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Home , Aulacorthum solani, Binodoxys communis, Soybean aphid

Chapter 12 93

12 Aphis glycines Matsumura, (: )

Jacques Brodeur Université de Montréal, Montréal, Québec

12.1 Status al., 2011 and references therein). The yield of soybean declined with the density of The soybean aphid, Aphis glycines per plant, and plants are Matsumura (Hemiptera: Aphididae), is a particularly susceptible to aphid injury multivoltine native to . In when infested at an early growth stage. it was fi rst detected in Aphid feeding can lead to a decrease in , USA in 2000 and rapidly spread plant growth, resulting in reduced pod set, through the continent (Venette and Rags- fewer and smaller seeds within pods at dale, 2004). Surveys of soybean, Glycine maturity and a decrease in protein and oil max (L.) Merr. (Fabaceae), fi elds in Ontario content. Aphis glycines also can transmit a and Quebec in 2001 revealed the presence number of plant-pathogenic to of the aphid in Canada (Brodeur et al., soybean, but outbreaks have not 2003; Hunt et al., 2003). The establishment occurred so far. However, A. glycines has of A. glycines in Canada represents a caused signifi cant virus epidemics in other spectacular example of biological invasion. crops, e.g. snap bean, Phaseolus vulgaris L. By 2002, all soybean-growing regions in (Fabaceae), potato, Solanum tuberosum L. Quebec were infested, and 51 of 54 (Solanaceae), squash, Cucurbita spp. sampled fields were colonized by A. (), during aphid dispersal. glycines (Brodeur et al., 2003). The aphid Growers now have to routinely budget for has rapidly colonized all US states and aphid scouting and, under some circum- Canadian provinces, e.g. Manitoba, Ontario, stances, application of to Quebec, where soybean is produced remain profi table. The introduction of A. (Ragsdale et al., 2011) and is causing glycines also has major consequences to profound changes in the agroecosystem the environment as can lead to (Heimpel et al., 2004). For instance, the A. applications over a vast area of glycines invasion has led to an increase in agricultural land that was previously densities of predators, thus putting untreated. For example, following a severe other at risk through indirect A. glycines outbreak in 2007, 57% of the effects, such as apparent competition. soybean grown in Quebec that was insured The introduction of A. glycines into was treated with insecticides (Financière Canada poses a serious threat to soybean Agricole du Québec, 2007). production and the environment. The aphid Aphis glycines is a holocyclic and can severely reduce the yield of soybean, heteroecious species, alternating from pri- either directly through its feeding activity mary (buckthorn; spp. (Rhamna- or indirectly through the transmission of ceae)) to secondary (soybean; G. max) viral diseases (see review by Ragsdale et hosts. Unfortunately, the establishment in © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 94 Chapter 12

North America of this exotic aphid was fi ed as resistant or mostly resistant, mainly made possible by the prior and intentional through and antixenosis mech- introduction of its two host plants: buck- anisms. Resistant varieties have been thorn from northern Europe and soybean commercialized since 2009. from Asia. In spring, on buckthorn, A. As aphid populations increase in glycines nymphs hatch from overwintering abundance and disperse, they trigger eggs and develop into parthenogenetic import ant functional and numerical re- fundatrices. After a few generations on the sponses by native and naturalized primary host, winged morphs emigrate to generalist predators. In Quebec, Mignault cultivated soybean where many over- et al. (2006) and Firlej et al. (2012) lapping generations occur throughout the characterized the species composition of summer. In autumn, winged females, called the foliar and ground fauna, respectively, gynoparae, and males are produced and associated with A. glycines in commercial emigrate on to buckthorn where they feed. soybean fi elds. (Coleoptera) Gynoparae produce nymphs that develop were the most abundant aphidophagous into oviparae, mate with males and deposit predators in sweep samples in 2002 overwintering eggs on Rhamnus spp. Aphis (58.6%) and 2003 (44.8%), with one native glycines has a great capacity to disperse species, lengi within and between fi elds as winged Timberlake, and three naturalized species, morphs are produced throughout the grow- (Pallas), Coccinella ing season. Winged morphs can disperse septempunctata L. and Propylea quatuor- between plants or enter low-level jet decimpunctata L., co-occurring with the streams and migrate over great distances soybean aphid throughout the growing (Rhainds et al., 2008; Zhang et al., 2008). season (Mignault et al., 2006). Carabidae (Coleoptera) beetles were the most com- mon ground predators captured in pitfall 12.2 Background traps. A total of 33 species from 15 genera were identifi ed, with the exotic Ptero- Aphis glycines was fi rst managed by foliar stichus melanarius (Illiger) represent ing applications of non-selective 75.8% and 84.5% of all individuals and insecticides (dim- trapped in 2004 and 2005, respectively ethoate and Lambda-cyhalotrin) during (Firlej et al., 2012). outbreaks according to decision thresholds, Mortality caused by generalist predators crop maturity and abundance of natural has been repeatedly shown to limit the enemies. More recently, growers have economic impact of A. glycines in Asia and started to use insecticides North America (reviewed by Ragsdale et (Thiamethoxame) applied as seed treat- al., 2011). In Quebec, Rhainds et al. (2007) ments (Magalhaes et al., 2008). This underlined the collective impact of preda- practice is controversial because aphid tors to regulate A. glycines populations, as population densities do not commonly indicated by the relatively low abundance reach the economic thresholds and because of aphids on plants experimentally infested the effi cacy of such systemic insecticides with aphids in comparison with control decreases with time and is likely not (caged) plants. The impact of carabid suffi cient to control A. glycines infestations beetles on A. glycines populations is less when they occur late in the season obvious than for foliar predators. There (Johnson et al., 2008). was no relationship between carabid trap The introduction of A. glycines into catches and A. glycines density, suggesting North America prompted intense research that carabid beetles do not respond in the development of soybean varieties numerically to soybean aphid populations resistant to aphid (Hill et al., at the spatial scale (Firlej et al., 2012). 2006; Kim et al., 2010). More than two However, using molecular gut-content dozen soybean varieties have been identi- analysis, Firlej et al. (2013) showed that a Chapter 12 95 signifi cant proportion of P. melanarius, the 12.3 Biological Control Agents dominant carabid species in soybean fi elds, typically feed on A. glycines early in the In Canada, in addition to the on-going season when aphid densities are very low. ecological studies on generalist predators As reported in other studies (Holland and attacking A. glycines in soybean fi elds, the Thomas, 1997; Winder et al., 2005), the possibility of introducing exotic parasit- authors hypothesized that carabids are oids to strengthen the complex of natural unlikely to prevent large A. glycines enemies is being evaluated. A classical infestations but they can limit population biological control programme was initiated growth rate under low aphid density. in the USA in 2001, the year following the The benefi cial impact of generalist discovery of A. glycines in North America. predators appears consistent across a wide After exploration in Asia, host specifi city range of soybean management systems studies and experiments to assess potential (Costamagna and Landis, 2006), although effi cacy as biological control agent of A. their effectiveness is infl uenced by the glycines, communis (Gahan) abundance of A. glycines (Costamagna and (: Bracon idae) was identifi ed Landis, 2007), the landscape structure and as a promising candidate and a permit from spatial distribution of aphid populations Department of Agriculture- (Desneux et al., 2006), within-fi eld man- and Plant Health Inspection agement practices (Ragsdale et al., 2011) Service was granted for fi eld release in the and high levels of intraguild USA (Wyckhuys et al., 2007). Releases of (Gagnon et al., 2011). This ecological B. communis began in 2007 in the north- context suggests a cautious approach central USA, with approval to conduct toward the introduction of exotic biological laboratory studies in Canada following in control agents and the promotion of 2009. measures to preserve or enhance predator populations, such as limiting the use of pesticides in soybean fi elds. In Asia, and entomopatho- 12.4 Evaluation of Biological Control genic fungi complete the typical guild of aphid natural enemies attacking A. Binodoxys communis has so far failed to glycines (Han, 1997). Although a total of establish in North America following seven hymenopteran parasitoids have been multiple releases (Ragsdale et al., 2011) reported attacking A. glycines in North and several nonexclusive explanations may America, parasitism levels have been so far account for this failure: low dispersal very low (see Ragsdale et al., 2011). How- ability, genetic bottlenecks and Allee ever, recent surveys indicated that effects in released populations, parasitoids are now gradually responding and intraguild predation (Ragsdale et al., more to the invasion of soybean fi elds by 2011). Furthermore, Gariepy (2011) A. glycines (Noma and Brewer, 2008; recently showed under laboratory and fi eld Heimpel et al., 2010), with the exotic conditions that the Chinese B. communis certus Yasnosh (Hymenoptera: strain tested by our US colleagues has a Aphelinidae) now being the dominant very poor capacity to enter into diapause soybean aphid parasitoid in soybean- (<0.8%) and thus to overwinter in North producing regions of Ontario (>90% of America. It was hypothesized that the B. soybean fields surveyed; Frewin et al., communis strain has gradually lost its 2010) and Quebec (Gariepy, 2011). Seven ability to enter diapause during the species of entomopathogenic fungi have extended periods of quarantine and labora- been observed infecting A. glycines in New tory confi nement during which it was York state (Nielsen and Hajek, 2005), but continuously exposed to non-diapause information about their contribution to rearing conditions. New foreign explor- pest population regulation remains limited. ations have been conducted to recover 96 Chapter 12 natural B. communis strains that can enter 12.5 Future Needs diapause. Since its invasion of North America, A. Future research to manage A. glycines glycines has acquired pest status and has infestations through biological control dramatically changed the should focus on: community of the soybean agroecosystem. In the USA, but to a much lesser extent in 1. A better understanding of the degree of Canada, efforts have been devoted towards seasonal synchrony between A. glycines classical biological control by introducing and its complex of natural enemies, espe- parasitoids of A. glycines from Asia. cially early in the growing season when However, the knowledge acquired over the soybean plants are more sensitive to feed- last decade on the ecology of A. glycines in ing injury; North America should lead to a 2. A quantitative description of the evolu- reconsideration of the need to continue a tion of parasitism and disease (fungal) classical biological control programme for infection through time and an evaluation of A. glycines. First, several studies showed the contribution of aphid parasitoids and that generalist predators may suppress disease to A. glycines control; soybean aphid populations and mitigate 3. A strategy to integrate biological control their impact on soybean plants. Second, into pest management programmes, with recent surveys indicated that aphid an estimation of how chemical seed treat- parasitoids, mainly A. certus, are becoming ment and plant resistance may impact the more and more common in soybean fi elds effi cacy of natural enemies; and could in the near future play the role 4. The infl uence of landscape structure, we would expect from classical biological agronomic practices and climate on levels control agents. Furthermore, the potential of aphid infestation, predation, parasitism risks to non-target organisms posed by and fungal infection; exotic species introduced for biological 5. The need to introduce exotic natural control are an important concern for enemies to supplement the actions of Canadian regulatory authorities. native and naturalized species.

References

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13 Aphis gossypii Glover, Melon/Cotton Aphid, solani (Kaltenbach), Foxglove Aphid, and Other Arthropod Pests in Greenhouse Crops

Rosemarije Buitenhuis,1 Graeme Murphy2 and Les Shipp3 1Vineland Research and Innovation Centre, Vineland Station, Ontario; 2Ontario Ministry of Agriculture, Food and Rural Affairs, Vineland Station, Ontario; 3Agriculture and Agri-Food Canada, Harrow, Ontario

13.1 Pest Status 13.1.1 Aphids

Greenhouse crops, both vegetables and Melon/cotton aphid, Aphis gossypii Glover, ornamentals, are attacked by various insect foxglove aphid, Aulacorthum solani and mite pests that can cause signifi cant (Kaltenbach), potato aphid, Macrosiphum losses if not controlled. The year-round euphorbiae (Thomas) and green peach nature and controlled climate of the green- aphid, Myzus persicae (Sulzer) (Hemiptera: house industry result in pest pressures that Aphididae), are all serious pests of a wide can cause signifi cant economic damage at range of greenhouse vegetable and orna- any time of the year. For vegetable crops, mental crops. Chrysanthemum aphids, such damage can translate into yield Macrosiphoniella sanborni (Gillette) losses; for ornamental crops, even low (Hemiptera: Aphididae), are pests of levels of pests and/or damage can detract chrysanthemums, Chrysanthemum spp. from crop quality and cause heavy fi nan- (Asteraceae). Aphid damage is mostly cial losses. The composition of the pest related to the deposits of honeydew, which complex can vary depending on the crop promotes the development of sooty species, but a number of arthropod pests moulds, the presence of the aphids are common across a broad range of both themselves and their cast-off skins. Aphids ornamental and vegetable greenhouse in greenhouses also transmit plant viruses crops. such as Cucumber mosaic virus (Bromo-

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie)