Effect of Potato virus Y Presence in Solanum tuberosum (Solanales: Solanaceae) and Chenopodium album on Aphid (Hemiptera: Aphididae) Behavior

Effect of Potato virus Y Presence in Solanum tuberosum (Solanales: Solanaceae) and Chenopodium... Abstract This study establishes the effect of Potato Virus Y (PVY; Potyvirus) in potatoes, Solanum tuberosum L. (Solanales: Solanaceae) and in common-lambs’ quarter Chenopodium album L. (Amaranthaceae) on Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) and Myzus persicae Sulzer (Hemiptera: Aphididae) behavior, host preference, transmission, and fitness under field and laboratory studies. In the field, several weeds, besides C. album, were collected, including: Sisymbrium altissimum L. (Brassicaceae), Erodium cicutarium L., Lactuca serriola L., Solanum sarrachoides Sendtner (Solanaceae), and S. dulcamara L. (Solanaceae). All weeds were serologically tested for the presence of PVY. From all weeds collected, 2.3 and 34% of C. album and S. sarrachoides, respectively, were PVY-positive. From those positive samples, 72% of the PVY found were PVYN; the remaining 28% was PVYO. In addition, several aphid species were collected from those weeds: Ovatus crataegarious Walker, Macrosiphum euphorbiae (Hemiptera: Aphididae), Hyalopterus pruni Geoffroy (Hemiptera: Aphididae), Rophalosiphum madis Fitch, and ‘others aphid’ species were collected. The highest number of aphids were collected in E. cicutarium, followed by S. dulcamara, L. serriola, S. altissimum, and C. album. In laboratory studies, PVY-infected C. album does not induce the production of aphids. Moreover, M. persicae did not appear to have a strong preference for either healthy or PVY-infected potato plant, but they did develop a preference for infected plants after prolonged feeding. M. persicae and M. euphorbiae transmitted PVY from C. album to S. tuberosum, 44 and 37.5 % of the time. Future research should seek to identify not only other sources and prevalence of PVY in the field but vector relationships. In insect-pathogen complex continues to persist in solanaceous field crops around the world. Non-persistent transmission, green peach aphid, potato aphid, alternative hosts, weed host Potato virus Y (PVY: Potyviridae) has long been a persistent problem in both commercial and seed potatoes, Solanum tuberosum L., production in the United States and worldwide (De Bokx and Hunttinga 1981, Hernández-de la Cruz et al. 2007, Gray et al. 2010, Lacroix et al. 2010, Kostiw 2011). PVY reduces overall yields as well as negatively impacts crop quality (Hane and Hamm 1999, Rykbost et al. 1999, Nolte et al. 2004). PVY-infected seed can serve as a source of contamination and presents a problem for seed certification, since the sympoms are variety dependent in potatoes and may not be recognized by visual inspection (Crosslin et al. 2006, Gray et al. 2010). In Europe, PVY is a major problem in solanaceous crops other than potatoes, including different species of pepper (Capsicum spp.) in Spain (Fereres et al. 1993) or tomatoes (Solanum lycopersicum L.) in Italy (Mascia et al. 2010). Unlike many potato viruses, PVY is vectored by aphids in a nonpersistent manner and may be acquired and transmitted in seconds by aphids, such as Myzus persicae Sulzer (Hemiptera: Aphididae) and Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) (Döring et al. 2006). Viruses that are vectored through nonpersistent transmission are often difficult to control, and insecticides do not effectively reduce disease spread (Döring et al. 2006). Noncolonizing aphid species can also serve as vectors of PVY but may or may not be as effective as colonizing aphids (Fereres et al. 1993, Boukhris-Bouhachem et al. 2011). Therefore, a thorough understanding of vector biology and behavior could help us develop more effective insect-disease management strategies (Fereres and Moreno 2009). Previous research suggested that plant-insect interactions can influence vector biology or behavior (Collar and Fereres 1998). For instance, vectors may be more attracted to infected hosts, therefore increasing the chances of virus transmission (Fereres et al. 1999, Alvarez et al. 2007). Infected hosts may also affect the physiology of the insects themselves: increasing alate production, which will in turn increase mobility of the vector and spread of the pathogen (Gildow 1980). The epidemiology of PVY could be affected by the presence of weeds that could act as reservoirs of the virus, but also PVY-infected weeds could modify the behavior and fitness of its aphid vectors. All these behavioral changes in the vectors could alter the spread of PVY in different ways depending on the type of virus-vector interaction. For instance, Mauck (2016) indicated that virus infection can elicit changes in host plant cues that can mediate vector orientation, feeding, and dispersal and that can potentially provide cues for better understanding of virus-insect evolution. To our knowledge, natural infections of PVY in Chenopodium album L. (Amaranthaceae; common lambsquarter) have not been reported in the United States to date but have been reported in Canada (Nanayakkara et al. 2012). In general, Chenopodium is a genus of numerous species including C. acicularis, C. acuminatum, C. auricomiforme with worldwide distribution, including C. quinoa, an important crop in the South American Andes (Sukhorukov and Zhang 2013). This plant is a weedy annual commonly known as lambs’ quarters, goosefoot, pigweed, or fat-hen. It can be a source of other viruses such as beet pseudo yellow virus (BPYV) (Harris and Maramorosch 1980). Specifically, C. album is a common weed found near potato fields in the United States and Canada (Whitson et al. 2002, Kazinczi et al. 2004, Kaliciak and Syller 2009, Nanayakkara et al. 2012). In Europe, nonsolanaceous PVY hosts have been identified including C. album, prickly lettuce Lactuca serriola L. (Asteraceae), redstem filaree Erodium cicutarium L. (Geraniaceae), small-flowered cranes’s bill Geranium pusillum L. (Geraniaceae), and purple deadnettle Lamium purpureum L. (Lamiaceae) (Zitter 2001, Kazinczi et al. 2004, Kaliciak and Syller 2009). In the United States, weeds from the Solanceae family are well-known reservoirs of PVY and well-studied (Srinivasan and Alvarez 2008, Kaliciak and Syller 2009, Cervantes and Alvarez 2011, Nie et al. 2012). Besides the complexity of the role of field solanaceous hosts or broad weed hosts as a source of the PVY virus, the different PVY strains, such as PVYN, PVYO, PVYN, PVYNTN that cause one or more of the following symptoms: leaf mosaic, necrosis, stunting, and/or reduced potato yields (Hane and Hamm 1999, Crosslin et al. 2006, Nie et al. 2012) are dynamically changing in prevalence. For instance, in the United States, PVYO used to be the dominant strain, however, in recent years, incidence of PVYNO and PVYN has increased dramatically (Crosslin et al. 2005, 2006; Gray et al. 2010); in Spain, PVYN is already the dominant strain (Rolland et al. 2008, Gray et al. 2010). Symptoms are difficult to recognize unless using serological methods (Karasev et al. 2011). The present study was designed 1) to investigate in the field whether C. album can be a source of inoculum of PVY; 2) to evaluate how the presence of PVY in S. tuberosum and C. album affects behavior, host preference, transmission, and fitness for M. persicae and M. euphorbiae under controlled conditions. Materials and Methods Fields were located in the lower and upper Columbia Basin of Oregon and Washington, respectively; laboratory studies were conducted in laboratories of the Instituto de Ciencias Agrarias in Madrid, Spain (40.4168°N, 3.7038°W), and at the Oregon State University Hermiston Agricultural Research and Extension Center, Irrigated Agricultural Entomology program, in Hermiston Oregon (45.8404°N, 119.2895°W). Sampling C. album Eight commercial fields were sampled for the presence of C. album in 2013 and 2014 potato-growing season. Besides, C. album, other common weeds were collected based on the abundance and proximity to potato fields. Weeds were sampled covering approximately 20 m around field borders. Commercial fields in the Columbia Basin are typically central pivot irrigated, ranging from 30 to 121 ha. To determine the presence of PVY at each site, a composite of 100 leaves from individual plants per weed species was collected, bagged, labeled, and taken to the laboratory for enzyme-linked immunosorbent assay (ELISA) testing (Crosslin et al. 2005). Weeds were collected monthly from June through August. Potato-growing season in the area in average goes from mid-April until first weeks in September, depending on planting date. To determine the presence of aphids, Berlese funnels (modified Tullgren funnel) and an inverted leaf blower (Ryobi 26 cc 200 mph, Model N. RY09050, Anderson, SC) were utilized. Berlese funnels were used for extracting aphids below and above ground; while the inverted leaf blower was used to collect aphids above ground. Aphids collected were identified by A. F. Murphy. Aphid Colonies and Host Plants Virus-free aphid colonies of M. persicae and M. euphorbiae were established from a single virginiparous female collected in Spain at Alcalá de Henares (40.4820°N, 3.3635°W) and Villa de Prado (40.2800°N, 4.3052°W), respectively. M. persicae colony was maintained on young turnip plants (Brassica rapa L. cv ‘Just Right’), while the M. euphorbiae colony was maintained on young lettuce (Lactuca sativa L. cv. longifolia ‘Moratina’). Plants were kept at D:N 23°C ± 2°C:18°C ± 2°C, photoperiod 16:8 L:D ± 2 h, and 60–80% R.H. Similar procedure was followed for aphids kept on PVY-infested plants. Virus-free colonies were kept in a separate growth chamber to avoid cross-contamination. Dual-Choice Alighting Assay For the dual-choice assays, one PVYN-infected C. album and one mock-inoculated C. album plant were placed 20 cm apart, inside an aphid-proof cage (65 × 45 × 50 cm) following a methodology similar to that described by Carmo-Sousa et al. (2016). A few exceptions were made. A mock- inoculated plant was previously ‘inoculated’ with deionized water so that any stress caused by the inoculation process did not influence aphid behavior. Plants used in the experiment were similar in size and age. Thirty M. persicae alates were removed from the colony with the help of an aspirator, and these aphids were immediately released all at once in the aphid-proof cage containing the C. album-infected and mock plants. Aphids were released once during the assay, either on the C. album mock-inoculated plants or C. album PVY-infected plants (n = 30) to allow aphids to stay or move to the contiguous plant. The number of alates settled on either plant was counted at 1, 10, 30, 60, 120, and 180 min after release, by observation only and with minimal disturbance of the plant. Two new plants were selected for each repetition; before cages were used, they were thoroughly cleaned and inspected for any remaining aphids to avoid cross contamination between replications. All assays were performed during daylight hours in a greenhouse at 25 ± 2°C. Free-Choice Settling Assay The preference of M. persicae to settle on either PVY-infected or mock-inoculated C. album plants was tested at different time intervals under free-choice conditions. A cage (1 × 1 × 1 m) constructed of clear plexiglass and netting similar to the one described by Garzo et al. (2003) was used in the experiment. Six PVYN-infected and six mock-inoculated C. album plants were placed, alternately in a circle inside the arena. Two hundred non-viruliferous winged M. persicae were placed in a black release container on a flight platform similar to the one described by Fereres et al. (1999). Aphids were released at 0.5 m above the test plants. The number of aphids settled on each test plant was counted at different intervals (0.5, 2, 4, and 48 h) using destructive methods. The experiment was replicated three times per time interval. For this purpose, after each time interval, each plant was covered with a plexiglass cylinder and transferred to the laboratory for aphid counting. Three replicates were performed for each time evaluation period. All assays were performed during daylight hours in a greenhouse at 25 ± 2°C. Contrasts were used to compare aphid numbers settling on infected or uninfected plants. Aphid Fitness on PVY-Infected Plants To determine if aphid progeny were affected by the presence of PVY in C. album, plants were infected with PVYO or PVYN; a mock-inoculated plant was used as a control. Seven plants per PVY strain or control were caged in individual screen sleeves. A single M. persicae alate was placed gently in each plant using a fine paintbrush. The alate was allowed to remain, feed on the plant, and reproduce for 48 h following the protocol described by Gildow (1980). After that period, the original alate was carefully removed and the offspring were counted and allowed to develop in a growth chamber for 14 d at 25 ± 2°C, photoperiod of 16:8 L:D, and 60–80% R.H. C. album as a PVY Source The ability to transmit PVYN from C. album to potatoes by M. persicae or M. euphorbiae was tested following a standardized procedure described by Fereres et al. (1993). Groups of 25–30 aphids per species were starved for 1 h before exposing them for an acquisition access period of 10 min on a PVY-infected C. album plant inoculated 3–4 wks earlier. After the acquisition access period, groups of five aphids were moved to a healthy receptor potato plant and were allowed to feed for an inoculation access period of 24 h. Aphids were then removed, and potato plants were sprayed with imidacloprid (Confidor) and transferred to a growth chamber at 25 ± 2°C with a photoperiod of 16:8 L:D and 60–80% R.H. All plants were tested after 4 wks using ELISA to determine PVY presence. The experiment was repeated three times (n = 25) for each aphid species. Data Analysis For the dual-choice assay, the relative percent of aphids settled on each type of host plant, in total and through time was evaluated using a Kruskal-Wallis since data could not be transformed to meet normality assumptions. For the free-choice settling assay, the mean relative percent of aphids settled on mock-inoculated or PVY-infected host plants was compared using a t-test at each time interval. Transmission study data were analyzed by summarizing number of infected potato plants for each species as a percentage of the total. This is a standard method of reporting transmission rates (Collar and Fereres 1998, Alvarez and Srinivasan 2005, Verbeek et al. 2009, Mello et al. 2011). For the host suitability study, the total number of aphids surviving on each plant was transformed using a Johnson transformation to assure normality and then compared across treatments (PVY strain) using a one-way analysis of variance. Inverted leaf blower and Berlese samples were compared using a Mann-Whitney test because the data could not be transformed to meet normality assumptions. All analyses were performed using Minitab 16 (Minitab, Inc., State College, PA). Results C. album, Other Weeds, PVY, and Aphids in the Field Besides C. album, tumble mustard Sisymbrium altissimum L. (Brassicaceae), redstem filaree E. cicutarium, prickly lettuce L. serriola, hairy nightshade Solanum sarrachoides Sendtner (Solanaceae), and bittersweet nightshade S. dulcamara (Solanaceae) were the most abundant. All weeds collected were tested for the presence of PVY. Only C. album and S. sarrachoides tested positive for PVY. From all weeds collected, 2.3 and 34% of C. album and S. sarrachoides, respectively, were PVY-positive. From those positive samples, 72% of the PVY found were PVYN; the remaining 28% was PVYO. In 2013, the highest number of aphids were collected in E. cicutarium, followed by S. dulcamara, L. serriola, S. altissimum, and C. album (data not shown). The most predominant aphid species near potato fields was Ovatus crataegarious Walker (mint aphid) (14% of aphids collected), followed by M. euphorbiae (13%), Hyalopterus pruni Geoffroy (mealy plum aphid) (12%), and Rophalosiphum madis Fitch (bird cherry oat aphid) (10%). Other aphids such as M. persicae, Brevicoryne brassicae L. (cabbage aphid), Hayhurstia atriplicis L. (chenopodium aphid), Aphis fabae Scopoli (black bean aphid), Acyrtosiphum pisum Harris (pea aphid), and the genera Nearctaphis, Dysaphis, Sitobion, Ceruarphis, Metopolophium, Hypemomyzus, Hyalomyzus, and Capitophora were also present but in lesser numbers (data not shown). In 2014, E. cicutarium harbored the highest number of aphids followed by L. serriola. As the previous year, O. crataegarious was the most abundant. The inverted leaf blower method collected a greater mean number of aphids per sample (25.08 ± 7.5) compared to the Berlese method (3.93 ± 1.4) (W = 68831; P < 0.001). Bioassays Table 1 shows the mean relative percentage of M. persicae alates settled on PVY-infected C. album or PVY-mock inoculated plants in the dual-choice tests. There were no significant differences for the relative percent of aphids settled on either infected of PVY-free plant (H = 0.02; df = 1; P = 0.900). However, there were differences on the relative percent of aphids on a host over time (H = 10.73; df = 5; P = 0.057). Table 1. Mean (±SE) relative percent of Myzus persicae Sulzer (Hemiptera: Aphididae) settled on PVY-infected C. album or mock-inoculated (control) Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  View Large Table 1. Mean (±SE) relative percent of Myzus persicae Sulzer (Hemiptera: Aphididae) settled on PVY-infected C. album or mock-inoculated (control) Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  View Large The mean (±SE) relative percent of M. persicae alates settled on a PVY-infected or PVY-mock inoculated plants can be seen in Table 2. There were no significant differences in the mean relative percent of M. persicae settled on mock-inoculated or PVYN-infected host plants at time intervals 0.5 h (t = 0.63; df = 2; P = 0.591), 2 h (t = 0.21; df = 3; P = 0.845), and 4 h (t = 1.05; df = 3; P = 0.371). However, the number of alates settled on healthy (mock-inoculated) plants was significantly higher than the one on infected plants at 48 h after release (t = 3.18; df = 4; P-value = 0.034). Table 2. Mean (±SE) relative percent of Myzus persicae Sulzer settling on PVY-infected C. album or mock-inoculated (control) Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  View Large Table 2. Mean (±SE) relative percent of Myzus persicae Sulzer settling on PVY-infected C. album or mock-inoculated (control) Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  View Large The mean number (± SE) of M. persicae progeny on mock-inoculated C. album plants was numerically higher when compared with number of progeny on PVYN or PVYOC. album plants but it was not statistically different (F = 0.89.; df = 2, 20; P = 0.427) (Table 3). Table 3. Mean number (±SE) of M. persicae present on PVYO, PVYN, or mock-inoculated (control) C. album 14 d after infestation with a single founding alate Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  View Large Table 3. Mean number (±SE) of M. persicae present on PVYO, PVYN, or mock-inoculated (control) C. album 14 d after infestation with a single founding alate Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  View Large Forty-four and 37.5% percent of potato plants tested positive by ELISA when exposed to M. persicae and M. euphorbiae, respectively. Potato plants were tested 4 wk after aphids were removed from plants. Discussion This study presents valuable information that establishes the role of C. album as a potential source of inoculum of PVY in the United States. Moreover, data from this study provide some insight regarding the role of the presence of PVY in potatoes and C. album and how that may affect the behavior, host preference, transmission, and fitness for M. persicae and M. euphorbiae under controlled conditions. Several weeds were tested for the presence of PVY, but only C. album and S. sarrachoides were PVY-positive. The latter one has been extensively studied (Alvarez and Srinivasan 2005, Srinivasan et al. 2006, Alvarez et al. 2007, Srinivasan and Alvarez 2008), hence our work focused on C. album. Although less than 3% of the C. album collected was PVY-positive, due to the proximity of this weed to potato field and geographical distribution (Nanayakkara et al. 2012, Krak et al. 2016), C. album can serve as a potential source of PVY. Samples that tested positive were collected in July and August, therefore PVY can be found not only in the potato crop itself in the tail end of the potato season (Singh 1987) in the Columbia Basin but also in C. album. Although negative for the presence of PVY in weeds such as S. altissimum, E. cicutarium, and L. serriola, the role of other weeds in the area as potential source of PVY remains to be investigated. Not surprisingly, there are greater numbers of aphids above ground as collected with the inverted leaf blower method. Weeds, including C. album, serve as a reservoir for aphids (data not shown). According to Agripedia (2017), over 200 crops can be grown in the state of Oregon alone, thus, it is not surprising to find such a diversity of aphids species in and around potato fields. Klein et al. (2017) reported the presence of over 30 aphid species in the area. Furthermore, Mondal et al. (2016) and Klein et al. (2017) indicated that the role of aphids such as M. persicae, M. euphorbiae, and R. padi as vectors or PVY is well understood, while the role of ‘other aphids’ as vectors of PVY, or other viruses, remain to be studied. Data from this study also identified characteristics of vector behavior related to PVY that might help explain how PVY is spread through a field. While searching for a suitable host, aphids land on host crops and nonhosts, to settle and reproduce. C. album is an integral part of the landscape, and several studies have determined the ability of C. album to serve as a sink for PVY (Singh 1987, Kaliciak and Syller 2009, Nanayakkara et al. 2012). However, according to our results, PVY-infected C. album does not induce the production of aphids, as was the case with Gildow et al. (1980) study, where infected host plants produced an abundance of winged aphids, increasing transmission. Srinivasan and Alvarez (2007) found that populations of M. persicae and M. euphorbiae were higher on potatoes infected with mixed infections of PVY and Potato leafroll virus (PLVR, Luteoviridae) another important potato disease. A similar trend was expected in this study. However, given the low mean number of aphids present after 14 d, it is apparent that C. album is not an ideal host for the M. persicae clones used in this study. Contrary to our findings, C. album is considered a host for this highly polyphagous species and has been used successfully as a host plant in other studies (Vorburger and Ramsauer 2008). M. persicae clones from different localities can present different preferences, fitness, and intrinsic growth rates for different hosts (Nikolakakis et al. 2003). While C. album did not lead to increased alate production in this study, the weed may still serve as a reservoir for PVY, particularly because it is not a preferred host plant. Instead, migrating aphids in search of a preferred host may probe infected plants and then migrate because of nonpreference, promoting the spread of PVY. Based on our results, M. persicae did not appear to have a strong preference for either healthy or PVY-infected plants. This was an unexpected finding with M. persicae, as several similar studies have found that this vector prefers infected host plants using a different host (Fereres et al. 1999, Srinivasan et al. 2006). However, Boquel et al. (2012) found similar results with PVY-infected and noninfected potatoes in a laboratory setting, where aphid vectors could not distinguish between infected and healthy hosts. It is possible that there are no distinctive differences in visual or olfactory cues between PVY-infected and healthy (mock-inoculated) C. album plants, particularly considering that infected plants appeared to be asymptomatic. If this is true, no preference would be anticipated (Fereres and Moreno 2009). While aphid vectors, namely M. persicae, appear to be unable to discriminate between infected and healthy hosts initially, they did develop a preference after extended feeding. This indicates that aphids landing on an infected host are likely to leave after extended feeding. This delayed nonpreference for infected plants could increase the spread of PVY due to aphids moving from infected plants to surrounding crops or vegetation. A similar relationship was found with Cucumber mosaic virus (CMV) and its aphid vector, Aphis gossypii Glover (Hemiptera: Aphididae) (Carmo-Sousa et al. 2014). Carmo-Sousa et al. (2014) found that A. gossypii was initially attracted to infected host plants but preferred to colonize noninfected plants, leading to increased transmission of CMV, also a virus with nonpersistent transmission. Both vectors, M. persicae and M. euphorbiae, transmitted PVY 44 and 37.5% of the time, respectively, demonstrating that C. album could serve as a reservoir for PVY. The transmission rate of PVY for M. persicae from potatoes to potatoes (preferred hosts) has been documented to be 57.5%, only slightly higher than the rate measured for C. album to potatoes in this study (Mello et al. 2011). For M. euphorbiae, the transmission rate for PVYN from tobacco to potato is 29%, lower than that found with C. album (De Bokx and van der Want 1987). Differences in host preferences for M. persicae clones have not resulted in significant differences in transmission rates for PVY (Kanavaki et al. 2006). Therefore, the transmission rates determined in this study should be broadly applicable to many populations of M. persicae. Regardless of the nonpreference of the M. persicae clones used in this study for C. album as a host, PVYN infection still influenced the behavior of M. persicae in a manner that would favor transmission. As the behavior identified for C. album likely differs with PVY-infected potatoes, a preferred host and another potential reservoir (Srinivasan and Alvarez 2007), future research should seek to identify these trends in a field setting. Undoubtedly, the prevalence of PVY in C. album in the field would be an important factor to assess to determine if C. album truly serves as a reservoir in the United States or Europe. Future research should seek to identify not only sources and the prevalence of PVYN in the field but also the abundance of the vectors themselves. While both of the vectors investigated in this study exhibited relatively high transmission rates, vector abundance plays an important role in the spread of PVY. It has been suggested with many viruses that are transmitted in a nonpersistent manner, and particularly PVY, that extremely abundant vectors with low transmission rates and limited preference for the host can still spread virus at economic levels (Pelletier et al. 2008). In spite of extensive research, this disease continues to persist in solanaceous field crops around the world and elude control measures. Although this study may provide some additional answers, more research is still needed to complete knowledge gaps in vector behavior and abundance, as well as identify more effective control measures. Acknowledgments The authors would like to acknowledge funding from NIFA-AFRI in the form of a postdoctoral fellowship, and the Oregon Potato Commission. Technical assistance was provided by M. Carmo-Sousa from the Fereres Research lab for research in Spain. 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Vegetable Crops: A Checklist of Major Weeds and Crops as Natural Hosts for Plant Viruses in the Northeast. http://vegetablemdonline.ppath.cornell.edu/Tables/WeedHostTable.html © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Effect of Potato virus Y Presence in Solanum tuberosum (Solanales: Solanaceae) and Chenopodium album on Aphid (Hemiptera: Aphididae) Behavior

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Entomological Society of America
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Abstract

Abstract This study establishes the effect of Potato Virus Y (PVY; Potyvirus) in potatoes, Solanum tuberosum L. (Solanales: Solanaceae) and in common-lambs’ quarter Chenopodium album L. (Amaranthaceae) on Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) and Myzus persicae Sulzer (Hemiptera: Aphididae) behavior, host preference, transmission, and fitness under field and laboratory studies. In the field, several weeds, besides C. album, were collected, including: Sisymbrium altissimum L. (Brassicaceae), Erodium cicutarium L., Lactuca serriola L., Solanum sarrachoides Sendtner (Solanaceae), and S. dulcamara L. (Solanaceae). All weeds were serologically tested for the presence of PVY. From all weeds collected, 2.3 and 34% of C. album and S. sarrachoides, respectively, were PVY-positive. From those positive samples, 72% of the PVY found were PVYN; the remaining 28% was PVYO. In addition, several aphid species were collected from those weeds: Ovatus crataegarious Walker, Macrosiphum euphorbiae (Hemiptera: Aphididae), Hyalopterus pruni Geoffroy (Hemiptera: Aphididae), Rophalosiphum madis Fitch, and ‘others aphid’ species were collected. The highest number of aphids were collected in E. cicutarium, followed by S. dulcamara, L. serriola, S. altissimum, and C. album. In laboratory studies, PVY-infected C. album does not induce the production of aphids. Moreover, M. persicae did not appear to have a strong preference for either healthy or PVY-infected potato plant, but they did develop a preference for infected plants after prolonged feeding. M. persicae and M. euphorbiae transmitted PVY from C. album to S. tuberosum, 44 and 37.5 % of the time. Future research should seek to identify not only other sources and prevalence of PVY in the field but vector relationships. In insect-pathogen complex continues to persist in solanaceous field crops around the world. Non-persistent transmission, green peach aphid, potato aphid, alternative hosts, weed host Potato virus Y (PVY: Potyviridae) has long been a persistent problem in both commercial and seed potatoes, Solanum tuberosum L., production in the United States and worldwide (De Bokx and Hunttinga 1981, Hernández-de la Cruz et al. 2007, Gray et al. 2010, Lacroix et al. 2010, Kostiw 2011). PVY reduces overall yields as well as negatively impacts crop quality (Hane and Hamm 1999, Rykbost et al. 1999, Nolte et al. 2004). PVY-infected seed can serve as a source of contamination and presents a problem for seed certification, since the sympoms are variety dependent in potatoes and may not be recognized by visual inspection (Crosslin et al. 2006, Gray et al. 2010). In Europe, PVY is a major problem in solanaceous crops other than potatoes, including different species of pepper (Capsicum spp.) in Spain (Fereres et al. 1993) or tomatoes (Solanum lycopersicum L.) in Italy (Mascia et al. 2010). Unlike many potato viruses, PVY is vectored by aphids in a nonpersistent manner and may be acquired and transmitted in seconds by aphids, such as Myzus persicae Sulzer (Hemiptera: Aphididae) and Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) (Döring et al. 2006). Viruses that are vectored through nonpersistent transmission are often difficult to control, and insecticides do not effectively reduce disease spread (Döring et al. 2006). Noncolonizing aphid species can also serve as vectors of PVY but may or may not be as effective as colonizing aphids (Fereres et al. 1993, Boukhris-Bouhachem et al. 2011). Therefore, a thorough understanding of vector biology and behavior could help us develop more effective insect-disease management strategies (Fereres and Moreno 2009). Previous research suggested that plant-insect interactions can influence vector biology or behavior (Collar and Fereres 1998). For instance, vectors may be more attracted to infected hosts, therefore increasing the chances of virus transmission (Fereres et al. 1999, Alvarez et al. 2007). Infected hosts may also affect the physiology of the insects themselves: increasing alate production, which will in turn increase mobility of the vector and spread of the pathogen (Gildow 1980). The epidemiology of PVY could be affected by the presence of weeds that could act as reservoirs of the virus, but also PVY-infected weeds could modify the behavior and fitness of its aphid vectors. All these behavioral changes in the vectors could alter the spread of PVY in different ways depending on the type of virus-vector interaction. For instance, Mauck (2016) indicated that virus infection can elicit changes in host plant cues that can mediate vector orientation, feeding, and dispersal and that can potentially provide cues for better understanding of virus-insect evolution. To our knowledge, natural infections of PVY in Chenopodium album L. (Amaranthaceae; common lambsquarter) have not been reported in the United States to date but have been reported in Canada (Nanayakkara et al. 2012). In general, Chenopodium is a genus of numerous species including C. acicularis, C. acuminatum, C. auricomiforme with worldwide distribution, including C. quinoa, an important crop in the South American Andes (Sukhorukov and Zhang 2013). This plant is a weedy annual commonly known as lambs’ quarters, goosefoot, pigweed, or fat-hen. It can be a source of other viruses such as beet pseudo yellow virus (BPYV) (Harris and Maramorosch 1980). Specifically, C. album is a common weed found near potato fields in the United States and Canada (Whitson et al. 2002, Kazinczi et al. 2004, Kaliciak and Syller 2009, Nanayakkara et al. 2012). In Europe, nonsolanaceous PVY hosts have been identified including C. album, prickly lettuce Lactuca serriola L. (Asteraceae), redstem filaree Erodium cicutarium L. (Geraniaceae), small-flowered cranes’s bill Geranium pusillum L. (Geraniaceae), and purple deadnettle Lamium purpureum L. (Lamiaceae) (Zitter 2001, Kazinczi et al. 2004, Kaliciak and Syller 2009). In the United States, weeds from the Solanceae family are well-known reservoirs of PVY and well-studied (Srinivasan and Alvarez 2008, Kaliciak and Syller 2009, Cervantes and Alvarez 2011, Nie et al. 2012). Besides the complexity of the role of field solanaceous hosts or broad weed hosts as a source of the PVY virus, the different PVY strains, such as PVYN, PVYO, PVYN, PVYNTN that cause one or more of the following symptoms: leaf mosaic, necrosis, stunting, and/or reduced potato yields (Hane and Hamm 1999, Crosslin et al. 2006, Nie et al. 2012) are dynamically changing in prevalence. For instance, in the United States, PVYO used to be the dominant strain, however, in recent years, incidence of PVYNO and PVYN has increased dramatically (Crosslin et al. 2005, 2006; Gray et al. 2010); in Spain, PVYN is already the dominant strain (Rolland et al. 2008, Gray et al. 2010). Symptoms are difficult to recognize unless using serological methods (Karasev et al. 2011). The present study was designed 1) to investigate in the field whether C. album can be a source of inoculum of PVY; 2) to evaluate how the presence of PVY in S. tuberosum and C. album affects behavior, host preference, transmission, and fitness for M. persicae and M. euphorbiae under controlled conditions. Materials and Methods Fields were located in the lower and upper Columbia Basin of Oregon and Washington, respectively; laboratory studies were conducted in laboratories of the Instituto de Ciencias Agrarias in Madrid, Spain (40.4168°N, 3.7038°W), and at the Oregon State University Hermiston Agricultural Research and Extension Center, Irrigated Agricultural Entomology program, in Hermiston Oregon (45.8404°N, 119.2895°W). Sampling C. album Eight commercial fields were sampled for the presence of C. album in 2013 and 2014 potato-growing season. Besides, C. album, other common weeds were collected based on the abundance and proximity to potato fields. Weeds were sampled covering approximately 20 m around field borders. Commercial fields in the Columbia Basin are typically central pivot irrigated, ranging from 30 to 121 ha. To determine the presence of PVY at each site, a composite of 100 leaves from individual plants per weed species was collected, bagged, labeled, and taken to the laboratory for enzyme-linked immunosorbent assay (ELISA) testing (Crosslin et al. 2005). Weeds were collected monthly from June through August. Potato-growing season in the area in average goes from mid-April until first weeks in September, depending on planting date. To determine the presence of aphids, Berlese funnels (modified Tullgren funnel) and an inverted leaf blower (Ryobi 26 cc 200 mph, Model N. RY09050, Anderson, SC) were utilized. Berlese funnels were used for extracting aphids below and above ground; while the inverted leaf blower was used to collect aphids above ground. Aphids collected were identified by A. F. Murphy. Aphid Colonies and Host Plants Virus-free aphid colonies of M. persicae and M. euphorbiae were established from a single virginiparous female collected in Spain at Alcalá de Henares (40.4820°N, 3.3635°W) and Villa de Prado (40.2800°N, 4.3052°W), respectively. M. persicae colony was maintained on young turnip plants (Brassica rapa L. cv ‘Just Right’), while the M. euphorbiae colony was maintained on young lettuce (Lactuca sativa L. cv. longifolia ‘Moratina’). Plants were kept at D:N 23°C ± 2°C:18°C ± 2°C, photoperiod 16:8 L:D ± 2 h, and 60–80% R.H. Similar procedure was followed for aphids kept on PVY-infested plants. Virus-free colonies were kept in a separate growth chamber to avoid cross-contamination. Dual-Choice Alighting Assay For the dual-choice assays, one PVYN-infected C. album and one mock-inoculated C. album plant were placed 20 cm apart, inside an aphid-proof cage (65 × 45 × 50 cm) following a methodology similar to that described by Carmo-Sousa et al. (2016). A few exceptions were made. A mock- inoculated plant was previously ‘inoculated’ with deionized water so that any stress caused by the inoculation process did not influence aphid behavior. Plants used in the experiment were similar in size and age. Thirty M. persicae alates were removed from the colony with the help of an aspirator, and these aphids were immediately released all at once in the aphid-proof cage containing the C. album-infected and mock plants. Aphids were released once during the assay, either on the C. album mock-inoculated plants or C. album PVY-infected plants (n = 30) to allow aphids to stay or move to the contiguous plant. The number of alates settled on either plant was counted at 1, 10, 30, 60, 120, and 180 min after release, by observation only and with minimal disturbance of the plant. Two new plants were selected for each repetition; before cages were used, they were thoroughly cleaned and inspected for any remaining aphids to avoid cross contamination between replications. All assays were performed during daylight hours in a greenhouse at 25 ± 2°C. Free-Choice Settling Assay The preference of M. persicae to settle on either PVY-infected or mock-inoculated C. album plants was tested at different time intervals under free-choice conditions. A cage (1 × 1 × 1 m) constructed of clear plexiglass and netting similar to the one described by Garzo et al. (2003) was used in the experiment. Six PVYN-infected and six mock-inoculated C. album plants were placed, alternately in a circle inside the arena. Two hundred non-viruliferous winged M. persicae were placed in a black release container on a flight platform similar to the one described by Fereres et al. (1999). Aphids were released at 0.5 m above the test plants. The number of aphids settled on each test plant was counted at different intervals (0.5, 2, 4, and 48 h) using destructive methods. The experiment was replicated three times per time interval. For this purpose, after each time interval, each plant was covered with a plexiglass cylinder and transferred to the laboratory for aphid counting. Three replicates were performed for each time evaluation period. All assays were performed during daylight hours in a greenhouse at 25 ± 2°C. Contrasts were used to compare aphid numbers settling on infected or uninfected plants. Aphid Fitness on PVY-Infected Plants To determine if aphid progeny were affected by the presence of PVY in C. album, plants were infected with PVYO or PVYN; a mock-inoculated plant was used as a control. Seven plants per PVY strain or control were caged in individual screen sleeves. A single M. persicae alate was placed gently in each plant using a fine paintbrush. The alate was allowed to remain, feed on the plant, and reproduce for 48 h following the protocol described by Gildow (1980). After that period, the original alate was carefully removed and the offspring were counted and allowed to develop in a growth chamber for 14 d at 25 ± 2°C, photoperiod of 16:8 L:D, and 60–80% R.H. C. album as a PVY Source The ability to transmit PVYN from C. album to potatoes by M. persicae or M. euphorbiae was tested following a standardized procedure described by Fereres et al. (1993). Groups of 25–30 aphids per species were starved for 1 h before exposing them for an acquisition access period of 10 min on a PVY-infected C. album plant inoculated 3–4 wks earlier. After the acquisition access period, groups of five aphids were moved to a healthy receptor potato plant and were allowed to feed for an inoculation access period of 24 h. Aphids were then removed, and potato plants were sprayed with imidacloprid (Confidor) and transferred to a growth chamber at 25 ± 2°C with a photoperiod of 16:8 L:D and 60–80% R.H. All plants were tested after 4 wks using ELISA to determine PVY presence. The experiment was repeated three times (n = 25) for each aphid species. Data Analysis For the dual-choice assay, the relative percent of aphids settled on each type of host plant, in total and through time was evaluated using a Kruskal-Wallis since data could not be transformed to meet normality assumptions. For the free-choice settling assay, the mean relative percent of aphids settled on mock-inoculated or PVY-infected host plants was compared using a t-test at each time interval. Transmission study data were analyzed by summarizing number of infected potato plants for each species as a percentage of the total. This is a standard method of reporting transmission rates (Collar and Fereres 1998, Alvarez and Srinivasan 2005, Verbeek et al. 2009, Mello et al. 2011). For the host suitability study, the total number of aphids surviving on each plant was transformed using a Johnson transformation to assure normality and then compared across treatments (PVY strain) using a one-way analysis of variance. Inverted leaf blower and Berlese samples were compared using a Mann-Whitney test because the data could not be transformed to meet normality assumptions. All analyses were performed using Minitab 16 (Minitab, Inc., State College, PA). Results C. album, Other Weeds, PVY, and Aphids in the Field Besides C. album, tumble mustard Sisymbrium altissimum L. (Brassicaceae), redstem filaree E. cicutarium, prickly lettuce L. serriola, hairy nightshade Solanum sarrachoides Sendtner (Solanaceae), and bittersweet nightshade S. dulcamara (Solanaceae) were the most abundant. All weeds collected were tested for the presence of PVY. Only C. album and S. sarrachoides tested positive for PVY. From all weeds collected, 2.3 and 34% of C. album and S. sarrachoides, respectively, were PVY-positive. From those positive samples, 72% of the PVY found were PVYN; the remaining 28% was PVYO. In 2013, the highest number of aphids were collected in E. cicutarium, followed by S. dulcamara, L. serriola, S. altissimum, and C. album (data not shown). The most predominant aphid species near potato fields was Ovatus crataegarious Walker (mint aphid) (14% of aphids collected), followed by M. euphorbiae (13%), Hyalopterus pruni Geoffroy (mealy plum aphid) (12%), and Rophalosiphum madis Fitch (bird cherry oat aphid) (10%). Other aphids such as M. persicae, Brevicoryne brassicae L. (cabbage aphid), Hayhurstia atriplicis L. (chenopodium aphid), Aphis fabae Scopoli (black bean aphid), Acyrtosiphum pisum Harris (pea aphid), and the genera Nearctaphis, Dysaphis, Sitobion, Ceruarphis, Metopolophium, Hypemomyzus, Hyalomyzus, and Capitophora were also present but in lesser numbers (data not shown). In 2014, E. cicutarium harbored the highest number of aphids followed by L. serriola. As the previous year, O. crataegarious was the most abundant. The inverted leaf blower method collected a greater mean number of aphids per sample (25.08 ± 7.5) compared to the Berlese method (3.93 ± 1.4) (W = 68831; P < 0.001). Bioassays Table 1 shows the mean relative percentage of M. persicae alates settled on PVY-infected C. album or PVY-mock inoculated plants in the dual-choice tests. There were no significant differences for the relative percent of aphids settled on either infected of PVY-free plant (H = 0.02; df = 1; P = 0.900). However, there were differences on the relative percent of aphids on a host over time (H = 10.73; df = 5; P = 0.057). Table 1. Mean (±SE) relative percent of Myzus persicae Sulzer (Hemiptera: Aphididae) settled on PVY-infected C. album or mock-inoculated (control) Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  View Large Table 1. Mean (±SE) relative percent of Myzus persicae Sulzer (Hemiptera: Aphididae) settled on PVY-infected C. album or mock-inoculated (control) Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  Time (min)  Number of repetitions  PVY infected  PVY mock  1  30  27.33 ± 5.5  27.33 ± 5.5  10  30  25.89 ± 4.9  25.11 ± 4.8  30  30  27.44 ± 4.6  27.33 ± 4.7  60  30  30.78 ± 4.3  28.78 ± 4.0  120  30  32.89 ± 3.5  30.89 ± 3.5  180  30  31.78 ± 3.4  32.56 ± 3.1  View Large The mean (±SE) relative percent of M. persicae alates settled on a PVY-infected or PVY-mock inoculated plants can be seen in Table 2. There were no significant differences in the mean relative percent of M. persicae settled on mock-inoculated or PVYN-infected host plants at time intervals 0.5 h (t = 0.63; df = 2; P = 0.591), 2 h (t = 0.21; df = 3; P = 0.845), and 4 h (t = 1.05; df = 3; P = 0.371). However, the number of alates settled on healthy (mock-inoculated) plants was significantly higher than the one on infected plants at 48 h after release (t = 3.18; df = 4; P-value = 0.034). Table 2. Mean (±SE) relative percent of Myzus persicae Sulzer settling on PVY-infected C. album or mock-inoculated (control) Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  View Large Table 2. Mean (±SE) relative percent of Myzus persicae Sulzer settling on PVY-infected C. album or mock-inoculated (control) Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  Time (h)  Number of repetitions  PVY infected  PVY mock  0.5  3  10.07 ± 1.5  13.15 ± 4.6  2  3  23.47 ± 5.2  24.75 ± 3.1  4  3  23.05 ± 4.1  30.45 ± 5.7  48  5  12.59 ± 2.8  21.99 ± 0.9  View Large The mean number (± SE) of M. persicae progeny on mock-inoculated C. album plants was numerically higher when compared with number of progeny on PVYN or PVYOC. album plants but it was not statistically different (F = 0.89.; df = 2, 20; P = 0.427) (Table 3). Table 3. Mean number (±SE) of M. persicae present on PVYO, PVYN, or mock-inoculated (control) C. album 14 d after infestation with a single founding alate Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  View Large Table 3. Mean number (±SE) of M. persicae present on PVYO, PVYN, or mock-inoculated (control) C. album 14 d after infestation with a single founding alate Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  Host plant  Mean (SE)  N  PVY-mock (control)  5.0 ± 1.9  7  PVYN  2.4 ± 1.4  7  PVYO  2.6 ± 0.9  7  View Large Forty-four and 37.5% percent of potato plants tested positive by ELISA when exposed to M. persicae and M. euphorbiae, respectively. Potato plants were tested 4 wk after aphids were removed from plants. Discussion This study presents valuable information that establishes the role of C. album as a potential source of inoculum of PVY in the United States. Moreover, data from this study provide some insight regarding the role of the presence of PVY in potatoes and C. album and how that may affect the behavior, host preference, transmission, and fitness for M. persicae and M. euphorbiae under controlled conditions. Several weeds were tested for the presence of PVY, but only C. album and S. sarrachoides were PVY-positive. The latter one has been extensively studied (Alvarez and Srinivasan 2005, Srinivasan et al. 2006, Alvarez et al. 2007, Srinivasan and Alvarez 2008), hence our work focused on C. album. Although less than 3% of the C. album collected was PVY-positive, due to the proximity of this weed to potato field and geographical distribution (Nanayakkara et al. 2012, Krak et al. 2016), C. album can serve as a potential source of PVY. Samples that tested positive were collected in July and August, therefore PVY can be found not only in the potato crop itself in the tail end of the potato season (Singh 1987) in the Columbia Basin but also in C. album. Although negative for the presence of PVY in weeds such as S. altissimum, E. cicutarium, and L. serriola, the role of other weeds in the area as potential source of PVY remains to be investigated. Not surprisingly, there are greater numbers of aphids above ground as collected with the inverted leaf blower method. Weeds, including C. album, serve as a reservoir for aphids (data not shown). According to Agripedia (2017), over 200 crops can be grown in the state of Oregon alone, thus, it is not surprising to find such a diversity of aphids species in and around potato fields. Klein et al. (2017) reported the presence of over 30 aphid species in the area. Furthermore, Mondal et al. (2016) and Klein et al. (2017) indicated that the role of aphids such as M. persicae, M. euphorbiae, and R. padi as vectors or PVY is well understood, while the role of ‘other aphids’ as vectors of PVY, or other viruses, remain to be studied. Data from this study also identified characteristics of vector behavior related to PVY that might help explain how PVY is spread through a field. While searching for a suitable host, aphids land on host crops and nonhosts, to settle and reproduce. C. album is an integral part of the landscape, and several studies have determined the ability of C. album to serve as a sink for PVY (Singh 1987, Kaliciak and Syller 2009, Nanayakkara et al. 2012). However, according to our results, PVY-infected C. album does not induce the production of aphids, as was the case with Gildow et al. (1980) study, where infected host plants produced an abundance of winged aphids, increasing transmission. Srinivasan and Alvarez (2007) found that populations of M. persicae and M. euphorbiae were higher on potatoes infected with mixed infections of PVY and Potato leafroll virus (PLVR, Luteoviridae) another important potato disease. A similar trend was expected in this study. However, given the low mean number of aphids present after 14 d, it is apparent that C. album is not an ideal host for the M. persicae clones used in this study. Contrary to our findings, C. album is considered a host for this highly polyphagous species and has been used successfully as a host plant in other studies (Vorburger and Ramsauer 2008). M. persicae clones from different localities can present different preferences, fitness, and intrinsic growth rates for different hosts (Nikolakakis et al. 2003). While C. album did not lead to increased alate production in this study, the weed may still serve as a reservoir for PVY, particularly because it is not a preferred host plant. Instead, migrating aphids in search of a preferred host may probe infected plants and then migrate because of nonpreference, promoting the spread of PVY. Based on our results, M. persicae did not appear to have a strong preference for either healthy or PVY-infected plants. This was an unexpected finding with M. persicae, as several similar studies have found that this vector prefers infected host plants using a different host (Fereres et al. 1999, Srinivasan et al. 2006). However, Boquel et al. (2012) found similar results with PVY-infected and noninfected potatoes in a laboratory setting, where aphid vectors could not distinguish between infected and healthy hosts. It is possible that there are no distinctive differences in visual or olfactory cues between PVY-infected and healthy (mock-inoculated) C. album plants, particularly considering that infected plants appeared to be asymptomatic. If this is true, no preference would be anticipated (Fereres and Moreno 2009). While aphid vectors, namely M. persicae, appear to be unable to discriminate between infected and healthy hosts initially, they did develop a preference after extended feeding. This indicates that aphids landing on an infected host are likely to leave after extended feeding. This delayed nonpreference for infected plants could increase the spread of PVY due to aphids moving from infected plants to surrounding crops or vegetation. A similar relationship was found with Cucumber mosaic virus (CMV) and its aphid vector, Aphis gossypii Glover (Hemiptera: Aphididae) (Carmo-Sousa et al. 2014). Carmo-Sousa et al. (2014) found that A. gossypii was initially attracted to infected host plants but preferred to colonize noninfected plants, leading to increased transmission of CMV, also a virus with nonpersistent transmission. Both vectors, M. persicae and M. euphorbiae, transmitted PVY 44 and 37.5% of the time, respectively, demonstrating that C. album could serve as a reservoir for PVY. The transmission rate of PVY for M. persicae from potatoes to potatoes (preferred hosts) has been documented to be 57.5%, only slightly higher than the rate measured for C. album to potatoes in this study (Mello et al. 2011). For M. euphorbiae, the transmission rate for PVYN from tobacco to potato is 29%, lower than that found with C. album (De Bokx and van der Want 1987). Differences in host preferences for M. persicae clones have not resulted in significant differences in transmission rates for PVY (Kanavaki et al. 2006). Therefore, the transmission rates determined in this study should be broadly applicable to many populations of M. persicae. Regardless of the nonpreference of the M. persicae clones used in this study for C. album as a host, PVYN infection still influenced the behavior of M. persicae in a manner that would favor transmission. As the behavior identified for C. album likely differs with PVY-infected potatoes, a preferred host and another potential reservoir (Srinivasan and Alvarez 2007), future research should seek to identify these trends in a field setting. Undoubtedly, the prevalence of PVY in C. album in the field would be an important factor to assess to determine if C. album truly serves as a reservoir in the United States or Europe. Future research should seek to identify not only sources and the prevalence of PVYN in the field but also the abundance of the vectors themselves. While both of the vectors investigated in this study exhibited relatively high transmission rates, vector abundance plays an important role in the spread of PVY. It has been suggested with many viruses that are transmitted in a nonpersistent manner, and particularly PVY, that extremely abundant vectors with low transmission rates and limited preference for the host can still spread virus at economic levels (Pelletier et al. 2008). In spite of extensive research, this disease continues to persist in solanaceous field crops around the world and elude control measures. Although this study may provide some additional answers, more research is still needed to complete knowledge gaps in vector behavior and abundance, as well as identify more effective control measures. Acknowledgments The authors would like to acknowledge funding from NIFA-AFRI in the form of a postdoctoral fellowship, and the Oregon Potato Commission. Technical assistance was provided by M. Carmo-Sousa from the Fereres Research lab for research in Spain. 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Environmental EntomologyOxford University Press

Published: Apr 2, 2018

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