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«Biology of rosy apple aphid, Dysaphis plantaginea Passerini, (Homoptera: Aphididae) on its summer hosts in eastern Washington AUTHORS. STEPHEN D. ...»

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THE PAN-PACIFIC ENTOMOLOGIST

87(4):273–283, (2012)

Biology of rosy apple aphid, Dysaphis plantaginea Passerini,

(Homoptera: Aphididae) on its summer hosts in eastern Washington

AUTHORS. STEPHEN D. COCKFIELD1,2, ELIZABETH H. BEERS1, KEITH S. PIKE3,

& GEORGE GRAF3

Tree Fruit Research & Extension Center, Washington State University, 1100 N.

Western Ave., Wenatchee, Washington 98801

Irrigated Agriculture Research & Extension Center, Washington State University, 24106 N. Bunn Rd., Prosser, Washington 99850 Abstract. In surveys of apple-production areas east of the Cascade Mountains of Washington, broadleaf plantain, Plantago major Linnaeus (Plantaginaceae) was common throughout while narrowleaf plantain, P. lanceolata Linnaeus, was most common south of Orondo, Douglas County (47.7u latitude). Rosy apple aphid was the most common aphid on these two herbaceous plants; however, colonies were scarce, on only 19% of broadleaf and 11% of narrowleaf plantain samples. Colonies were also generally small, fewer than 25 individuals.

Adult rosy apple aphid was collected on plantain from late May through October. Adults reached their highest levels in July before declining in August. Colonies increased again in September and October. Relatively few predators (mainly syrphids) and parasitoids (two species of Aphidius) were found on plantain. On apple, the most common predators were the mirid Campylomma verbasci (Meyer-Dur), earwigs, coccinellids, cecidomyiids and syrphids;

¨ the most common primary parasitoid was Lysiphlebus testaceipes (Cresson). Secondary or hyperparasitoids consistently outnumbered the primary parasitoids. Plantains growing outside of orchards but within 1 km of apple trees had the highest incidence of RAA infestation. The potential for management of RAA on its summer hosts is discussed.

Key Words. Rosy apple aphid, Dysaphis plantaginea, host plant, phenology, predator, parasitoid.

INTRODUCTION

Rosy apple aphid, Dysaphis plantaginea Passerini, is a destructive pest of apple, Malus 3 domestica (Borkhausen) (Rosaceae), in the apple-growing regions of Europe and North America (Beers et al. 1993, Hemptinne et al. 1994, Brown and Mathews 2007, Brown and Myers 2010). While conventional orchards suffer sporadic damage, organic orchards can be severely affected by this pest. Aphid feeding causes distorted growth of leaves and shoots, misshapen and stunted fruit, as well as deposition of honeydew on healthy fruit. Infestations are difficult to detect at bud break when hatch of the overwintered eggs occurs. Colonies, however, can increase rapidly in size and number after apple bloom (late April-late May) and can severely damage trees by mid-summer. As colonies develop, the aphids induce leaf curling, which partially shelters the aphids from pesticide applications and natural enemies (Brown and Mathews 2007), making them more difficult to control.

Rosy apple aphid spends 2–7 generations on apple before producing winged forms which migrate to the summer host, plantain, Plantago spp. (Plantaginaceae) (Baker and Turner 1916). The common name ‘‘rosy’’ indicates the color of the aphids on apple (pinkish purple); on the summer host, a yellow-green color morph is produced.

Three to eight generations develop on the summer host before migrants return to Corresponding author: PO Box 1461, Malott, Washington 98829, E-mail: pest@bossig.com The Pan-Pacific Entomologist panp-87-04-04.3d 27/1/12 01:21:50 273 Cust # 2011-30 274 THE PAN-PACIFIC ENTOMOLOGIST Vol. 87(4) apple in the fall. Blommers (1999) divided the annual cycle into five periods critical for management and control, including development on the summer host, and noted that research focused on one period, the outbreak phase on apple. The period spent on the summer host has been rarely studied in situ, and the most detailed work has been done in Europe (Bonnemaison 1959, Blommers et al. 2004). Orchard management practices, such as mowing, have been shown to influence growth of the summer host and thus the summer population of rosy apple aphid, although this tactic has shown little impact on subsequent populations on apple (Brown and Myers 2010).

Agricultural land in the arid areas of western North America supports three species of plantain (Plantago): the perennial narrowleaf (P. lanceolata Linnaeus) and broadleaf (P. major Linnaeus) plantain, and the annual wooly plantain (P.

patagonica Jacquin) (Whitson et al. 2002). Narrowleaf and broadleaf plantain originated in Europe while wooly plantain is native to western North America. The emergence of rosy apple aphid as a pest of apple in the arid interior regions of the Pacific Northwest appeared to follow the spread of narrowleaf plantain from the Atlantic coastal regions (Matheson 1919). In eastern North America, although broadleaf plantain is also a summer host, it is less preferred (Ross 1915, Brittain 1916). However, in the interior of British Columbia, rosy apple aphid occurs on broadleaf plantain, the most common species in apple orchards (Brown and Myers 2010). Wooly plantain has not been reported as a summer host. To date, there are no studies on the host status of the three plantain species in eastern Washington State.

Biological control of rosy apple aphid on apple trees has been studied in eastern North America (Brown and Mathews 2007) and Europe (Wyss et al. 1999, Minarro ˜ et al. 2005, Dip et al. 2010). Research has been directed at the most common natural enemies such as the coccinellids Harmonia axyridis Pallas (Brown and Mathews 2007) and Adalia bipunctata L., the syrphid Episyrphus balteatus (DeGeer), the midge Aphidoletes aphidimyza (Rondani), and the braconid Ephedrus persicae Froggatt (Wyss et al. 1999, Peusens et al. 2006). Although natural enemies can considerably impact rosy apple aphid populations in apple trees (Brown and Mathews 2007, Stewart-Jones et al. 2008, Wyss et al. 1999), biological control as a management tool in commercial orchards has been elusive. There is little recent information on the natural enemies of rosy apple aphid in Washington State (Carroll and Hoyt 1986, Pike et al.





1996), and almost none on the natural enemies attacking this species on plantain.

The objectives of the present study were to survey narrowleaf and broadleaf plantain in the irrigated arid regions of eastern Washington State and determine the relative abundance of rosy apple aphid on these species; to determine the seasonal fluctuations in populations on the summer hosts; and lastly, to identify common predators and parasitoids of rosy apple aphid on apple and in association with the summer hosts.

METHODS AND MATERIALS

Survey of Aphids on Plantain. A survey was conducted by sampling narrowleaf and broadleaf plantain for summer generations of rosy apple aphid in 2005 and 2006.

One or both species were sampled per site depending on presence in the orchard. We also checked each site for wooly plantain. A total of 101 sites were sampled in Yakima (42 sites), Walla-Walla (1), Skamamia (6), Okanogan (6), Klickitat (7), Kittitas (2), Grant (3), Franklin (1), Douglas (7), Chelan (9), and Benton counties The Pan-Pacific Entomologist panp-87-04-04.3d 27/1/12 01:21:50 274 Cust # 2011-30 2012 COCKFIELD ET AL.: BIOLOGY OF ROSY APPLE APHID 275 (13) in Washington State and Umatilla County (4) in Oregon. Half of the sites (50) were in apple orchards. Most others (31) were in orchards other than apple, or in irrigated crops (4) such as blueberry, Vaccinium spp. (Ericaceae) or grape, Vitis vinifera Linnaeus (Vitaceae), within apple-growing areas. A few (12) were in irrigated lawns of city parks. The latitude and elevation were recorded to determine the pattern of distribution of each species.

Samples were collected at each site from May through October to survey aphid species. Sites were sampled once (68 sites) or two or more times (33). Each plant sample consisted of cutting plants at ground level, with sufficient material taken to fill a 4-liter plastic bag. A bag held up to a dozen small plants or one large plant.

Aphids were obtained by extraction in a Berlese funnel (2 h exposure, with temperature at the top of funnel held at 40u C) and preserved in 70% ethanol. Only adult aphids could be identified to species. A chi-square test was performed on the number of samples of each plant species positive or negative for the presence of rosy apple aphid. The seasonal abundance of rosy apple aphid was determined by plotting the number of identified aphids (adults) and the date of collection.

Distance from Apple Trees. Sample sites were divided into three categories to determine the likelihood of rosy apple aphid living at a distance from its woody host (apple). Sites were categorized as within an apple orchard, outside an apple orchard but within 1 km from apple trees, or greater than 1 km from apple trees. Samples were counted as either positive or negative for the presence of adult rosy apple aphid.

A chi-square test was conducted to detect any changes in the probability of positive samples with distance from apple trees.

Natural Enemies. Predators were extracted from the fresh plant samples with a Berlese funnel as described above. A duplicate sample was collected upon each site visit in Okanogan, Chelan, and Douglas Counties and held for rearing parasitoids from parasitized aphids. Plantains were collected in the same manner as the aphid survey samples and transferred to a 6-liter plastic box with a ventilated lid held at room temperature for one month. Rosy apple aphids were cryptic and uncommon in these samples, often consisting of a single specimen. Therefore, it is not known which species of aphids were parasitized; paired samples used for aphid extraction indicated possible aphid hosts. Parasitoids were identified using various keys and descriptions (Smith 1944, Gibson et al. 1997, and Pike et al. 1997) for primary parasitoids (Aphelinidae and Braconidae); Dessart 1972, Takada 1973, Fergusson 1980, Andrews 1978, Gibson et al. 1997 for secondary parasitoids (Megaspilidae, Charipidae, Pteromalidae) and by comparison with verified specimens. Voucher specimens of aphids and parasitoids are deposited in collections at Washington State University, Prosser, Washington.

Natural enemies of rosy apple aphid were also collected from infested apple trees from May through August at several locations in Okanogan (3), Douglas (4), Chelan (4), and Grant (1) counties in 2005 and 2006. Samples from apple consisted of 4-liter plastic bags filled with infested foliage, up to 1000+ aphids per sample. Predators and parasitoids were collected directly from the samples, and additional adult parasitoids were reared from samples as described above.

–  –  –

Figure 1. Plantains, Plantago spp.

, at 101 sample sites in apple-production regions of eastern Washington State and northern Oregon. A, elevation and species found at each site. B, location of the sites (filled squares), major towns (open squares), mountains, and rivers.

ranged from less than 100 m along the southwestern Columbia River Valley to greater than 800 m in the foothills of the Cascade Mountains. Broadleaf plantain was found throughout the Columbia and Okanogan River Valleys at a broad range of elevations. However, narrowleaf plantain was rarely found north of 47.7u latitude (near Orondo, Douglas County), although it occurred at a range of elevations south of Yakima (46.6).

Survey of Aphids on Plantain. Aphids in general were uncommon on plantains;

only 24% of the samples were positive for aphids of any species. Rosy apple aphid was detected on 74 (19%) of the 387 samples of narrowleaf plantain. Six (2%) had a few specimens of Aphis spp., six (2%) had Aulacorthum solani (Kaltenbach), six (2%) had Rhopalosiphum padi (Linnaeus), five (1%) had Pemphigine sp., and three (1%) had Myzus ascalonicus Doncaster. Seven other species, most likely errant, were collected in single samples. The numbers of aphids in the samples was generally low (ca. 25 or fewer), but one sample contained an extremely high number of rosy apple aphid, estimated to be over 2000 individuals.

Of the 297 broadleaf plantain samples collected, 32 (11%) were positive for adult rosy apple aphid, or about half the percentage of positive samples found on narrowleaf plantain. The probability of encountering adult rosy apple aphid on the two species was not equal (x2 5 8.94, df 5 1, P 5 0.003). Eight samples (3%) were infested with Aphis spp., six (2%) had R. padi, four (1%) had Rhopalosiphum spp., and three (1%) had A. solani. Six other aphid species were collected in single samples.

–  –  –

Figure 2. Number of adult rosy apple aphids extracted from a 4-liter volume of plantain vegetation collected from agricultural land on different dates in 2005 (n 5 201) and 2006 (n 5 465).

Seasonal Abundance. A total of 201 plantain samples were collected in 2005 and 465 in 2006. The sample with over 2000 rosy apple aphids, collected on 14 July 2005, was omitted from the graph. The pattern of seasonal abundance of rosy apple aphid on plantain was similar in both years (Fig. 2). Densities were low in May, when migration from the winter host was starting, peaking in late June and early July.

Populations dipped in August, but rose again in September and October.

Distance from Apple Trees. Rosy apple aphid was found in 77 (13%) of 573 plantain samples (both species) taken in apple orchards. However, this species was found in 15 (31%) of 48 samples from sites outside orchards but within 1 km from apple trees and 11 (18%) of 62 samples from sites farther than 1 km. There was a significant difference in probability of infestation based on distance from the woody host (x2 5 11.35, df 5 2, P 5 0.0034). Plantain found outside an apple orchard but within 1 km from apple trees had the highest probability of infestation.



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