The taxonomy of crop pests: The aphids - Canacollcanacoll.org/Hemip/Staff/Foottit/PDFs/Miller_and_Foottit c20.pdf · their taxonomy is in good order. This percep-tion might lead to

Chapter 20

The taxonomyof crop pests:The aphidsGary L. Miller1 and Robert G. Foottit2

1 Systematic Entomology Laboratory, PSI, Agricultural Research Service, U.S.Department of Agriculture, Bldg. 005, BARC-W, Beltsville, MD 20705, USA;2 Agriculture and Agri-Food Canada, Canadian National Collection of Insects, Ottawa,ON, K1A 0C6 Canada

‘For the most part, the most economically important insect and mite pests are known to science,and their position in our classification system is resolved’.

— Anonymous, USDA, ARSResearch Action Plan, 2004

Insect Biodiversity: Science and Society, 1st edition. Edited by R. Foottit and P. Adler© 2009 Blackwell Publishing, ISBN 978-1-4051-5142-9

463

T here is a perception that certain insect pestsof crops are well-studied biologically and thattheir taxonomy is in good order. This percep-

tion might lead to the impression by those who areunfamiliar with the intricacies of acquiring taxonomicunderstanding of biological diversity that we know allthere is to know. In fact, science is a discipline thatcontinually builds on its previous discoveries and tech-nologies as it advances our knowledge. Much researchis needed even in economically important insect groupswhose taxonomy might be regarded as advanced. Inthis chapter, using the Aphidoidea as an exampleand, in particular, using the early works of NorthAmerican aphidology as background, we explore var-ious dimensions of taxonomic knowledge in this pestgroup.

HISTORICAL BACKGROUND

Plants have been cultivated and traded since perhaps8000 BC (Huxley 1978) and insect pests have longplagued humans and their crops. Ancient civilizationsrecorded swarms of locusts and other insect pestilence(Harpaz 1973, Konishi and Ito 1973). As humansexpanded crop cultivation, associated insect problemssoon followed. The European colonists of the NewWorld faced their own set of insect-related problemswith the cultivation of both native and introducedcrops. For example, tobacco, which is native to theNew World, experienced insect damage from horn-worms and flea-beetles from the outset of its cultivation(Garner 1946). The introduction of new plants alsobegan early during European colonization. Sugarcanewas transported from the Canary Islands to Hispaniolaon Columbus’s second voyage in 1493 (Deerr 1949).Some of these early introduced plants also had theirassociated pests, including aphids. The close associa-tion of aphids with their hosts meant those insects andtheir eggs were being transported through commerceas well (Howard 1898). The cabbage aphid, Brevico-ryne brassicae (Linnaeus), was noted in North Americaas early as 1791 (Miller et al. 2006). Early entomolo-gists were well aware that commerce and travel wereresponsible for the transport of some of these pests.In 1856, Asa Fitch speculated that B. brassicae wasbrought along with cabbage plants on shipboard cargo(Miller et al. 2006).

ECONOMIC IMPORTANCE AND EARLYTAXONOMY

Aphids are small, soft-bodied insects mostly rangingbetween 1.5 and 3.5 mm in length (Blackman andEastop 2000); they feed on plants with piercing-sucking mouthparts. Besides the mechanical damagethey cause by this action, aphids also serve as thelargest group of vectors of plant viruses (Eastop 1977,Chan et al. 1991). The damage is further compoundedby fouling of the host plant with honeydew. Notedas long ago as in Reaumur’s (1737) work, honeydewis excreted from the anus and is high in plant sugarsand other compounds. Besides having an influenceon predators (Glen 1973) and parasitoids (Faria2005), it serves as a substrate for the growth of fungalcomplexes that cause sooty mold (Westcott 1971).In addition to reducing the photosynthetic ability ofplants, sooty mold reduces a plant’s aesthetic marketvalue (Worf et al. 1995).

More than 250 species of the Aphidoidea (in thefamilies Adelgidae, Phylloxeridae, and Aphididae) feedon agricultural or horticultural crops (Blackman andEastop 2000). While this figure only represents approx-imately 5% of the world aphid fauna, the economicconsequences of aphid damage are huge. For example,Wellings et al. (1989) estimated for 13 selected cropsthat aphids contribute about 2% of the total lossesattributed to insects and believed that figure was agross underestimate. Aphids are one of the importantvegetable pests (Capinera 2002). Of the 80 groups ofvascular plants in the world only 8 lack aphids, andthose groups represent only 3% of the plant species(Eastop 1978).

Most aphid references refer to economic impact andsome of the very earliest works of the sixteenth andseventeenth centuries have been noted by Blackmanand Eastop (2000). Although aphids have extraordi-nary damaging horticultural effects, some of society’searly interest involved their beneficial or positiveattributes. Galls of certain aphid species (e.g., Baizongiapistaciae [Linnaeus] and Schlechtendalia chinensis [Bell])have been used for centuries in medicine, tanning,and dyeing (Fagan 1918). Woodcuts as early as 1570illustrate galls of B. pistaciae on Pistacia (Blackman andEastop 1994) and by 1596 ‘Chinese galls’ of Melaphischinensis [= S. chinensis] on Rhus javanica (a sumac)were noted as insect induced (Eastop 1979).

The taxonomy of crop pests: the aphids 465

Fig. 20.1 (a) (top). Some of the early aphid work producedby Reaumur (1737) included his woodcuts, which were usedfor identification. Linnaeus (1758) referenced both of theaphid species in his work. (Figs. 1–4. Aphis rosae(= Macrosiphum rosae). Figs. 5–15. Aphis sambuci.)(b) (bottom). Nearly three centuries later, short DNAsequences from a uniform locality of the genome (barcodes)for Macrosiphum rosae and Aphis sambuci are being explored

Prior to Linnaeus’s (1758) work, many of thepapers concerning aphids had little taxonomic value.A notable exception is Reaumur’s (1737) ‘Memoirespour servir a l’histore des insectes’. This work includedinformation on aphid life history and biology as

well as detailed illustrations. Linnaeus (1758) usedReaumur’s (1737) work as a reference in connectionwith a number of the species he named. The nominalspecies, Aphis sambuci Linnaeus (1758), is illustratedin habitus and as several detailed figures on one ofReaumur’s (1737) plates (Fig. 20.1a). For aphids(sensu lato), Linnaeus (1758) described 1 genus (Aphis)and 25 species, as well as the genus Chermes, whichcontained 1 adelgid species.

EARLY APHID STUDIES – A NORTHAMERICAN EXAMPLE

Some of the earliest, if not the earliest, systematic workon North American aphids was that of Rafinesque1

(1817, 1818), who described 36 species and 4 sub-genera. Rafinesque’s (1817) interest and intent ‘tostudy all the species of this genus [Aphis] found in theUnited States’ was initiated by his observations thatthey were ‘often highly injurious’ to their host plants.Other early North American workers often treated theeconomic importance of aphids. For example, Har-ris’ (1841) report on insects injurious to vegetationincludes sections on ‘plant-lice’. While little taxonomicinformation was included, Harris did incorporate obser-vations on life history, biology, predators, host plants,and control. Fitch’s work (e.g., Fitch 1851) in themid-1800s not only included life history informationon aphids but also new species descriptions. Between1851 and 1872, Fitch proposed names for 58 species ofAphidoidea (Barnes 1988). Walsh’s (1863) treatmentof the Aphididae (sensu lato) included his ‘SynopticalTable of U.S. Genera’, which was essentially a key.By the 1870s–1880s, entomologists such as Thomas(1877), Monell (1879), and Oestlund (1886) werespecializing in the study of aphids.

Difficulty in distinguishing aphids was noted as earlyas Linnaeus (Walsh 1863) and early workers in NorthAmerica also lamented the lack of study and knowledgeof the aphids. Walsh (1863), in Illinois, complainedabout the need for ‘Public Scientific Libraries’ that hismore fortunate ‘Eastern brethren’ had. He added thatthe ‘specific distinctions’ of the aphids themselves were‘generally evanescent in the dried specimen’. Thomas(1879) reiterated Walsh’s comments and believed thereasons for the neglected study of aphids rested on

1Hottes (1963) proposed to suppress Rafinesques’s aphidnames and subsequent workers (e.g., Remaudiere andRemaudiere 1997) have recorded his names as unavailable.

466 Gary L. Miller and Robert G. Foottit

two issues, the difficulty in preserving specimens andthe paucity of systematic works, most of which wereEuropean. With delays of months to years to procurea reference work (Oestlund 1886), the situation forsome was daunting. In 1886, Oestlund still consid-ered the systematics of the aphids ‘unsatisfactory’ butregarded the lack of literature as the greatest want forthe ‘frontier naturalist’. Later, Oestlund’s (1919) tonechanged when his concern focused on the then- recentaphid classification difficulties ‘on account of the greatnumber of new genera and species made known’.

Especially noteworthy with Oestlund’s (1886) ear-lier concern about the state of aphid study is hisfailure to mention the difficulty of preserving speci-mens. By the 1860s, North Americans, along with theirEuropean counterparts, were making progress in pre-serving pinned insect specimens in cabinets (Sorensen1995). Instead of being pinned or glued on smallboards, aphids were routinely preserved on micro-scope slides.2 Changes in the way aphids were beingstudied and preserved were accompanied by changesand improvements in species descriptions and toolsfor identification. The earliest North American aphiddescriptions (e.g., Rafinesque 1817, 1818; Haldemann1844) were based almost entirely on coloration, gen-eral appearance, and host association. Subsequentworkers (e.g., Walsh 1863, Riley 1879, see also Milleret al. 2006) relied on descriptions of general appear-ance but also routinely included measurements of bodylength and wing length in their species descriptions.Walsh’s (1863) generic descriptions added compar-isons to other morphological structures (e.g., relativelength of siphunculi in comparison to tarsal length), apractice that was uncommon at the time. By the late

2Pergande’s ledger and card file at the United States Aphi-doidea Collection, Beltsville, Maryland, provides an excellentrecord of the progression of preserved aphid specimens. His ear-liest ledger entries, while he was in St. Louis, Missouri (1877),record collected aphid specimens as being pinned, mounted onboards, or preserved in alcohol. By 1878 in Washington, DC,he noted aphids as being ‘mounted in balsam’ and preserved inalcohol. Other aphidologists were also using balsam-mountedspecimens, as Pergande noted the receipt of ‘Pemphigus acerisn. sp.’ from aphidologist Monell that were ‘mounted on slide’in 1878. At the USNM, Pergande was evidently still gluingspecimens to pieces of board as late as 1880 but he also‘mounted some on a slide’. In 1903, Pergande recorded thathe examined ‘the old Fitch collection of Aphides’ for Aphis maliFitch, which were ‘pinned’ and then ‘mounted all of them inbalsam’. Slide mounting had indeed become a standard wayto study and preserve the aphids by the turn of the century.

1880s, a new dimension was added to the descriptionsof aphid morphology. Relative descriptors of antennalsegment length, such as ‘about half as long as the pre-ceding’ (e.g., Monell 1879) or ‘subequal’ (e.g., Oestlund1886), were being replaced with discrete measure-ments in one-hundredth of a millimeter (e.g., Oestlund1887). These changes generally corresponded withmajor advances that were being made in microscopy,especially the development and design of microscopeobjectives and lenses that maximized both magnifica-tion and resolution.

Other changes were taking place in aphid taxonomyin North America. Earliest works reflected Linnaeus’s(1758) simple classification (e.g., Haldemann 1844).The list of aphid species referable to Linnaeus’s sin-gle genus, Aphis, was being expanded. The taxonomicworks of European aphidologists such as Kaltenbach(1843), Koch (1854), Passerini (1860), and Buck-ton (1876) influenced the early taxonomic studies ofthe North American workers (Walsh 1863, Thomas1877, 1878, 1879). While these works included keysto genera and tribes, species treatments consisted ofsimple descriptions and lists. Monell’s (1879) contri-bution is worth mentioning because he also developedidentification keys for related species of select genera.

The use of species keys advanced the ability toidentify aphids. Oestlund’s (1887) study of Minnesotaaphids provided detailed keys to subfamilies, genera,and species of select genera. In what was a synthesisof the knowledge of North American aphids, he alsoincluded detailed species descriptions, an up-to-dateliterature review of North American authors, anda host plant list. It was also a reflection of thefruits of government-sponsored entomology at thattime (Sorensen 1995). Of the 65 publications listedin Oestlund’s (1887) aphid bibliography, nearly75% of the works reflect government-sponsored orgovernment-associated entomology.

A major work published at the beginning of the twen-tieth century, Hunter’s (1901) catalog ‘The Aphididaeof North America’, provided much of the pertinent lit-erature on and taxonomy of North American aphids.Various authors had published lists of described speciesbut Hunter (1901) not only contributed an expandedspecies list but also included the known systematicand economic literature referable to the species, alongwith host plant information. Knowledge of NorthAmerican aphids had grown from 36 species pro-posed by Rafinesque (1817, 1818) to 166 speciesidentified by Monell (1879), an increase of nearly five


times, to 325 species identified by Hunter (1901), anincrease of more than nine times. The compilation ofthe North American aphid fauna would continue togrow to 1416 species (Foottit et al. 2006).

RECOGNIZING APHID SPECIES

As the number of recognized aphid species has grownsince Linnaeus (1758) (Fig. 20.2), there have beendifficulties in recognizing or even defining an aphidspecies (e.g., Shaposhnikov 1987). The conceptual andoperational use of species concepts and definitions inaphid taxonomy throughout the world is complicatedby their reproductive biology. Aphids are characterizedby cyclical parthenogenesis, but there may also bepurely anholocyclic populations not manifesting thesexual phase of the life cycle. Recommendations havebeen made for the taxonomic treatment of aphidpopulations that are permanently parthenogenetic;

formal species status could be given to a biologicallyrecognizable anholocyclic group derived from a sexualancestor (Blackman and Brown 1991, Foottit 1997,Havill and Foottit 2007).

One way to observe trends in aphid systematics isto compare the rates of synonymy and the accumu-lation of new taxa; as more research is done, morespecies are described and new synonymies are discov-ered (Fig. 20.2). From 1758 (when Linnaeus’s workwas published) until 1840, the number of describedvalid aphid species (sensu lato) and cumulative aphidnames was only 109 and the difference between the twoparameters remained relatively small. Starting around1841, shortly before Kaltenbach’s (1843) work, thedifference between cumulative aphid names and cumu-lative valid names over time began to increase, albeitgradually, until about the late 1910s. The numberof valid species increased nearly eightfold from 129to 1011 species between 1841 and 1919. Between1840 and 1949, there were nearly twice as many

Fig. 20.2 (Inset). Cumulative aphid names proposed versus cumulative currently valid aphid names from 1758 to 2000.(Main). Number of proposed aphid names versus valid aphid names from 1758 to 2000


proposed names as valid names (3891 vs. 2000).During the twentieth century, a steady and dramaticrise in both cumulative and valid names was real-ized, with the exception of the period of World WarII. From 1920 to the present, the number of validaphid names has increased from 1026 to 4885, anincrease of almost five times. Activities slowed in thelast several decades of the twentieth century and earlytwenty-first century showed a slowing of activity.From 1950 to 2000 there were 1.3 times the num-ber of proposed names versus valid names (3495 vs.2721) (Fig. 20.2 main). This trend might reflect aslowing of activity but it could also reflect a lack ofopportunity to reassess previous work. Taxonomicstudy continues on the Aphidoidea with descriptionof new species and reassessment of old synonymies(Eastop and Blackman 2005). Historically and evenrecently, the number of aphid species (sensu lato) hasbeen estimated (e.g., Oestlund 1886, Kosztarab et al.1990), but the numbers have always been too low.With close to 5000 valid aphid species currently (e.g.,Remaudiere and Remaudiere 1997), more remains tobe done.

Data on the synonymies of aphid species can befurther extracted from the most recent world aphidcatalogs. Eastop and Hille Ris Lambers’s (1976)catalog listed 21 species with 10 or more synonyms(Ilharco and Van Harten 1987). Remaudiere andRemaudiere’s (1997) catalog recorded 28 species with10 or more synonyms. The five species with the highestnumber of synonyms, as listed in Remaudiere andRemaudiere’s (1997) catalog, include polyphagous,economically important species: Brachycaudushelichrysi (Kaltenbach) (47 synonyms), Aphis gossypiiGlover (42), Aulacorthum solani (Kaltenbach) (37),Aphis fabae Scopoli (36), and Myzus persicae (Sulzer)(32). The large number of synonyms for some species(e.g., B. helichrysi) could be explained partly bypolyphagy and morphological variation on differenthosts (Hunter 1901, Ilharco and Van Harten 1987)or by poor communication between aphid workers(Ilharco and Van Harten 1987). Because aphidmorphology is strongly influenced by environmentalfactors, establishing valid species boundaries anddetermining synonymies remain problematic (Eastopand Blackman 2005). Other reasons for synonymycould include a lack of funding for follow-upinvestigations on samples of limited geographic rangepreviously collected or the ‘publish or perish’ syndromethat might pressure taxonomists into describing new

species from small samples (Eastop and Blackman2005).

THE FOCUS BECOMES FINER

Technological advances in nineteenth-centurymicroscopy were followed by equally significantadvances in twentieth-century microbiology andstatistical analyses. An early pioneer in aphid geneticwork was Nobel Laureate Thomas Hunt Morgan, whois better known for his later work with Drosophilamelanogaster and establishment of the chromosometheory of heredity. Some of Morgan’s (1906) earlierstudies included karyological drawings of variousphylloxerids. Unfortunately, of the earliest studieson aphid karyology, many are suspect due touncertainties in proper identification of the respectiveaphid species (Kuznetsova and Shaposhnikov 1973)and lack of voucher material. Subsequent karyotypestudies of aphids have been used at various taxonomiclevels. For example, the karyotype is often stableat the generic level, although exceptions do occur(e.g., Amphorophora), and in several genera, differencesin gross chromosomal morphology are taxonomicallyimportant (Blackman 1980a). Importance of the aphid(sensu lato) karyotype and chromosomal numbers hasbeen addressed in detailed reviews by several authors(e.g., Kuznetsova and Shaposhnikov 1973; Blackman1980a, 1980b, 1985; Hales et al., 1997). By the earlyto mid-1980s, aphid karyotype analysis had movedtoward measuring the density of the stained nucleusas a tool for determining DNA content (Blackman1985). Molecular genetic techniques however wereshifting in the late 1980s. DNA restriction fragmentlength polymorphisms (RFLP) were being applied toaphid taxonomy and systematics (Foottit et al. 1990).The early to mid-1990s saw aphid systematics furtherbenefiting from the use of polymerase chain reaction(PCR) and sequencing techniques (e.g., Sorensenet al. 1995, von Dohlen and Moran 1995). Thesetechniques continue to be refined today (e.g., vonDohlen et al. 2006, Havill et al. 2007, Coeur d’acieret al. 2008).

Morphometrics, the quantitative characterization,analysis, and comparison of biological form (Roth andMercer 2000), have been used to examine morphologi-cal variation in aphids and adelgids and have influencedtaxonomic decision making. Several such studies haveexamined geographic variation and morphological


character variation in aphids (e.g., Pemphigus spp.by Sokal (1962), Sokal et al. (1980); Adelges piceae(Ratzeburg) by Foottit and Mackauer (1980); andCinara spp. by Foottit and Mackauer (1990), Foottit(1992), and Favret and Voegtlin (2004)). Morphomet-ric approaches have been increasingly used to analyzemorphological patterns in complexes of pest speciescombined with analysis of other types of data (e.g.,Myzus spp. by Blackman (1987), Rhopalosiphum maidis(Fitch) by Blackman and Brown (1991), and Myzusantirrhinii (Macchiati) by Hales et al. (2000)).

Increasingly, molecular approaches are beingused to resolve taxonomic problems throughoutthe Aphidoidea at all taxonomic levels. The rapidand recent historical development in the use ofthese techniques includes RFLP (Foottit et al. 1990;Valenzuela et al. 2007), sequencing of nuclearand mitochondrial markers (Havill et al. 2007),microsatellites (Hales et al. 2000), DNA barcoding(Foottit et al. in press; Fig. 20.1b), and other molecularmarkers (Hales et al. 1997).

The resolution is finer using molecular techniques(Fig.20.1b) but workers are still uncovering prob-lems that require even newer approaches. Evidencesuggests that phytophagous insects such as aphidsacquire new plant hosts and adapt rapidly to newconditions (Raymond et al. 2001). This results ingenetic diversity among aphid populations and evenin sibling species making it difficult, if not impos-sible, to determine this diversity using comparativemorphological techniques alone (Eastop and Black-man 2005). A combination of classical approachesand new molecular genetic applications likely willprove necessary to determine the extent of diver-sity in aphid populations and species complexes (e.g.,Lozier et al. 2008). Morphologically indistinguishablespecies that are differentiated genetically will requirea reevaluation of species concepts and the handling ofclonal lineages (Foottit 1997). These situations mayrequire a workable nomenclatural system of index-able names for infraspecific taxa (Kim and McPheron1993).

ADVENTIVE APHID SPECIES

Society depends on agronomic, horticultural, and for-est plants for its survival, growth, and development.As phytophagous insects, aphids are intimately tiedto their host plants and cause significant economic

crop losses through direct feeding damage and trans-mission of plant viruses. With increased internationaltrade and the consequent increased movement of com-modities, the connection between aphids and theirhosts has resulted in increased rates of introductions(Foottit et al. 2006). In the absence of natural con-trol measures, some of these aphids have had a majoreconomic impact. In North America alone, in recentyears, the establishment of the soy bean aphid, Aphisglycines Matsumura, the brown citrus aphid, Toxopteracitricidus (Kirkaldy) and the Russian wheat aphid, Diu-raphis noxia (Kurdjumov), has resulted in millions ofdollars in crop losses (Foottit et al. 2006).

Although some notable world treatments addressadventive aphids (e.g., Blackman and Eastop 1994,Blackman and Eastop 2000, Blackman and Eastop2006) as do recent regional taxonomic inventories(e.g., Teulon et al. 2003, Foottit et al. 2006, Mondoret al. 2007), thorough taxonomic analyses of otherregional faunas are needed. Where aphid faunas havebeen developed, the proportion of adventive species ishigh. For example, percentages of adventive speciesrange from 19% of the North America aphid fauna(Foottit et al. 2006) to 100% of the Hawaiian aphidfauna as adventive (Mondor et al. 2007). Adventiveaphids represent an increasing threat in most regions ofthe world; their detection will require new approachessuch as DNA barcoding (Armstrong and Ball 2005).

Historically, questions concerning the taxonomicdetermination of conspecific aphid species from differ-ent biogeographic regions has concerned aphid tax-onomists (e.g., Hunter 1901, Foottit et al. 2006). Thebiogeographic origins of some adventive aphids can becomplicated or ill defined. An example of these, amongmany (Foottit et al. 2006), is that of the woolly appleaphid, Eriosoma lanigerum (Hausman). Also known asthe American blight, it gained notoriety as an applepest in Europe where it was considered as originatingfrom America. Although generally considered nativeto North America (e.g., Smith 1985), its reported originhas long been questioned (Harris 1841, Eastop 1973).The ability to identify the pest aphid species from thesource region as well as the region of introductionrelies on accurate taxonomic information. We needextensive sampling to encompass the range of aphidvariability from different hosts in different regions. Tomake predictions for possible future introductions andformulate necessary regulations, timely identificationsbased on sound taxonomic science is critical.


CONCLUSIONS

From examination of the taxonomic history of the Aphi-doidea, several conclusions can be drawn. Extensivestudy at all levels, including faunal studies, revisionarywork, and development of a stable classification systemfor species and genera is needed. Given the complexlife cycles of aphids and their parthenogenetic modeof reproduction, taxonomy has to be developed at theinfraspecific level.

Society has increasing needs, particularly inunderstanding processes involving adventive species,managing and protecting crops, and assessing theeffects of climate change. Given these needs, it isimportant to deliver timely and accurate taxonomicinformation. This delivery can be accomplishedmost efficiently through an accessible Web-basedsystem.

While aphids might be considered a well-studied pestgroup, much work remains to be done. Those aphidsthat garnered Reaumur’s (Fig 20.1) attention nearlythree centuries ago remain a group in need of study,albeit in finer detail.

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The taxonomy of crop pests: The aphids - Canacollcanacoll.org/Hemip/Staff/Foottit/PDFs/Miller_and_Foottit c20.pdf · their taxonomy is in good order. This percep-tion might lead to