Recent aphid-vectored viruses in the northeastern U.S. led to extensive surveys of aphid (Hemiptera: Aphididae) species composition. We report the species composition and richness of alate aphids associated with processing snap bean (Phaseolus vulgaris L.; Fabales: Fabaceae) agroecosystems from field surveys conducted during 5 yr in New York and 3 yr in Pennsylvania. Rates of species accumulation were similar between the 2 states, and asymptotic, suggesting reasonably adequate sampling intensity. Our results suggest that about 95 to 100 aphid species are present as alates within these agroecosystems, a surprisingly high percentage (∼14 to 18%) of the total aphid richness. Host records suggest that 61% of the alate aphid species we collected from pan traps placed within snap bean fields were dispersing through this agroecosystem, originating from woody plants in the surrounding landscape. We compiled this information with a recent study of aphid species composition from peach orchards and an exhaustive inspection of museum samples, and present an updated list of the aphid species in Pennsylvania.
Aphids are a small, but diverse group of insects with an origin in the Jurassic and a total of 4800 species world-wide (Grimaldi & Engel 2005; Dixon 1985a; Dixon 1985b). They are primarily phloem feeders and when present in high densities can damage their host plant. Aphids excrete excess carbohydrates from their diet of phloem sap, providing a nutrient-rich substrate for sooty mold fungi to grow. Sooty mold can be a major problem in a number of agricultural crops because the mold can either render produce unmarketable or reduce plant quality of the commodity. Aphids are also important vectors of viruses that can kill their host plant or substantially reduce crop yield and quality (Agrios 2005). Some viruses are transmitted by aphids in a non-persistent, stylet-borne manner. They are obtained quickly by their aphid vector during short tasting probes, adhere to the stylet lining by binding to helper component proteins or directly to the stylet, and remain there until they are flushed out during another tasting probe (Ng & Falk 2006). Non-persistently transmitted viruses can be vectored by alates, sometimes by multiple aphid species (Gildow et al. 2008) regardless of whether or not there is reproduction on the plant host, and the epidemiology of these viruses can be influenced heavily by the alate aphid community.
Several viruses of this type have been introduced recently, or increased in frequency, in the northeastern U.S. One, plum pox virus (PPV), threatened the stone fruit industry following its arrival in the U.S. This virus causes sharka disease in parts of Europe and South America where it is endemic (Roy and Smith 1984; Rosales et al. 1998). Type D isolates were detected in the U.S. in Pennsylvania in 1999 (Damsteegt et al. 2001), and surveillance and eradication efforts of this invasive species included destruction of approximately 23% of the non-cherry stone fruit orchards of Pennsylvania (Wallis et al. 2005). As part of these efforts, studies were conducted to determine the potential aphid species that might serve as reservoir or route of transmission in the region where this virus was first detected (Wallis et al. 2005). Soon thereafter, in the early 2000s, Northeastern and Midwestern U.S., snap bean crops (Phaseolus vulgaris L; Fabales: Fabaceae.) had virus-like symptoms (leaf mosaic and blistering, deformed pods) and experienced dramatic yield loss (Larsen et al. 2002). Among the viruses detected were alfalfa mosaic virus, bean common mosaic virus, bean pod mottle virus, bean yellow mosaic virus, clover yellow mosaic virus, clover yellow vein virus (C1YVV), cucumber mosaic virus (CMV), tobacco streak virus and white clover mosaic virus (Grau et al. 2002; Larsen et al. 2002; Shah et al. 2006). CMV was the most prevalent virus detected in these snap bean fields (Larsen et al. 2002; Shah et al. 2006). As is the case with PPV, CMV is transmitted by aphids in a non-persistent, stylet-borne manner (Nault 1997). CMV-infected plants were often found in clumps in snap bean fields, which were consistent with aphid-initiated virus epidemics (Shah et al. 2005). CMV epidemics also occurred more frequently in New York than in Pennsylvania. The CMV epidemics coincided with the appearance of a newly invasive aphid, Aphis glycines Matusmura (Nault et al. 2009), and as was the case with stone fruit, the threat of viral epidemics led to extensive surveys of the alate aphids species composition in the affected crop.
These recent surveys of aphid collected from snap bean fields in Pennsylvania and New York, and peach orchards in Pennsylvania, were quite extensive. Also from Pennsylvania, J. O. Pepper specialized in aphid identification and actively collected them for most of the 20th century. His collections centered at his home in central Pennsylvania (State College) and included much of the surrounding forest and farmland. The bulk of his collection is housed in the Frost Entomological Museum (University Park, Pennsylvania), and he also contributed slides to the United States National Collection (Beltsville, Maryland). Pepper (1965) reported 345 species in a published list of the aphids of Pennsylvania and their host plants. To date, this is the most comprehensive published list of aphids for the state. However, since taxonomy and systematics are in flux, the names that Pepper published are currently out of date and in need of revision.
The purpose of this study was to identify the species composition and estimate aphid species richness in snap bean agroecosystems in the northeastern states from field surveys, and generate a current list of aphid species in this region using field survey data, literature, and an examination of the J. O. Pepper aphid collection.
Materials and Methods
Detailed methods for alate aphid collection in snap bean fields in Pennsylvania and New York were published in Nault et al. (2009). To summarize, we used water pan traps baited with a green ceramic tile (Webb et al. 1994) and filled with a 20% propylene glycol solution in snap bean fields in both states from 2002 – 2006 in NY and 2004 – 2006 in PA. Traps were installed in a total of 56 fields in western NY (12 each yr, except for 2004 which had 8 fields) and 18 fields in Centre county PA (6 each yr). The traps in Centre County formed an approximately 40 mile transect in the southern portion of the county roughly following state routes 45 and 192. The traps were checked weekly for aphids from the early trifoliate stage (early to mid Jul) until field harvest. Collection methods in the peach (Prunus pérsica (L.) Stokes; Rosales: Rosaceae) orchard are documented in Wallis et al (2005), and also used the water pan traps baited with a green tile. Trapping occurred during 2 yr in 2 orchards in central Pennsylvania.
For both studies, aphids were removed from pan traps and then stored in 70% ethanol (EtOH), then transferred to potassium hydroxide and heated for 1 h or until clear. Cleared aphids were rinsed for 10 min each in a sequence of 95% EtOH, absolute EtOH, and clove oil. Once rinsed, each aphid was placed on a drop of Canada balsam on a glass slide and positioned to expose diagnostic features before a coverslip was placed on top. Aphids collected in New York were identified by R. Eckel (RVWE Consulting, Frenchtown, New Jersey), whereas those from Pennsylvania were identified by W. Sackett and A. Bachmann using keys by Smith et al. (1992) and Blackman & Eastop (2000). Voucher specimens are located at the New York State Agricultural Experiment Station in Geneva, New York, and the Department of Entomology, Pennsylvania State University, University Park, Pennsylvania.
Alate aphid species representing > 1 % of the capture from water pan traps in commercial snap bean fields in Pennsylvana (2004–2006) and New York (2002–2006). Derived from Table 1 in Nault et al. (2009).
Species of alate aphids with host associations, collected from water pan traps in commercial snap bean fields in Pennsylvania (2004–2006) and NY (2002–2006), and from similar traps in peach orchards in central Pennsylvania (2003–2004, wallis et al. 2005). Primary and secondary host plant associations for North America taken from Blackman & Eastop (1994 [AWT], 2000 [AWC], and 2006 [HPS]).
Table 2. (Continued)
1 Species of alate aphids with host associations, collected from water pan traps in commercial snap bean fields in Pennsylvania (2004–2006) and NY (2002–2006), and from similar traps in peach orchards in central Pennsylvania (2003–2004, wallis et al. 2005). Primary and secondary host plant associations for North America taken from Blackman & Eastop (1994 [AWT], 2000 [AWC], and 2006 [HPS]).
Table 2. (Continued)
2 Species of alate aphids with host associations, collected from water pan traps in commercial snap bean fields in Pennsylvania (2004–2006) and NY (2002–2006), and from similar traps in peach orchards in central Pennsylvania (2003–2004, wallis et al. 2005). Primary and secondary host plant associations for North America taken from Blackman & Eastop (1994 [AWT], 2000 [AWC], and 2006 [HPS]).
Table 2. (Continued)
3 Species of alate aphids with host associations, collected from water pan traps in commercial snap bean fields in Pennsylvania (2004–2006) and NY (2002–2006), and from similar traps in peach orchards in central Pennsylvania (2003–2004, wallis et al. 2005). Primary and secondary host plant associations for North America taken from Blackman & Eastop (1994 [AWT], 2000 [AWC], and 2006 [HPS]).
Species rarefaction curves were calculated for the Pennsylvania and New York collections individually and for both states combined using Estimates (Colwell 2005).
A complete list of aphids from Pennsylvania was compiled using the J. O. Pepper Aphid Slide Collection, which is housed at the Frost Entomological Museum (University Park, Pennsylvania), as well as species recorded in Pepper (1965). We searched the slide collection in addition to using Pepper (1965) because Pepper continued to collect aphids and make slides into the late 1980s, but did not publish any updates to his original 1965 paper. Because the collection and Pepper (1965) contained aphid species names from the early 20th century, we consulted 2 online aphid databases to ensure that the final list used the most current nomenclature (Aphid Species File — http://aphidspeciesfile.org, accessed 22-IV-2012 and Aphids on the World's Plants — http://www.aphidsonworldsplants.info/, accessed 1-XI-2013). We combined our findings from the Pepper collection material with the results of our pan trapping study and Wallis et al. (2005) to create a more current list of the aphids of Pennsylvania (Tables 3–11).
Species in six subfamilies of the family aphididae occurring in Pennsylvania.
In snap bean fields in New York and Pennsylvania, a total of 8,821 aphids were identified, with 7,484 from New York and 1,337 from Pennsylvania. A total of 97 species were caught; 71 from New York and 41 from Pennsylvania. We were unable to identify only 254 (2.8%) of the aphids. Of the aphids captured, those species representing 1% or greater of the total number caught in either state are listed in Table 1 (originally published in Nault et al. 2009) with their abundances. A comprehensive list of all aphid species found in Pennsylvania and New York snap bean fields is shown in Table 2 along with their host associations based on Blackman & Eastop (1994, 2000, and 2006). From this host information we estimated that 61 percent of the species dispersing through snap bean fields in both states were most likely coming in from the surrounding forests as their hosts are woody, not herbaceous, species (Fig. 1).
Species accumulations followed asymptotic patterns (Fig. 2) suggesting reasonably adequate sampling of the aphid species present as alates in commercial snap bean fields. Overall, there were fewer aphids collected in Pennsylvania, but based on the rarefaction curve there were a similar number of total species represented in a sample of the same number of individuals (Figs. 2 and 3, at 1,250 individuals there would be 45 species sampled in Pennsylvania and 50 in New York). Based on the historical collections reported by Pepper, there are approximately 350 aphid species in Pennsylvania. Historical reports in Leonard (1963) suggest that there are approximately 430 aphid species in New York.
Species in the subfamily Aphidinae, tribe Aphidini occurring in Pennsylvania.
Species in the subfamily Calaphidinae occurring in Pennsylvania.
Species in the subfamily Chaitophorinae occurring in Pennsylvania.
Combining the list of aphids collected from snap bean fields, peach orchards and those published by J. O. Pepper in 1965, we developed a new, more comprehensive list of the aphids present in Pennsylvania. We found 7 species present in our collections that were not present in the slide collection housed in the Frost Entomological Museum (University Park, Pennsylvania) or published in Pepper (1965) (Table 3). One of these aphids, Aphis glycines Matsumura, was introduced to the US around the turn of the 21st century and is now widespread throughout the Midwest, Northeast and southeastern Canada (Ragsdale et al. 2011).
Our passive trapping in snap bean fields alone yielded a surprisingly high percentage of the species present throughout Pennsylvania and New York (∼14% and ∼18% respectively). Our sampling method concentrated on only one habitat (commercial snap bean fields), but did intercept aphids moving from the surrounding forests and hedgerows. The high degree of landscape heterogeneity and crop diversity in the trapping areas includes plant species that serve as hosts for many of the aphid species that represented less than 1% of the total capture (Pfleeger et al. 2006). These aphids were captured in very small numbers (mostly singletons), and are not important contributors to the plant virus epidemics reported by Wallis et al. (2005) and Nault et al. (2009).
Of the aphids we captured, 2 species were especially notable; Therioaphis trifolii Monell, which comprised 31.8% of the identified aphids, and A. glycines which represented 18.2 % of the identified aphids. Both of these aphids were introduced to North America (A. glycines from Asia and T. trifolii from Europe) and were quite destructive to crops immediately after their introduction (in soybean and alfalfa, respectively). Aphis glycines continues to cause significant economic damage in soybean (Ragsdale et al. 2011). While not known to colonize Phaseolus spp., both species are competent vectors of the legume strain of CMV (Gildow et al. 2008).
Species in the subfamily Drepanosiphinae occurring in Pennsylvania.
Species in the subfamily Eriosomatinae occurring in Pennsylvania.
Species in the subfamily Lachninae occurring in Pennsylvania.
The intermittent appearance of CMV in central Pennsylvania snap bean crops could be influenced by a unique agricultural landscape. Agricultural fields are located in valleys bordered by the low, but steep, forested ridges of the Appalachian Mountains. The ridge and valley system might be acting like a barrier, keeping CMV out for most of the season. We did not search for a CMV reservoir outside of testing a few alfalfa fields, which were also negative for CMV. It is possible, that much like our A. glycines population, legume strains of CMV may be transient. If this is the case, migrating aphids may be scrubbed of virions when they land in one of the many bordering forests containing many non-host plants.
The Pepper (1965) aphid list in addition to the Pepper slide collection allowed us to compile a comprehensive list of the aphids present in Pennsylvania, but the nomenclature was in need of updating. Our efforts to update the nomenclature, and incorporate our more recent sampling efforts, resulted in a modern list of aphids of Pennsylvania that includes recently introduced species.
The authors would like to thank Fred Gildow, William Sackett and Dana Roberts. Funding for this work was provided by the Pennsylvania Vegetable Growers Association.