Anderson, Aaron (aaron.g.anderson@colostate@colostate.edu) – Colorado State University;
Bautista, Renato (Renato.c.bautista@hawaii.gov) – Hawaii Department of Agriculture;
Chun, Stacy (staceychun_spepper@hawaii.edu) – Hawaii Department of Agriculture;
Collier, Tim (tcollier@uwyo.edu) – University of Wyoming;
Delfosse, Ernest (delfosse@msu.edu) – Michigan State University;
Evans, Edward (Ted) (ewevans@biology.esu.edu) – Utah State University;
Follett, Peter, (peter.follett@ars.usda.gov) – USDA-ARS, Hilo, Hawaii;
Gaskin, Joh, (john.gaskin@ars.usda.gov) – USDA-ARS;
Haverhals, Marijka (marijka@uidaho.edu) – University of Idaho;
Hedstrom, Chris (hedstroc@onidiorst.edu) – Oregon Dept. of Agriculture;
Hinz, Hariet (h.hinz@cabi.org) – CABI;
Kaneshige, Craig (?) – Hawaii Department of Agriculture;
King, Cynthia (Cynthia.b.king@hawaii.gov) – Hawaii Department of Land and Nat. Resources;
Ko, Mann (?) – Department of Agriculture;
Krugner Rodrigo (kruger@ars.usda.gov) – USDA-ARS, Parlier, CA;
Lambert, Adam (lambert@msi.ucsb.edu) – UC-Santa Barbara;
Littlefield, Jeff (jeffreyl@montana.edu) – Montana State University;
Matsunaga, Janis (Janis.N.Matsunaga@hawaii.gov) – Hawaii Department of Agriculture;
McEvoy, Peter (mcevoyp@science.oregonstate.edu) – Oregon State University;
Messing, Russell (messing@hawaii.edu) – University of Hawaii;
Miller, Ross (rmiller@uog.edu) – University of Guam;
Miller, John (jpm@cns.montana.edu) – Montana State University;
Mills, Nick (nmills@berkeley.edu) – UC-Berkeley;
Morgan, David (dmorgan@cdfa.ca.gov) – California Department Food & Agriculture;
Naranjo, Steve (steve.naranjo@ars.usda.gov) – USDA-ARS, Arizona;
Nechols, Jim (jnechols@oznet.ksu.edu) – Kansas State University;
Norton, Andrew (Andrew.norton@colostate.edu) – Colorado State University;
Novak, Steve (snovak@boisestate.edu) – Boise State University;
Ode, Paul (paul.ode@colostate) – Colorado State University;
Oishi, Darcy (?) – Hawaii Department of Agriculture;
Ramadan, Mohsen (moshen.m.ramadan@hawwaii.gov) – Hawaii Department of Agriculture;
Schwarzlaender, Mark (markschw@uidaho.edu) – University of Idaho;
Sforza, Rene (rsforza@ars-ebcl.org) – USDA, ARS, EBCL;
Shearer, Peter (peter.shearer@oregonstate.edu) – Oregon State University;
Smith, Lincoln (link.smith@ars.usda.gov) – USDA-EBCL;
Spafford, Helen (hspaffor@hawaii.edu) – University of Hawaii;
Thompson, David (dathomps@nmsu.edu) – New Mexico State University;
Tichenor, Robert (robert.h.tichenor@aphis.usda.gov) – USDA-APHIS-PPQ;
Wager-Page, Shirley (Shirley.a.wager-Page@aphis.usda.gov) – USDA-APHIS-PPQ;
Wright, Mark (markwrig@hawaii.edu) – University of Hawaii;
Goal A: Import and Establish Effective Natural Enemies
Objective 1. Survey indigenous natural enemies.
Surveys for natural enemies of arthropod and weed pests were conducted either in the native home of the pest or within the country of invasion. Examples follow.
Collections were made for the introduction into California of Peristenus digoneutis for biocontrol of Lygus in strawberry fields. Explorations and collections were conducted in French Brittany. Peristenus digoneutis, a parasitoid of Lygus, was sent as cocoons to USDA-ARS, Newark, DE. After emergence in quarantine, the P. digoneutis adults were sent for rearing at the New Jersey Department of Agriculture, Division of Plant Industry. Mite-infested Russian olive branches were collected in Armenia and hand-carried to the quarantine at the CABI Centre in Switzerland. Mite-infested leaves were pinned to leaves of ten test plant species and to Russian olive. While A. angustifoliae was not detected on any of the test plants, mites were found on all inoculated Russian olive shoots. In August/September, surveys were made near the Amurdarya river in the border region of Uzbekistan, Tajikistan and Afghanistan. Particular emphasis was put on assessing the natural enemy complex associated with the fruits of Russian olive. Any adult insect will be collected and stored in a deep-freezer until no further insects hatch, and then sent to taxonomists for identification. A survey was carried out in 2014 in France, Denmark and Sweden to locate and collect western and northern populations of Rhinusa pilosa against Linaria vulgaris (toadflax). A total of 20 galls were collected at one location in central Denmark. The development stage of these galls strongly suggests differences in ecological properties of the northern R. pilosa populations and their potential suitability for more northern areas in North America.
Objective 2. Conduct foreign exploration and ecological studies in native range of pest.
Several institutions in the western US conducted foreign exploration and importation of natural enemies for both new and established arthropod and weed pests this past year. Many of these exploratory trips are only partially successful. Species sent to quarantine facilities must survive the trip and reproduce. Subsequent cultures will then be used for non-target host testing and evaluation for potential release. (See Objectives 1 and 4).
Objective 3. Determine systematics and biogeography of pests and natural enemies.
Systematics studies generate both molecular and morphological data that are essential to distinguishing between biotypes of both pests and natural enemies. These data also provide information about species biogeography, which ultimately helps select the best biological control species.
Using DNA tools it was determined that Bohemian knotweed was the most common taxon of Japanese, giant, and the hybrid Bohemian knotweeds (Fallopia japonica, F. sachalinensis and F. bohemica) which have invaded the western US and Canada. This result is in contrast to earlier reports of F. bohemica being uncommon or non-existent in the US. The abundance and genetic diversity of Bohemian knotweed make it a priority for control in North America. To understand how natural enemies (in this case, lacewing larvae) defend themselves against their own natural enemies, the occurrence and diversity of larval debris-carrying in chrysopid taxa worldwide was assessed. The results show a strong pattern of generic level variation in morphological modifications for debris carrying; each genus has its own, usually distinct, set of features underlying its debris carrying behavior or its nakedness. Higher taxonomic levels show significant variation that is consistent with repeated evolution and loss of larval debris carrying. This comparative study will help biocontrol practitioners select appropriate natural enemies for use in specific ecosystems. From 2005-2008 releases of the northern tamarisk beetle, Diorhabda carinulata, were made in northcentral Kansas but without success. A closely related species, the larger tamarisk beetle, Diorhabda carinata, was observed in southwestern Kansas. This population appears to have hybridized with another species, Diorhabda elongata, both of which occur in northwestern Oklahoma. It is likely that D. carinata/elongata migrated northward into southwestern Kansas following a corridor along the Cimarron River in Oklahoma. In 2014, this population expanded its range in Kansas and is now confirmed in six additional counties. Field-collected tamarisk beetles were released in Cheyenne and Trego counties. A one-year survey of egg parasitoids of adventive Lepidoptera on Oahu was conducted. The egg parasitoid guild composition was compared with previous, briefer, surveys of egg parasitoids.
Objective 4. Determine environmental safety of exotic candidates prior to release.
Many non-target studies and host-specificity tests are underway. Examples follow.
Host specificity testing continued for the Chondrilla crown moth, Oporopsamma wertheimsteini against rush skeletonweed. Two collections of pupae were made in Armenia. No-choice tests are being conducted in Montana and choice cage tests in Bulgaria. Several shipments of the gall mite Aceria drabae were received at the Montana State University quarantine lab from Eastern Europe in 2014, for use against hoarycress. Mites were dead in most of these shipments but a rearing colony was established from two collections. Results of host-specificity tests conducted so far with the seed feeding weevil C. turbatus show that it is the most specific agent investigated. However, because it only reduces seed output of L. draba, it will not contribute to the control of existing stands, but rather reduce the spread of L. draba. The new species, the root-gall forming weevil C. assimilis has been observed to be able to cause major reductions in the growth and vigor of L. draba. Both biocontrol agents of Rhaponcticum repens, i.e. the gall midge Jaapiella ivannikovi and the gall wasp Aulacidea acroptilonica, have established in North America. Both species have successfully overwintered at a number of release sites in different states of the USA. The mite species Aceria acroptiloni is a promising biological control candidate with a very narrow host-range. With approximately 50% of the test plants tested under quarantine conditions, it is expected that two more successful seasons should suffice to complete the host-specificity studies with A. acroptiloni. An important biological control project is to slow down the spread of Russian olive into semi-natural and natural areas by introducing biocontrol agents that reduce the reproductive output of Russian olive, but do not kill the planted trees. Results from host-range and impact studies conducted with the mite Aceria angustifoliae support previous findings, suggesting that this mite is very specific and has significant impact on seed production. Field investigations with Ananarsia eleagnella suggest that this biological control candidate has a narrow host range, but the design of the choice oviposition experiments under field-cage conditions need to be optimized. Molecular work with Rhinusa spp. and Mecinus spp. has confirmed the complex relationship of most toadflax insects with their host plants in Europe and the need to test Rhinusa spp. and Mecinus spp. from L. vulgaris and L. genistifolia separately. Rhinusa pilosa has been recommended for field release for yellow toadflax in the United States by TAG, and was approved for release in Canada in spring 2014. Foreign exploration for natural enemies of French broom in its native range has identified a weevil, Lepidapion argentatum as a potential biocontrol agent. It has two modes of reproducing on G. monspessulana: the female either lays eggs in pods, where larvae feed on developing seeds, or in stems, where larvae develop inside induced galls. In order to evaluate the specificity of this weevil, no-choice tests were performed on growing stems of 17 species, closely related to French broom.
Objective 5. Release, establish and redistribute natural enemies.
Many releases and redistributions of natural enemies (tens of thousands) were carried out against pests in 2014.
The yellow toadflax root-galling weevil Rhinusa linarieae was imported from established populations in British Columbia. This agent is being maintained in lab culture with field releases planned for late spring 2015. This group also mass-reared the yellow toadflax stem weevil Mecinus janthinus. Continued monitoring of these species following field release will allow us to determine if their impact on yellow toadflax populations is sufficient to reduce herbicide applications for this weed pest and to promote a healthy plant community. In Wyoming, a major focus in 2014 was biological control of Russian knapweed using two relatively new agents, a gall wasp and a gall fly. Activities included making releases and checking previous release sites for establishment of both species, and continuing population monitoring for the gall fly. Releases of the gall wasp were conducted at five sites in five Wyoming counties. Whole plants and plant parts of Mikania micrantha were collected from original release sites in Fiji near Suva where the rust, Puccinia spegazzinii, had been originally released and established after importation from Ecuador via Switzerland. Infested plants and plant parts were hand carried to Guam, and attempts were made to infest local M. micrantha with the rust under high temperature and humidity conditions similar to those encountered in the field in Fiji. Only a few Guam plants were successfully infested, and the infestation died after these plants were moved to an outside propagation area. Lab bioassays indicate that the Guam genotype of coconut rhinoceros beetle (CRB) is resistant to all available strains of Oryctes nudivirus (OrNV). Work is currently underway to try and find OrNV, which is pathogenic for Guam CRB. Green muscardine fungus (GMF), Metarhizium majus, produced by the Philippine Coconut Authority, has been released on Guam, and has spread by auto-dissemination to all parts of the island. In cooperation with colleagues at UC Berkeley, the EBCL reared and shipped more than 16,000 Psyttalia lounsburyi wasps to California for field release in support of biological control of olive fruit fly in California olives.
Objective 6. Evaluate natural enemy efficacy and study ecological/physiological basis for interactions.
The coccinelid, Rhyzobius lophanthae, introduced to Guam in 2005, continues to be ubiquitous and control Cycad Aulacaspis Scale (CAS) on mature plants. But it does not protect seedlings. An Arrhenophagus sp., was discovered infesting male CAS. This is considered to be a fortuitous introduction. Because this parasitoid only attacks male scales, minimal impact on the CAS population was expected. However, 2 years after initial detection, these parasitoids are numerous and there appears to be a significant reduction in the severity of the scale infestation. Additional introductions of CAS natural enemies are being investigated to complement predation by R. lophanthae. The chrysopid, Pseudomallada, is considered a valuable source of biocontrol agents for use in European agriculture. A study evaluated the seasonal cycles of three US species and compared them with information from a variety of European species. Results indicate that the US species can be reared and may be useful for biological control in certain situations. The establishment and effectiveness of Aceria malherbae has been reported to vary across western North America, with genetic variation of field bindweed as a possible contributing factor. Four field bindweed populations, collected from Montana, California, Oregon, and New Mexico, were exposed to A. malherbae to determine if growth parameters conducive or detrimental to the development of the mite. When grown in a common environment, plant height, stem length, and number of branches and leaves significantly varied among bindweed populations although biomass did not differ. Galling by A. malherbae was lower on plants from New Mexico than Oregon. Field studies assessed the relationship between habitat characteristics and plant cover of bindweed infestations and the presence and abundance of A. malherbae. Multidimensional scaling of site characteristics indicated a spatial relationship, though no habitat relationship, among established A. malherbae populations. In within-field studies, a significant positive relationship was observed between percent grass cover and mite abundance and a negative relationship between field bindweed and mite abundance. Fields of small grains (wheat, barley, and oats) in northern Utah were sampled weekly throughout the growing season to determine the phenology of rates of parasitism of the cereal leaf beetle by the parasitoid Tetrastichus julis (Eulophidae) in relation to cereal leaf beetle larval phenology. Evaluation of biocontrol of erythrina gall wasps (Quadrastichus erythrinae) continued. Significant positive impacts of parasitoid (Eurytoma erythrinae) on foliage recovery in the trees was demonstrated.
Goal B: Conserve Natural Enemies to Increase Biological Control of Target Pests.
Objective 7. Characterize and identify pest and natural enemy communities and their interactions.
Geographic populations of Chrysoperla rufilabris, from KS, TX, and GA were evaluated at different temperatures and photoperiods to determine environmental factors that induce reproductive diapause, and to assess whether geographic differences exist. Results suggest that C. rufilabris adults do not respond to constant daylengths at 25 degrees C as the percentage diapause was similar under long and short photoperiods. However, subjecting the insects to a decrease in daylength during late-larval or adult stages induced a higher percentage of diapause compared to fixed photoperiods. Rearing lacewings under a lower temperature (20 degrees C) increased the incidence of diapause in those experiencing a decrease in photoperiod, and the largest percentage of adults entered reproductive diapause if they experienced both a decrease in temperature and photoperiod. A strict symbiosis between Lasioptera donacis and a fungus, which has already been demonstrated in other Lasioptera species, was hypothesized. Evidence of a close association of the leaf sheath miner with one particular fungal taxa and the characterization of this taxa was carried out by the genetic Unit at EBCL. Field, nursery trials and laboratory bioassays were conducted to better understand the relationship between the plant (A. donax), the midge (L. donacis) and A. arundinis, and to obtain the crucial biological information to evaluate the host range of L. donacis. The evolutionary history of Anagyrus sp. pseudococci was explored within the context of the applied use in a biocontrol program against the vine mealybug, Planococcus ficus, an invasive insect found in California. As A. pseudococci are natively found throughout the Mediterranean basin, parasitoid ecotypes from France, Spain, and Portugal were chosen to compare parasitism success. Parameters used to determine efficiency as a biocontrol agent were parasitoid egg load, host handling time, host encounters, and parasitoid effectiveness was measured with host encapsulation rate. There was no difference in the first three measures, although host encapsulation rate did significantly differ between ecotypes. This suggests a lower co-evolutionary host-parasitoid relationship for certain ecotypes than other, as more distantly co-evolved parasitoids are more effective at parasitizing hosts.
Objective 8. Identify and assess factors potentially disruptive to biological control.
Surveys continued for invasive ants on the islands of Guam, Saipan, Tinian, and Rota in the Mariana Islands during 2014. This activity is part of an ongoing project on the surveillance of Wasmannia auropunctata and Solenopsis invicta. A related study seeks to describe attendance behavior of Guam’s invasive ants towards aphids, scales and mealybugs commonly encountered in the Marianas, and the effects this might have on biological control agents against hemipteran plant pests. A series of controlled laboratory studies were completed to measure potential impacts of transgenic Bt crops on a range of natural enemy species (Chrysoperla, Geocoris, Orius, Zelus, Cotesia). Protocols involve tri-trophic exposure scenarios in which the prey or host are fed on Bt crops and then exposed to predators or parasitoids. To control for prey or host quality mediated effects, Bt resistance and susceptible prey and hosts were employed. Results have uniformly shown neutral effects of Bt proteins on multiple biological parameters of these natural enemies. Grazing at some field sites significantly decrease the number of Jaapiella and Aulacidea gall. Parasitism of Aulacidea was as low in 2014, although additional parasitoid species were observed. No parasitism of Jaapiella was observed in 2014. The disruptive effects of insecticide application on biocontrol of the cereal leaf beetle were identified from when insecticides are commonly applied during the growing season in relation to the phenology of parasitoid and its parasitism by T. julis. Degree day models were developed to describe the phenology of the beetle and wasp populations and guide growers on when during the growing season to apply insecticides (if needed) to minimize disruption of biological control.
Factors that modulate the expression of cannibalism by Geocoris pallens (“big-eyed bugs”) were studied. Cannibalism appears to be a key factor disrupting the ability of G. pallens to control Lygus hesperus and Tetranychus spp. spider mites in cotton. The possibility that a pathogen is spreading through Geocoris pallens populations, and may be responsible for significant declines in Geocoris population densities is being studied. It was determined that the endosymbiont Wolbachia is not a pathogen, but rather increases the reproductive success of the parasitoid wasp Anagrus sophiae. The reproductive success of Anagrus erythroneurae and Anagrus daanei, two major parasitoids of leafhoppers in grape vineyards, is sometimes constrained by their finite supply of mature eggs (“egg limitation”). Furthermore, in many cases, the longevity of these Anagrus spp. is limited in the field by lack of access to floral nectar.
Objective 9. Implement and evaluate habitat modification, horticultural practices, and pest suppression tactics to conserve natural enemy activity.
Large plot field studies were conducted to validate biological control based thresholds for managing Bemisia tabaci in cotton. In 2014, studies expanded to commercial growers in AZ and Mexico. An extensive education and outreach effort accompanied the research program to train growers and PCAs on natural enemy identification and use of the new thresholds. Analyses are underway. Landscape-scale census studies are being used to understand the source-sink relationships of predator communities among cotton and surrounding crops. To determine the effects of sub-lethal herbicide applications on gall induction and development of Aceria malherbae (against bindweed), a bioassay was conducted with four herbicides, each having different modes of action. Atrazine, glyphosate, imazapic, and picloram were applied at 25% of their recommended dosages on plants infested and not infested with A. malherbae. Sub-lethal herbicide applications had an adverse effect on plant stem height, total stem length, numbers of leaves or branches, or on above- ground or below-ground biomass; whereas A. malherbae did not. Synergistic impacts of herbicide applications and A. malherbae on growth parameters of field bindweed were not observed. Pre- and post-spray gall counts were not significantly different indicating that gall induction and development was not altered by these sub-lethal dosages. A study on the effect of intercropping cover crops such as sunn hemp with corn to encourage natural enemies of Thysanoptera and Helicoverpa zea, was conducted and compared to conservation biocontrol with augmentative releases of Trichogramma pretiosum. The study showed that sunn hemp intercropping increased Trichogramma parasitism of H. zea eggs significantly, but the impact on the pest and corn yield was lower than using augmentative releases of Trichogramma. Abundance was enhanced by intercropping with sunn hemp.
Goal C: Augment Natural Enemies to Increase Biological Control Efficacy.
Objective 10. Assess biological characteristics of natural enemies.
Results have been reported under other objectives.
Objective 11. Develop procedures for rearing, storing, quality control and release of natural enemies, and conduct experimental releases to assess feasibility.
Results have been reported under other objectives.
Objective 12. Implement augmentation programs and evaluate efficacy of natural enemies.
Results have been reported under other objectives.
Goal D: Evaluate Environmental and Economic Impacts and Raise Public Awareness of Biological Control.
Objective 13. Evaluate the environmental and economic impacts of biological control agents.
A synthesis on the economic evaluation of biological control was completed for the Annual Review of Entomology. The focus was to assess the economics of arthropod biological control by arthropod natural enemies in managed plant systems. Analytical approaches useful for valuing biological control were examined, the authors updated the record of progress in economic evaluation of classical and augmentative biological control, and then focused on the economics of conservation biological control, which has received the least attention and for which methodology and concepts are still developing. They provided a conceptual transect that highlights the methods that can be brought to bear on valuing biological control along the spectrum from individual growers to society as a whole and close with a call to arms that highlights the constraints, challenges, and opportunities for assessing the economics of biological control to advance IPM.
Objective 14. Develop and implement outreach activities for biological control programs.
In March 2014 approximately 30 quarantine personnel from the CNMI, the Republic of Palau, the Republic of the Marshall Islands, and the Federated States of Micronesia, and Guam were trained in the importance of natural enemies in regulating populations of invasive insect pests in Micronesia, with special recognition of the potential impact of Hemiptera and ants if not intercepted or detected at or shortly after introduction to the islands. Regulations for importing natural enemies and prohibiting the entry of potential pests were discussed, along with methods for inspection and enforcement of regulations. This activity was the 12th of its kind hosted by the University of Guam and sponsored jointly by the Secretariat of the Pacific Commission, the Guam Department of Agriculture, and USDA-APHIS. A series of brief one-page Extension Circulars were developed to highlight the importance and application of biological control in the cotton system (many of which were also translated into Spanish). They were distributed widely to growers, pest control advisor, county extension personnel and other industry representatives in AZ and Mexico in 2013 and 2014. They were also posted on the Arizona Crop Information Site (http://ag.arizona.edu/crops/). Work was completed on an extensive Extension bulletin on natural enemies in Arizona, California, New Mexico and Texas field crops
- The level of competence of APHIS-PPQ workers, port inspectors, and customs officials within Micronesia is gradually being raised as more personnel are trained in annual PPQ workshops. Increased participation by Guam Customs officers appears to reflect heightened awareness of the threat to Guam posed by invasive species and the increased cargo and human traffic resulting from the ongoing military buildup.
- Entomopathogenic fungi and nematodes were evaluated against the wheat stem sawfly, Cephus cinctus. These treatments were effective in reducing the damage caused by C. cinctus and yield levels were significantly increased the plots treated with biologicals versus control plots.
- Conservation of natural enemies is a key component in cotton management systems and research has provided methods for quantifying and deploying biological control for developing IPM systems that maximize the effects of natural enemies in pest population control and regulation.
- An extensive Extension outreach program has educated growers and pest control advisors in AZ and Mexico on the value and utility of biological control for pest suppression in cotton.
A synthesis was completed to document the economic value of biological control in managed plant system, including novel focus on conservation biological control. This work should help to increase the visibility and merit of biological control to multiple stakeholders included those who make funding decisions to spur needed innovations in IPM.
- Approximately 26,000 Aulacidea acroptilonica were redistributed to field sites in CA, CO, ID, MT, NV, OR, and WY to combact Russian knapweed. The gall wasp is now established and increasing in population at least eight sites in Montana. The gall midge Jaapiella ivannokovi is also well established in Montana with populations ranging up to 1.3 million galls at some establishments.
- New agents are being investigated for the biological control of Russian knapweed, hoarycress, invasive hawkweeds, and rush skeletonweed. The target weeds have either no biological control agents currently available or the agents already established are not effective over the range of the target weed. In addition, a better understanding of biological control and its implementation will be achieved by monitoring the impacts associated with these biological control agents. In particular the habitat specificity of these arthropods may delineate their potential range or effectiveness.
- Degree-day models can be used to assist growers in determining when best during a given spring to sample for cereal leaf beetle eggs and young larvae to assess the likelihood of subsequent need for insecticide application to individual fields. In those cases where insecticide application to a particular field is warranted, the degree day models can also assist growers in selecting when during the growing season to apply the insecticide so as to minimize adverse effect on biological control (i.e., to minimize inadvertent killing of wasps along with their hosts).
- It is expected that Diorhabda beetles will have a significant impact on the reduction of saltcedar in riparian areas of Western Kansas similar to what has been recorded in other High Plains areas where these biological control agents have been established for longer periods.
- An understanding of factors controlling diapause induction in Chrysoperla rufilabris will allow better predictions of the seasonal occurrence and population growth of this natural predator of several soft-bodied pests.
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Asiimwe, P., S. E. Naranjo & P. C. Ellsworth. 2014. Effects of irrigation regime on interactions between Lygus hesperus, insecticides and predators in cotton. Environ. Entomol. 43:263-273.
Augé M., Le Bourgeois T., Liégeois M., & RFH Sforza 2014. Cows and insects helping out to control the weediness of leafy spurge in France. pp173-180. Proceedings of the XIV International Symposium on Biological Control of Weeds, pp 159-166.
Benelli, G. Daane, K. M., Canale, A., Niu, C.Y., Messing, R. H., Vargas, R. I. 2014. Sexual communication and related behaviours in Tephritidae – current knowledge and potential applications for Integrated Pest Management. Journal of Pest Science 87:385-405. DOI 10.1007/s10340-014-0577-3
Benelli, G. G., C. Stefanini, G. Giunti, S. Geri, R. H. Messing & A. Canale. 2014. Associative learning for danger avoidance nullifies innate positive chemotaxis to host olfactory stimuli in a parasitic wasp. Naturewissenschaften 101: 753–757.
Benelli, G. G., G. Giunti, A. Canale & R. H. Messing. 2014. Lek dynamics and cues evoking mating behavior in tephritid flies infesting soft fruits: implications for behavior-based control tools. Applied Entomology and Zoology, 49: 363-373.
Benelli, G. G., N. G. Kavallieratos, E. Donati, M. Mencattelli, G. Bonsignori, C. Stefanini, A. Canale & R. H. Messing. 2014. May the wild male loose? Male wing fanning performance and mating success in wild and mass-reared strains of the aphid parasitoid Aphidius colemani Viereck. BioControl 59:487–500.
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