Pea Aphid Outbreaks and Virus Epidemics on Peas in the US Pacific Northwest: Histories, Mysteries, and Challenges

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1 2006 Plant Management Network. This article is in the public domain. Accepted for publication 3 August Published. Pea Aphid Outbreaks and Virus Epidemics on Peas in the US Pacific Northwest: Histories, Mysteries, and Challenges Stephen L. Clement, Research Entomologist, USDA-ARS, Plant Germplasm Introduction and Testing Research Unit, 59 Johnson Hall, Washington State University, Pullman Corresponding author: Stephen L. Clement. slclement@wsu.edu Clement, S. L Pea aphid outbreaks and virus epidemics on peas in the US Pacific Northwest: Histories, mysteries, and challenges. Online. Plant Health Progress doi: /php rv. Introduction The pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), adversely affects the health and vigor of peas, Pisum sativum L., in the US Pacific Northwest by sucking sap from leaves, stems, and pods (Fig. 1) and by transmitting viruses (Fig. 2) (6,14,21,31). These viruses are transmitted persistently [genus Enamovirus, Pea enation mosaic virus (PEMV); genus Luteovirus, Bean leaf roll virus (BLRV)] and non-persistently [genus Alfamovirus, Alfalfa mosaic virus (AMV); genus Carlavirus, Pea streak virus (PeSV)] by the pea aphid (20). In eastern Washington, for example, field peas are devastated by pea aphid feeding damage and legume viruses during periodic pea aphid outbreak years (6,24). When massive pea aphid flights arrive in this region without warning, pea producers are caught off guard and cannot implement timely control measures (6). Fig. 1. Pea aphids feeding on field peas, Pullman, WA, June 2006 (photo by L. R. Elberson). Fig. 2. Field peas showing virus symptoms (possibly pea enation mosaic virus and bean leaf roll virus), Grangeville, ID, July 2005 (photo courtesy of S. Eigenbrode). This review documents the history of pea aphid outbreaks and epidemics of pea aphid-transmitted viruses on peas in the Pacific Northwest, with emphasis on outbreaks and epidemics in the Palouse region of eastern Washington (Fig. 3) over 23 years (1983 to 2005). Outbreaks and epidemics in the Palouse are documented using an index (Fig. 4) incorporating pea aphid population estimates and viral symptom developments on plants in commercial pea fields. Secondly, our understanding of pea aphid-host plant-virus relationships is reviewed to gather clues on the possible sources of winged and viruliferous aphids that colonize pea fields in the spring and early summer in the Palouse region. The most important virus disease of Palouse field peas is PEMV (21), however, the source of pea aphids and PEMV that adversely affect these peas is a mystery, although alfalfa (Medicago sativa L.) is the likely reservoir of other pea aphid-transmitted viruses and the source of aphids that colonize peas in other Pacific Northwest areas (8,11,15,16,17,25). Thirdly, this article examines various

2 factors and their possible controlling influence on changes in pea aphid densities, with special attention to winter temperatures. Mild winters have been historically linked to widespread spring and early summer outbreaks in Oregon and Washington (8,11,18,27). And, as the author can attest, many present-day pea producers and pest managers in the Palouse associate pea aphid problems with mild winters. Finally, this article will enable researchers and industry leaders to target resources to areas requiring more research for better understanding of pea aphid-host plant-virus relationships in the Pacific Northwest. Fig. 3. Map showing locations of pea aphid outbreaks and virus epidemics, , on peas and other legumes in western Oregon (no. 1), the Blue Mountain region of eastern Oregon and Washington (no. 2), southern Idaho (no. 3), and the Palouse region of eastern Washington (no. 4). Fig. 4. Twenty-three year history of pea aphid outbreaks and virus epidemics on field peas in the Palouse region of eastern Washington. Values for were extrapolated from published accounts and personal observations of researchers. For 1987 to 2005, index values of 3 to 4 reflect outbreakepidemic years (arrows [ ] show all outbreak years). Defining a Pea Aphid Outbreak and Virus Epidemic Rockwood and Reeher (27) defined spring pea aphid outbreaks in western Oregon (Fig. 3, no. 1) as "the occurrence of countless millions of aphids and observable aphid damage in many fields over a wide area." In other studies,

3 discussed and referenced herein, the term "outbreak" was associated with the appearance of destructive and high temporal densities of pea aphids (8,11), or not defined at all. In this paper, an outbreak, modified from Berryman (2), is the relatively sudden appearance and widespread distribution of very high densities of the pea aphid on field peas. My perception of a virus epidemic on peas, based on plant pathology parlance in papers cited herein, is an explosive increase in symptomatic plants, coupled with significant economic impact. Pea Aphid Sampling and Outbreak-Epidemic Index Aphid densities were recorded every 7 to 21 days from 15 May to 7 July, , by visually counting the number of aphids on 10 to 30 plants in a commercial field. All fields were in Whitman County, WA, and within 30 km of Pullman ( "N, "W). This calendar sampling period coincided with the major developmental period of the commercial pea crop in eastern Washington, covering the late vegetative (internode expansion) stage and up through the flowering and pod-filling stages (F. Muehlbauer, personal communication). Intervals between sampling days were shortened when aphid counts started to average 5 per plant in late May and early June. A variable number of unsprayed fields (5 to 25) were sampled each year, with 5 fields surveyed in years when I observed zero or very few aphids and no plant virus symptoms by mid-june. In each field, plants were selected every 1 to 2 m along well-spaced transects (1 to 4 per field) and aphids were counted on each plant for 1 to 2 min. This "quick in situ aphid count" method, which generated relative estimates of pea aphid densities during the major part of the field pea growing season, was sufficient to pinpoint the onset and duration of pea aphid infestations, including outbreak densities. When aphids were counted, any symptoms of pea aphid-transmitted viruses were recorded (plant stunting, chlorosis, enations, chlorotic islands, or windows on leaves) (14,24). No attempt was made to distinguish on the basis of symptoms between the four pea aphid-transmitted viruses that can potentially cause losses in peas and other grain legumes in eastern Washington. Virus infection was not confirmed using enzyme-linked immunosorbent assay or other molecular techniques. The outbreak-epidemic index (Fig. 4) was devised using aphid counts and observations on relative incidence of virus symptomatic plants in sampled fields (1987 to 2005) where an index value of 0 approaching 1 = aphids absent or "few" counted on plants and no virus symptoms detected in all sampled fields; 1 approaching 2 = high counts (mean of 10 to 99 aphids per plant), coincident with few virus symptoms, in 26 to 50% of the fields; 2 approaching 3 = very high counts (averaging >100 aphids per plant) and obvious virus symptoms in 51 to 75% of the fields; and 3 approaching 4 = counts averaging >100 aphids per plant and >50% of the plants exhibiting advanced virus symptoms in 76 to 100% of the fields. Index values of 3 to 4 signify an outbreak and epidemic. Additional support for selecting these index values to denote outbreaks and epidemics comes from observations that only large numbers of pea aphids are associated with severe virus infections in peas (25). The following counts in 2005 are illustrative of the sudden onset of high aphid densities on Palouse field peas during outbreak years: average of 12 to 16 pea aphids per plant per field (7 fields) on 4 June, rising to 75 aphids per plant in 4 of the 6 fields on 11 June, and culminating with an index value of 3-4 on 18 June when aphid counts averaged >100 per plant in 5 of the 6 fields. The values for 1983 to 1986 in Fig. 4 are not directly derived from this index but are reasonable representations of the presence (1983) (14,22) and absence (1984 to 1986) (F. Muehlbauer, personal communication) of outbreaks and epidemics in the Palouse region. History of Outbreaks and Epidemics The first pea aphid outbreaks in the Pacific Northwest were reported by Rockwood and Reeher (27), who documented spring outbreaks in and eight more between 1919 and 1942 on fall-sown annual legumes (Austrian winter peas, Pisum sativum L. ssp. arvense, and common vetch, Vicia sativa L.)

4 in western Oregon (Fig. 3, no. 1). In the Blue Mountain region of eastern Washington and eastern Oregon (Fig. 3, no. 2), pea aphid outbreak numbers were first noted in 1934 on spring (green) peas cultivated for the canning industry. This infant industry, started in spring 1933, was almost destroyed by this outbreak (8,11). In the Palouse region of eastern Washington (Fig. 3, no. 4), where spring peas are cultivated mainly for dry seed (field peas) production (26), high year-to-year fluctuations in pea aphid densities occurred on this crop between 1983 and 2005 (Fig. 4). During aphid outbreak years (1983, 1990, 1996, and 2005) (Fig. 4) in this region, field peas and other grain legume crops were devastated by damage due to aphid feeding and virus infection [(6,14,21) and F. Muehlbauer, personal communication). With the exception of 1999, when commercial pea fields were devoid of pea aphids, there were always some Palouse fields supporting pea aphid populations in non-outbreak years (reflected by index values of 1 to 2 for 18 years) (Fig. 4). The predominant identifiable viruses causing the 1983 and 1990 epidemics in the Palouse region were PEMV and BLRV (14,21,22), whereas PEMV was responsible for a 1954 virus epidemic on green peas in the Blue Mountain region (25). Likewise, PEMV was responsible for the 1996 and 2005 epidemics in the Palouse (F. Muehlbauer, personal communication). Additionally, major BLRV and PeSV epidemics on Pacific Northwest peas have been associated with large migratory flights of the pea aphid, with the 1980 BLRV epidemic on peas in southern Idaho (Fig. 3, no. 3) the best documented example (15,16,17). Pea Aphid-Host-Virus Relationships The pea aphid overwinters exclusively as diapausing eggs on perennial plants such as clover and alfalfa in northern areas like Canada, England, and Sweden (3,4,9,28). In the Pacific Northwest this aphid overwinters in the egg stage on alfalfa and other perennial legumes, or as summer forms (nymphs, adults) on perennial legumes in warmer areas or protected places (8,10,18,19,25). The aphid could potentially overwinter as summer forms in Pacific Northwest regions experiencing mild winters, as Eichmann and Webster (11) discovered when they "found it in small numbers in alfalfa at Pullman, WA, during each month of the mild winter of 1937 to 1938." Although high survival of overwintering eggs and summer forms on alfalfa have led to aphid outbreaks on spring peas in the Blue Mountain region (8), this aspect of pea aphid biology has not been investigated in other Pacific Northwest regions. Interestingly, entomologists (3) have questioned the value of using winter egg populations to assess the potential for subsequent pea aphid outbreaks and problems on peas because it is very difficult to find overwintering eggs on perennial legumes, let alone quantifying their densities. Blue Mountain alfalfa fields are the source of migrating pea aphids that colonize spring peas in this region in April and May (8,11,25). Likewise, pea aphids move from alfalfa to peas in southern Idaho (15,16,17). By contrast, the actual source of aphids that appear in the spring and early summer on field peas in the Palouse region is unknown, although it is assumed they originate from alfalfa and other perennial legumes (16,18). If we accept a role for alfalfa and other perennial legumes in subsequent pea aphid-field pea-virus relationships on the Palouse, we need to pinpoint the geographical locations of these legumes. Perhaps alfalfa fields or other perennial legumes in the Blue Mountain region and other localities 60 to 120 km west and southwest of Pullman are the source of alate aphids that migrate east and infest Palouse field peas. Areas to the west and southwest of Pullman support larger plantings of alfalfa [yearly average of 38,500 hectares in four counties (Benton, Franklin, Walla Walla, Columbia), 1985 to 2003] compared to Whitman County (yearly average of 5,100 hectares, ) (USDA, Washington Agricultural Statistics Service, Olympia, WA, Aphids may arrive in the Palouse region with the assistance of the prevailing spring and early summer wind movements, which generally come from the west-southwest (National Climatic Data Center, National Oceanic and Atmospheric Administration, Asheville, North Carolina, This is plausible because the pea aphid can move long distances when assisted by winds (11,19).

5 Alfalfa is an important reservoir for BLRV, PeSV, and AMV in the Pacific Northwest (14,16,17,18). This knowledge, combined with information in the preceding paragraph, indicates that aphids plausibly acquire these viruses from alfalfa before migrating and infecting pea crops in the Blue Mountain region and southern Idaho. Because BLRV was one of the predominant viruses (with PEMV) causing the 1990 epidemic on field peas and other grain legumes in eastern Washington (21), we can assume that infected alfalfa was the likely source of viruliferous aphids. Importantly, however, a 6-year survey (1988 to 1994) of alfalfa in eastern Washington and virus transmission experiments showed that alfalfa is not currently a host for PEMV in this region (24). By contrast, an earlier report stated that alfalfa was the principal perennial host for PEMV in the Blue Mountain region (25); however, this conclusion was "based primarily on circumstantial evidence" (24). The absence of PEMV in alfalfa logically opposes requisite involvement of this perennial legume in subsequent pea aphid-field pea-pemv relationships in the Palouse region. Thus, unlike the link between pea aphid, alfalfa, and other viruses (BLRV, PeSV, AMV) in the Pacific Northwest, we are left with no plausible source for winged pea aphids that migrate to eastern Washington and transmit PEMV, the most important viral disease of food legumes during outbreak years in this region [(21) and F. Muehlbauer, personal communication]. In a broader sense, this information casts doubt on notions that severe PEMV epidemics in the Palouse are associated with large migratory flights of the pea aphid from alfalfa. Research has not determined if other legumes can serve as reservoir hosts for PEMV in eastern Washington (24). Winter Temperatures and Pea Aphid Outbreaks It is widely thought that minimum winter temperatures influence the earliness of pea aphid population increases that lead to outbreaks (8,11,15,18,27). The concept that specific winter temperatures and patterns are directly linked to spring pea aphid outbreaks in the Pacific Northwest originated with Rockwood and Reeher (27) who, based on temperature records and field notes for 29 years in western Oregon, reported that outbreaks did not occur when (i) the minimum winter temperature fell below -9.5 C; (ii) mean temperatures for any 7 to 8 day period (September to June) were C; and (iii) when the lowest monthly mean temperature was 2.8 C. Apparently, the mild winters permitted high survival of adult forms on legumes and set the stage for outbreaks. Cooke (8) embraced the association of "mild winters" with pea aphid outbreaks while reporting that "severe outbreaks in the Blue Mountain area rarely, if ever, followed winter seasons in which subzero temperatures occurred between January 15 and February 10." Against this backdrop, winter temperature records (1982 to 2005) from the Blue Mountain (Walla Walla, WA) and Palouse (Pullman) regions were related to pea aphid outbreak and non-outbreak years in the Palouse to see if mild winters herald outbreaks in this region. This exercise used December to February temperature patterns, albeit slightly modified from Rockwood and Reeher (27), to define a mild winter as one with no days with temperatures C and/or one in which the mean for three low monthly mean temperatures was C. Using these patterns, I was unable to consistently link mild winters with ensuing aphid outbreaks. Based on December-to-February temperature records from Walla Walla, expected and actual outcomes (outbreak, no-outbreak) were incongruent or nearly so for 7 years (Table 1). For example, the mild winters of , , and did not give rise to pea aphid outbreaks, and the winter temperatures of , , and were such that one should not expect an ensuing outbreak. Yet, 1990, 1996, and 2005 were outbreak years (Fig. 4; Table 1). For , the mean low monthly temperature value did not quite meet the benchmark of C; however, there were no days below -9.5 C so one could argue that the 1983 outbreak followed a fairly mild winter (Table 1). Importantly, there was agreement between expected and actual outcomes for 16 years (70% prediction rate); that is, no outbreaks occurred when there were winter days -9.5 C and/or low monthly temperatures averaged C (data not shown).

6 Table 1. Relationship of winter temperature patterns in the Blue Mountain region (Walla Walla) to a selected number of pea aphid outbreak and non-outbreak years in the Palouse region of eastern Washington. x Year No. days -9.5 C Means of low monthly temperatures ( C) Outcome: outbreak () no outbreak (-) Dec - Feb Dec - Feb 3-mo ave Expected Actual x Temperature data from Whitman Mission, US National Park Service, Walla Walla, WA, and the National Climatic Data Center, National Oceanic and Atmospheric Administration, Asheville, NC, Likewise, analysis of Pullman winter temperatures showed that mild winter temperatures alone were not sufficient to account for spring pea aphid outbreaks (data not shown). Nor was Hampton (15) able to relate winter temperatures with high pea aphid densities and the transmission of BLRV to peas in southern Idaho. In short, the collective evidence contradicts notions that pea aphid outbreaks in eastern Washington consistently follow mild winters. Other Factors and Pea Aphid Outbreaks Beyond winter temperatures, other factors are thought to influence the frequency of pea aphid outbreaks in eastern Washington and other Pacific Northwest regions. For example, high numbers of overwintering pea aphids on succulent alfalfa plants could give rise to outbreak numbers on peas, providing alfalfa cutting operations and the development of mature and less succulent alfalfa plants force large migration flights of winged aphids (8,11,16,25). Also, Rockwood and Reeher (27) stated that an abundance of suitable host plants early in the fall and critical periods of rainfall in September and in the spring have considerable effect on pea aphid populations but are secondary to the factor of winter temperatures. Rain and wind storms, common in the spring in the Pacific Northwest, may also reduce pea aphid numbers by knocking aphids from host plants (11,25), thereby influencing whether or not an outbreak occurs. Finally, rain storm events and prevailing wind speeds and trajectories might influence the spring migration of winged pea aphids and subsequent outbreak events in eastern Washington. A wide variety of natural enemies (e.g., coccinellids, syrphid larvae, hymenopterous parasitoids, fungus diseases) attack pea aphids in alfalfa in the Blue Mountain region (8,11); however, their role in significantly reducing pea aphid numbers in the Pacific Northwest is unclear. Interestingly, coccinellid predators appeared to have a continuous and marked effect on pea aphid numbers in Vancouver, Canada (13), and the seven-spotted ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae), dampened the potential of pea aphid populations to reach high numbers in alfalfa fields in northern Utah (12). These conclusions suggest a need for a detailed assessment of pea aphid-coccinellid interactions in Pacific Northwest alfalfa fields, especially since the introduced C. septempunctata and other coccinellid species occur in the Pacific Northwest (7,23). Such a study would help us understand if coccinellid predators contribute to significant reductions in pea aphid numbers, thus reducing the potential for outbreaks in the region. Conclusions This review shows that several pea aphid outbreaks have occurred between the years 1917 and 2005 in the Pacific Northwest, with outbreaks and associated virus epidemics occurring every 5 to 9 years ( ) on field peas in the Palouse. This knowledge is important from a pest and plant health perspective ±

7 because it shows that pea producers in this region will not experience significant and widespread pea aphid and virus induced yield losses in most years. Unfortunately, Palouse producers have no advance warning of pea aphid outbreak and virus epidemic years. Although a forecasting system might provide producers with advance knowledge of impending outbreaks, thereby leading to timely and informed pest control decisions, it is premature to embark upon the development of one. This is because we lack comprehensive information about the important factors that influence pea aphid outbreaks. The preceding section highlights some potentially important factors, which likely operate as multiple-level interactions. Although weather influences aphid outbreaks (30), an important conclusion from this study is that mild winters alone cannot account for subsequent spring pea aphid outbreaks. Interestingly, European entomologists were unsuccessful using aphid counts and weather data to develop reliable forecasting systems for the pea aphid. These researchers stated that "a general forecast of pea aphid levels in peas is impracticable" in Sweden (3) and "it is not yet clear what determines changes in the year-to-year abundance of A. pisum" in Germany (29). Moreover, the Swedish entomologists questioned the value of using suction trap catches for predicting pea aphid infestations on peas. Likewise, pea aphid capture data from an aphid suction trap (1) in eastern Washington was too variable to predict impending outbreaks and the magnitude of pea aphid colonization episodes on field peas [(5) and Clement, unpublished information]. Finally, the fact that alfalfa is not a reservoir for PEMV in eastern Washington underscores the problem of using pea aphid data from alfalfa fields to develop a reliable forecasting system. In light of the requirement for significantly more research to complete a picture of pea aphid-host plant-virus relationships in the Pacific Northwest, and the challenges associated with developing a reliable pea aphid forecasting system, the best course of action for protecting field peas from devastating yield losses during periodic outbreaks may be the development and deployment of virus-resistant cultivars. Acknowledgments I am indebted to Leslie Elberson for unwavering technical assistance and for help assembling the manuscript. Also, I am grateful to Walter Kaiser, Frank Dugan, Fred Muehlbauer, Richard Larsen, Sanford Eigenbrode, Hanu Pappu, and Todd Scholz for valuable discussions and reviews. Additionally, I thank Fred Muehlbauer for his personal communication, Larry O Keeffe for pea aphid literature, and Sanford Eigenbrode for his photograph of virus-infected peas. Mention of commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. Literature Cited 1. Allison, D., and Pike, K. S An inexpensive suction trap and its use in an aphid monitoring network. J. Agric. Entomol. 5: Berryman, A. A The theory and classification of outbreaks. Pages 3-27 in: Insect Outbreaks. P. Barbosa and J. C. Schultz, eds. Academic Press, Inc., San Diego, CA. 3. Bommarco, R., and Ekbom, B Phenology and prediction of pea aphid infestations on peas. Int. J. Pest Manag. 41: Bronson, T. E Observations on winter survival of pea aphid eggs. J. Econ. Entomol. 28: Clement, S. L Ex situ genebank practices: Protecting germplasm nurseries from insect pests. Plant Genet. Res. News 119: Clement, S. L., Wightman, J. A., Hardie, D. C., Bailey, P., Baker G., and McDonald, G Opportunities for integrated management of insect pests of grain legumes. Pages in: Linking Research and Marketing Opportunities for Pulses in the 21st Century. R. Knight, ed. Kluwer Academic, Dordrecht, The Netherlands.

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