planipennisi using no-choice assays. In these target Agrilus spp. assays, groups of female and male T. planipennisi were exposed to actively-feeding larvae of eight Conclusions buprestid species, five cerambycid species, and a wood-boring sawfly, all implanted in small branches Considering the known adverse consequences of of their respective host plants. We also assayed EAB on ash resources in North America, the lack of larvae of a tenebrionid beetle and two lepidopteran other options (except cutting down trees), the high species by implantation in small ash branches, and potential benefit of these parasitoids, and the low sphingid larvae by exposure on host leaves. Tetras- potential risk to native Agrilus spp., we requested tichus planipennisi rejected all species except permission from the US Department of Agriculture actively-feeding EAB larvae implanted in ash early in 2007 to release the three parasitoids at branches. selected sites in Michigan. After review by scientists and land managers at federal and state agencies, by Spathius agrili was first reported in Tianjin, university faculty members, and a 60-day public China2 where it is a prevalent parasitoid of EAB in comment period, it was agreed that the potential stands of Fraxinus velutina, an ash species native to benefits far outweighed the risks and release permits North America and planted extensively in this part were issued. Field releases of O. agrili and T. of China. Although S. agrili was also found further planipennisi began in July 2007, and releases of S. north in Jilin Province3, most of the research on this agrili are expected to begin later in the summer or parasitoid was done in Tianjin, which is the southern early fall. known range of EAB. In Tianjin, the emergence of S. 1 agrili adults was well synchronized with the availa- Poland, T.M. & McCullough, D.G. (2006) Emerald bility of third- and fourth-instar EAB larvae, its ash borer: invasion of the urban forest and the threat preferred host stages. It completes three generations to North America’s ash resource. Journal of Forestry per year with parasitism increasing from 12% in 104, 118–124. August to 42% in October4. Females oviposit through the tree bark, paralyzing the larva and laying a 2Liu, G.-J. & Liu, E.-S. (2002) Preliminary report on clutch of eggs on the integument. At maturity, larvae control of EAB. An internal report of Ornamental of S. agrili spin a cocoon and pupate within the host Tree Management of Guangang Area, Tianjin City, gallery. Each female lays an average of nine eggs PR China. (range two to 18) per clutch, with an average of 23 eggs during her lifetime; average female longevity is 3Liu, H.-P., Bauer, L.S., Gao, R.-T., Zhao, T.-H., Pet- 29 days. Laboratory rearing of S. agrili is generally rice, T.R. & Haack, R.A. (2003) Exploratory survey similar to that of T. planipennisi. for the emerald ash borer, Agrilus planipennis (Cole- optera: Buprestidae), and its natural enemies in To evaluate the host specificity of S. agrili, no-choice China. Great Lakes Entomologist 36, 191–204. assays were conducted in China and the USA. In addition, from 2003 to 2005, potential host larvae 4Yang, Z.-Q., Strazanac, J.S., Marsh, P.M., van from other trees were collected in Tianjin, China Achterberg, C. & Choi,W.-Y. (2005) First recorded where S. agrili parasitism of EAB was high. These parasitoid from China of Agrilus planipennis: A new larvae were then reared to the adult stage and all species of Spathius (Hymenoptera: Braconidae, 54N Biocontrol News and Information 28(3)

Doryctinae). Annals of the Entomological Society of tation of formal control programmes against America 98, 636–642. parthenium on the African continent and neigh- bouring islands has been lacking. This is most likely 5Yang, Z.-Q., Yao, Y.-X. & Wang, X.-Y. (2006) A new due to lack of recognition of the potential threat or species of emerald ash borer parasitoid from China extent of the problem, lack of official policies on con- belonging to the genus Tetrastichus Haliday trol of invasive plants or introduction of natural (Hymenoptera: Eulophidae). Proceedings of the Ento- enemies, and lack of funding and coordinated efforts. mological Society of Washington 108, 550–558. There has been little documented on the impact of parthenium in African countries, with the exception 6Liu, H.-P., Bauer, L.S., Zhao, T.-H., Gao, R.-T., of Ethiopia. Although parthenium has been present Song, L.-W., Luan, Q.-S., Jin, R.-Z. & Gao, C.-Q. in South Africa since the late 1800s, dramatic (2007) Seasonal abundance of Agrilus planipennis increase in spread and abundance was only noted fol- (Coleoptera: Buprestidae) and its natural enemies lowing the cyclonic event that affected the east coast Oobius agrili (Hymenoptera: Encyrtidae) and Tet- of southern Africa in 1984. Currently within rastichus planipennisi (Hymenoptera: Eulophidae) southern Africa, the northern and northeastern in China. Biological Control 42, 61–71. regions of South Africa, most of Swaziland, and parts of southern Mozambique are severely invaded by 7Zhang, Y.-Z., Huang, D.-W., Zhao, T.-H., Liu, H.-P. parthenium and it is known to occur in Zimbabwe. & Bauer, L.S. (2005) Two new egg parasitoids Until recently, no official control programmes have (Hymenoptera: Encyrtidae) of economic importance been implemented. from China. Phytoparasitica 33, 253–260. In late 2003, South Africa initiated a biological con- By: Leah S. Bauera,b, Houping Liub, Juli R. Gouldc & trol research programme on parthenium, through Richard C. Reardond the national government Department of Water Affairs and Forestry’s Working for Water Pro- aUSDA Forest Service, Northern Research Station, gramme, prioritizing the introduction of the stem- E. Lansing, MI 48823, USA. Email: [email protected] boring curculionid weevil Listronotus setosipennis, the leaf-feeding chrysomelid beetle Zygogramma bDept. of Entomology, Michigan State University, E. bicolorata, the stem-galling tortricid moth Epiblema Lansing, MI 48824, USA. strenuana, and the summer rust fungus Puccinia melampodii. These agents were selected on the basis cUSDA APHIS, Otis AFB, MA 02542, USA. of their success in the extensive Australian biocon- trol programme on parthenium which was initiated dUSDA Forest Service, Forest Health Protection, in the 1970s, their impact on the plant, and their Morgantown, WV 26505, USA. likely suitability for the local climatic conditions. The winter rust fungus Puccinia abrupta var. parthenii- cola is already present in South Africa, Kenya and Managing the Impact of Parthenium Invasions in Ethiopia – its mode and time of introduction Africa unknown. Parthenium biocontrol agents are cur- rently undergoing testing on relevant local plant Parthenium hysterophorus or parthenium weed, an species in quarantine in South Africa to determine annual herb in the family Asteraceae originating their specificity and suitability, and the likelihood of from neotropical Central and South America, is well their release is promising. The first releases in South known to cause major economic losses to crop produc- Africa are anticipated in 2008, pending approval tion and grazing land, and impact severely on from relevant government authorities. The thermal biodiversity, and human and animal health in many physiological parameters of insect agents are being parts of the world. Its status, impacts and opportuni- investigated in the laboratory; these data will be uti- ties for its biological control, as well as results of lized to determine potential and optimal areas for control in Australia and India particularly, have establishment. Within South Africa, other research been discussed in an extensive literature (e.g. 1,2,3,4). is also being conducted on the chemical control of Its prolific seed production, allelopathic properties parthenium in conservation areas, as well as the and tolerance of a range of soil and climatic condi- interaction of native grass species with parthenium tions enable it to be a highly aggressive invader. including the effects of its allelopathic properties. Parthenium is present, and highly invasive in many cases, in Australia, India, Pakistan, Bangladesh, An opportunity to expand biocontrol of parthenium Nepal, Sri Lanka, southern China, Taiwan, beyond South Africa arose with the initiation of a Vietnam, Israel, several Pacific islands (including United States Agency for International Development New Caledonia, Papua New Guinea and Vanuatu), (USAID) Integrated Pest Management Collaborative the Seychelles, Madagascar, Mauritius, Reunion and Research Support Program (IPM CRSP) project on on the African continent (Kenya, Ethiopia, Somalia, ‘Management of the Weed Parthenium (Parthenium Mozambique, South Africa, Swaziland and hysterophorus L.) in Eastern and Southern Africa Zimbabwe). using Integrated Cultural and Biological Control Measures’ in 2005. The objectives of this four-year Despite long-standing control programmes in Aus- project, which is being conducted in selected coun- tralia and India dating back to the early 1970s, and tries within the southern and eastern African although parthenium has been present in Africa for regions, are to (1) survey and map the distribution of decades and has spread widely throughout some parthenium in South Africa, Swaziland, Botswana, countries (e.g. Ethiopia and Swaziland), implemen- Uganda and Ethiopia, (2) determine the socioeco-