The Taxonomy of Crop Pests: the Aphids

Chapter 20

The taxonomy of crop pests: The aphids

Gary 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, ARS Research Action Plan, 2004

463 here is a perception that certain insect pests ECONOMIC IMPORTANCE AND EARLY of crops are well-studied biologically and that TAXONOMY T their taxonomy is in good order. This perception might lead to the impression by those who are Aphids are small, soft-bodied insects mostly ranging unfamiliar with the intricacies of acquiring taxonomic between 1.5 and 3.5 mm in length (Blackman and understanding of biological diversity that we know all Eastop 2000); they feed on plants with piercing- there is to know. In fact, science is a discipline that sucking mouthparts. Besides the mechanical damage continually builds on its previous discoveries and tech- they cause by this action, aphids also serve as the nologies as it advances our knowledge. Much research largest group of vectors of plant viruses (Eastop 1977, is needed even in economically important insect groups Chan et al. 1991). The damage is further compounded whose taxonomy might be regarded as advanced. In by fouling of the host plant with honeydew. Noted this chapter, using the Aphidoidea as an example as long ago as in Réaumur’s (1737) work, honeydew and, in particular, using the early works of North is excreted from the anus and is high in plant sugars American aphidology as background, we explore var- and other compounds. Besides having an influence ious dimensions of taxonomic knowledge in this pest on predators (Glen 1973) and parasitoids (Faria group. 2005), it serves as a substrate for the growth of fungal complexes that cause sooty mold (Westcott 1971). In addition to reducing the photosynthetic ability of HISTORICAL BACKGROUND plants, sooty mold reduces a plant’s aesthetic market value (Worf et al. 1995). Plants have been cultivated and traded since perhaps More than 250 species of the Aphidoidea (in the 8000 BC (Huxley 1978) and insect pests have long families Adelgidae, Phylloxeridae, and Aphididae) feed plagued humans and their crops. Ancient civilizations on agricultural or horticultural crops (Blackman and recorded swarms of locusts and other insect pestilence Eastop 2000). While this figure only represents approx- (Harpaz 1973, Konishi and Ito 1973). As humans imately 5% of the world aphid fauna, the economic expanded crop cultivation, associated insect problems consequences of aphid damage are huge. For example, soon followed. The European colonists of the New Wellings et al. (1989) estimated for 13 selected crops World faced their own set of insect-related problems that aphids contribute about 2% of the total losses with the cultivation of both native and introduced attributed to insects and believed that figure was a crops. For example, tobacco, which is native to the gross underestimate. Aphids are one of the important New World, experienced insect damage from horn- vegetable pests (Capinera 2002). Of the 80 groups of worms and flea-beetles from the outset of its cultivation vascular plants in the world only 8 lack aphids, and (Garner 1946). The introduction of new plants also those groups represent only 3% of the plant species began early during European colonization. Sugarcane (Eastop 1978). was transported from the Canary Islands to Hispaniola Most aphid references refer to economic impact and on Columbus’s second voyage in 1493 (Deerr 1949). some of the very earliest works of the sixteenth and Some of these early introduced plants also had their seventeenth centuries have been noted by Blackman associated pests, including aphids. The close associa- and Eastop (2000). Although aphids have extraordi- tion of aphids with their hosts meant those insects and nary damaging horticultural effects, some of society’s their eggs were being transported through commerce early interest involved their beneficial or positive as well (Howard 1898). The cabbage aphid, Brevico- attributes. Galls of certain aphid species (e.g., Baizongia ryne brassicae (Linnaeus), was noted in North America pistaciae [Linnaeus] and Schlechtendalia chinensis [Bell]) as early as 1791 (Miller et al. 2006). Early entomolo- have been used for centuries in medicine, tanning, gists were well aware that commerce and travel were and dyeing (Fagan 1918). Woodcuts as early as 1570 responsible for the transport of some of these pests. illustrate galls of B. pistaciae on Pistacia (Blackman and In 1856, Asa Fitch speculated that B. brassicae was Eastop 1994) and by 1596 ‘Chinese galls’ of Melaphis brought along with cabbage plants on shipboard cargo chinensis [= S. chinensis]onRhus javanica (a sumac) (Miller et al. 2006). were noted as insect induced (Eastop 1979). The taxonomy of crop pests: the aphids 465

well as detailed illustrations. Linnaeus (1758) used Réaumur’s (1737) work as a reference in connection with a number of the species he named. The nominal species, Aphis sambuci Linnaeus (1758), is illustrated in habitus and as several detailed figures on one of Réaumur’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,which contained 1 adelgid species.

EARLY APHID STUDIES – A NORTH AMERICAN EXAMPLE

Some of the earliest, if not the earliest, systematic work on North American aphids was that of Rafinesque1 (1817, 1818), who described 36 species and 4 sub- genera. Rafinesque’s (1817) interest and intent ‘to study all the species of this genus [Aphis] found in the United States’ was initiated by his observations that they were ‘often highly injurious’ to their host plants. Other early North American workers often treated the economic importance of aphids. For example, Har- ris’ (1841) report on insects injurious to vegetation includes sections on ‘plant-lice’. While little taxonomic information was included, Harris did incorporate observations on life history, biology, predators, host plants, and control. Fitch’s work (e.g., Fitch 1851) in the mid-1800s not only included life history information on aphids but also new species descriptions. Between 1851 and 1872, Fitch proposed names for 58 species of Aphidoidea (Barnes 1988). Walsh’s (1863) treatment of the Aphididae (sensu lato) included his ‘Synoptical Table of U.S. Genera’, which was essentially a key. By the 1870s–1880s, entomologists such as Thomas (1877), Monell (1879), and Oestlund (1886) were Fig. 20.1 (a) (top). Some of the early aphid work produced specializing in the study of aphids. by Réaumur (1737) included his woodcuts, which were used Difficulty in distinguishing aphids was noted as early for identification. Linnaeus (1758) referenced both of the as Linnaeus (Walsh 1863) and early workers in North aphid species in his work. (Figs. 1–4. Aphis rosae America also lamented the lack of study and knowledge (= Macrosiphum rosae). Figs. 5–15. Aphis sambuci.) of the aphids. Walsh (1863), in Illinois, complained (b) (bottom). Nearly three centuries later, short DNA about the need for ‘Public Scientific Libraries’ that his sequences from a uniform locality of the genome (barcodes) more fortunate ‘Eastern brethren’ had. He added that for Macrosiphum rosae and Aphis sambuci are being explored the ‘specific distinctions’ of the aphids themselves were ‘generally evanescent in the dried specimen’. Thomas Prior to Linnaeus’s (1758) work, many of the (1879) reiterated Walsh’s comments and believed the papers concerning aphids had little taxonomic value. reasons for the neglected study of aphids rested on A notable exception is Réaumur’s (1737) ‘Mémoires 1Hottes (1963) proposed to suppress Rafinesques’s aphid pour servira ` l’histore des insectes’. This work included names and subsequent workers (e.g., Remaudière and information on aphid life history and biology as Remaudière 1997) have recorded his names as unavailable. 466 Gary L. Miller and Robert G. Foottit two issues, the difficulty in preserving specimens and 1880s, a new dimension was added to the descriptions the paucity of systematic works, most of which were of aphid morphology. Relative descriptors of antennal European. With delays of months to years to procure segment length, such as ‘about half as long as the pre- a reference work (Oestlund 1886), the situation for ceding’ (e.g., Monell 1879) or ‘subequal’ (e.g., Oestlund some was daunting. In 1886, Oestlund still consid- 1886), were being replaced with discrete measure- ered the systematics of the aphids ‘unsatisfactory’ but ments in one-hundredth of a millimeter (e.g., Oestlund regarded the lack of literature as the greatest want for 1887). These changes generally corresponded with the ‘frontier naturalist’. Later, Oestlund’s (1919) tone major advances that were being made in microscopy, changed when his concern focused on the then- recent especially the development and design of microscope aphid classification difficulties ‘on account of the great objectives and lenses that maximized both magnifica- number of new genera and species made known’. tion and resolution. Especially noteworthy with Oestlund’s (1886) ear- Other changes were taking place in aphid taxonomy lier concern about the state of aphid study is his in North America. Earliest works reflected Linnaeus’s failure to mention the difficulty of preserving speci- (1758) simple classification (e.g., Haldemann 1844). mens. By the 1860s, North Americans, along with their The list of aphid species referable to Linnaeus’s sin- European counterparts, were making progress in pre- gle genus, Aphis, was being expanded. The taxonomic serving pinned insect specimens in cabinets (Sorensen works of European aphidologists such as Kaltenbach 1995). Instead of being pinned or glued on small (1843), Koch (1854), Passerini (1860), and Buck- boards, aphids were routinely preserved on micro- ton (1876) influenced the early taxonomic studies of scope slides.2 Changes in the way aphids were being the North American workers (Walsh 1863, Thomas studied and preserved were accompanied by changes 1877, 1878, 1879). While these works included keys and improvements in species descriptions and tools to genera and tribes, species treatments consisted of for identification. The earliest North American aphid simple descriptions and lists. Monell’s (1879) contri- descriptions (e.g., Rafinesque 1817, 1818; Haldemann bution is worth mentioning because he also developed 1844) were based almost entirely on coloration, gen- identification keys for related species of select genera. eral appearance, and host association. Subsequent The use of species keys advanced the ability to workers (e.g., Walsh 1863, Riley 1879, see also Miller identify aphids. Oestlund’s (1887) study of Minnesota et al. 2006) relied on descriptions of general appear- aphids provided detailed keys to subfamilies, genera, ance but also routinely included measurements of body and species of select genera. In what was a synthesis length and wing length in their species descriptions. of the knowledge of North American aphids, he also Walsh’s (1863) generic descriptions added compar- included detailed species descriptions, an up-to-date isons to other morphological structures (e.g., relative literature review of North American authors, and length of siphunculi in comparison to tarsal length), a a host plant list. It was also a reflection of the practice that was uncommon at the time. By the late fruits of government-sponsored entomology at that time (Sorensen 1995). Of the 65 publications listed 2Pergande’s ledger and card file at the United States Aphi- in Oestlund’s (1887) aphid bibliography, nearly doidea Collection, Beltsville, Maryland, provides an excellent 75% of the works reflect government-sponsored or recordoftheprogressionofpreservedaphidspecimens.Hisear- government-associated entomology. liest ledger entries, while he was in St. Louis, Missouri (1877), A major work published at the beginning of the twen- record collected aphid specimens as being pinned, mounted on tieth century, Hunter’s (1901) catalog ‘The Aphididae boards, or preserved in alcohol. By 1878 in Washington, DC, he noted aphids as being ‘mounted in balsam’ and preserved in of North America’, provided much of the pertinent lit- alcohol. Other aphidologists were also using balsam-mounted erature on and taxonomy of North American aphids. specimens, as Pergande noted the receipt of ‘Pemphigus aceris Various authors had published lists of described species n. sp.’ from aphidologist Monell that were ‘mounted on slide’ but Hunter (1901) not only contributed an expanded in 1878. At the USNM, Pergande was evidently still gluing species list but also included the known systematic specimens to pieces of board as late as 1880 but he also and economic literature referable to the species, along ‘mounted some on a slide’. In 1903, Pergande recorded that with host plant information. Knowledge of North he examined ‘the old Fitch collection of Aphides’ for Aphis mali Fitch, which were ‘pinned’ and then ‘mounted all of them in American aphids had grown from 36 species pro- balsam’. Slide mounting had indeed become a standard way posed by Rafinesque (1817, 1818) to 166 species to study and preserve the aphids by the turn of the century. identified by Monell (1879), an increase of nearly five The taxonomy of crop pests: the aphids 467 times, to 325 species identified by Hunter (1901), an formal species status could be given to a biologically increase of more than nine times. The compilation of recognizable anholocyclic group derived from a sexual the North American aphid fauna would continue to ancestor (Blackman and Brown 1991, Foottit 1997, grow to 1416 species (Foottit et al. 2006). Havill and Foottit 2007). One way to observe trends in aphid systematics is to compare the rates of synonymy and the accumu- RECOGNIZING APHID SPECIES lation of new taxa; as more research is done, more species are described and new synonymies are discov- As the number of recognized aphid species has grown ered (Fig. 20.2). From 1758 (when Linnaeus’s work since Linnaeus (1758) (Fig. 20.2), there have been was published) until 1840, the number of described difficulties in recognizing or even defining an aphid valid aphid species (sensu lato) and cumulative aphid species (e.g., Shaposhnikov 1987). The conceptual and names was only 109 and the difference between the two operational use of species concepts and definitions in parameters remained relatively small. Starting around aphid taxonomy throughout the world is complicated 1841, shortly before Kaltenbach’s (1843) work, the by their reproductive biology. Aphids are characterized difference between cumulative aphid names and cumu- by cyclical parthenogenesis, but there may also be lative valid names over time began to increase, albeit purely anholocyclic populations not manifesting the gradually, until about the late 1910s. The number sexual phase of the life cycle. Recommendations have of valid species increased nearly eightfold from 129 been made for the taxonomic treatment of aphid to 1011 species between 1841 and 1919. Between populations that are permanently parthenogenetic; 1840 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 468 Gary L. Miller and Robert G. Foottit proposed names as valid names (3891 vs. 2000). species from small samples (Eastop and Blackman During the twentieth century, a steady and dramatic 2005). rise in both cumulative and valid names was real- ized, with the exception of the period of World War II. From 1920 to the present, the number of valid THE FOCUS BECOMES FINER aphid names has increased from 1026 to 4885, an increase of almost five times. Activities slowed in the Technological advances in nineteenth-century last several decades of the twentieth century and early microscopy were followed by equally significant twenty-first century showed a slowing of activity. advances in twentieth-century microbiology and From 1950 to 2000 there were 1.3 times the num- statistical analyses. An early pioneer in aphid genetic ber of proposed names versus valid names (3495 vs. work was Nobel Laureate Thomas Hunt Morgan, who 2721) (Fig. 20.2 main). This trend might reflect a is better known for his later work with Drosophila slowing of activity but it could also reflect a lack of melanogaster and establishment of the chromosome opportunity to reassess previous work. Taxonomic theory of heredity. Some of Morgan’s (1906) earlier study continues on the Aphidoidea with description studies included karyological drawings of various of new species and reassessment of old synonymies phylloxerids. Unfortunately, of the earliest studies (Eastop and Blackman 2005). Historically and even on aphid karyology, many are suspect due to recently, the number of aphid species (sensu lato)has uncertainties in proper identification of the respective been estimated (e.g., Oestlund 1886, Kosztarab et al. aphid species (Kuznetsova and Shaposhnikov 1973) 1990), but the numbers have always been too low. and lack of voucher material. Subsequent karyotype With close to 5000 valid aphid species currently (e.g., studies of aphids have been used at various taxonomic Remaudière and Remaudière 1997), more remains to levels. For example, the karyotype is often stable be done. at the generic level, although exceptions do occur Data on the synonymies of aphid species can be (e.g., Amphorophora), and in several genera, differences further extracted from the most recent world aphid in gross chromosomal morphology are taxonomically catalogs. Eastop and Hille Ris Lambers’s (1976) important (Blackman 1980a). Importance of the aphid catalog listed 21 species with 10 or more synonyms (sensu lato) karyotype and chromosomal numbers has (Ilharco and Van Harten 1987). Remaudière and been addressed in detailed reviews by several authors Remaudière’s (1997) catalog recorded 28 species with (e.g., Kuznetsova and Shaposhnikov 1973; Blackman 10 or more synonyms. The five species with the highest 1980a, 1980b, 1985; Hales et al., 1997). By the early number of synonyms, as listed in Remaudière and to mid-1980s, aphid karyotype analysis had moved Remaudière’s (1997) catalog, include polyphagous, toward measuring the density of the stained nucleus economically important species: Brachycaudus as a tool for determining DNA content (Blackman helichrysi (Kaltenbach) (47 synonyms), Aphis gossypii 1985). Molecular genetic techniques however were Glover (42), Aulacorthum solani (Kaltenbach) (37), shifting in the late 1980s. DNA restriction fragment Aphis fabae Scopoli (36), and Myzus persicae (Sulzer) length polymorphisms (RFLP) were being applied to (32). The large number of synonyms for some species aphid taxonomy and systematics (Foottit et al. 1990). (e.g., B. helichrysi) could be explained partly by The early to mid-1990s saw aphid systematics further polyphagy and morphological variation on different benefiting from the use of polymerase chain reaction hosts (Hunter 1901, Ilharco and Van Harten 1987) (PCR) and sequencing techniques (e.g., Sorensen or by poor communication between aphid workers et al. 1995, von Dohlen and Moran 1995). These (Ilharco and Van Harten 1987). Because aphid techniques continue to be refined today (e.g., von morphology is strongly influenced by environmental Dohlen et al. 2006, Havill et al. 2007, Coeur d’acier factors, establishing valid species boundaries and et al. 2008). determining synonymies remain problematic (Eastop Morphometrics, the quantitative characterization, and Blackman 2005). Other reasons for synonymy analysis, and comparison of biological form (Roth and could include a lack of funding for follow-up Mercer 2000), have been used to examine morphologi- investigations on samples of limited geographic range calvariationinaphidsandadelgidsandhaveinfluenced previously collected or the ‘publish or perish’ syndrome taxonomic decision making. Several such studies have that might pressure taxonomists into describing new examined geographic variation and morphological The taxonomy of crop pests: the aphids 469 character variation in aphids (e.g., Pemphigus spp. crop losses through direct feeding damage and trans- by Sokal (1962), Sokal et al. (1980); Adelges piceae mission of plant viruses. With increased international (Ratzeburg) by Foottit and Mackauer (1980); and trade and the consequent increased movement of com- Cinara spp. by Foottit and Mackauer (1990), Foottit modities, the connection between aphids and their (1992), and Favret and Voegtlin (2004)). Morphomet- hosts has resulted in increased rates of introductions ric approaches have been increasingly used to analyze (Foottit et al. 2006). In the absence of natural con- morphological patterns in complexes of pest species trol measures, some of these aphids have had a major combined with analysis of other types of data (e.g., economic impact. In North America alone, in recent Myzus spp. by Blackman (1987), Rhopalosiphum maidis years, the establishment of the soy bean aphid, Aphis (Fitch) by Blackman and Brown (1991), and Myzus glycines Matsumura, the brown citrus aphid, Toxoptera antirrhinii (Macchiati) by Hales et al. (2000)). citricidus (Kirkaldy) and the Russian wheat aphid, Diu- Increasingly, molecular approaches are being raphis noxia (Kurdjumov), has resulted in millions of used to resolve taxonomic problems throughout dollars in crop losses (Foottit et al. 2006). the Aphidoidea at all taxonomic levels. The rapid Although some notable world treatments address and recent historical development in the use of adventive aphids (e.g., Blackman and Eastop 1994, these techniques includes RFLP (Foottit et al. 1990; Blackman and Eastop 2000, Blackman and Eastop Valenzuela et al. 2007), sequencing of nuclear 2006) as do recent regional taxonomic inventories and mitochondrial markers (Havill et al. 2007), (e.g., Teulon et al. 2003, Foottit et al. 2006, Mondor microsatellites (Hales et al. 2000), DNA barcoding et al. 2007), thorough taxonomic analyses of other (Foottit et al. in press; Fig. 20.1b), and other molecular regional faunas are needed. Where aphid faunas have markers (Hales et al. 1997). been developed, the proportion of adventive species is The resolution is finer using molecular techniques high. For example, percentages of adventive species (Fig.20.1b) but workers are still uncovering prob- range from 19% of the North America aphid fauna lems that require even newer approaches. Evidence (Foottit et al. 2006) to 100% of the Hawaiian aphid suggests that phytophagous insects such as aphids fauna as adventive (Mondor et al. 2007). Adventive acquire new plant hosts and adapt rapidly to new aphids represent an increasing threat in most regions of conditions (Raymond et al. 2001). This results in genetic diversity among aphid populations and even the world; their detection will require new approaches in sibling species making it difficult, if not impos- such as DNA barcoding (Armstrong and Ball 2005). sible, to determine this diversity using comparative Historically, questions concerning the taxonomic morphological techniques alone (Eastop and Black- determination of conspecific aphid species from differ- man 2005). A combination of classical approaches ent biogeographic regions has concerned aphid tax- and new molecular genetic applications likely will onomists (e.g., Hunter 1901, Foottit et al. 2006). The prove necessary to determine the extent of diver- biogeographic origins of some adventive aphids can be sity in aphid populations and species complexes (e.g., complicated or ill defined. An example of these, among Lozier et al. 2008). Morphologically indistinguishable many (Foottit et al. 2006), is that of the woolly apple species that are differentiated genetically will require aphid, Eriosoma lanigerum (Hausman). Also known as a reevaluation of species concepts and the handling of the American blight, it gained notoriety as an apple clonal lineages (Foottit 1997). These situations may pest in Europe where it was considered as originating require a workable nomenclatural system of index- from America. Although generally considered native able names for infraspecific taxa (Kim and McPheron to North America (e.g., Smith 1985), its reported origin 1993). has long been questioned (Harris 1841, Eastop 1973). The ability to identify the pest aphid species from the source region as well as the region of introduction ADVENTIVE APHID SPECIES relies on accurate taxonomic information. We need extensive sampling to encompass the range of aphid Society depends on agronomic, horticultural, and for- variability from different hosts in different regions. To est plants for its survival, growth, and development. make predictions for possible future introductions and As phytophagous insects, aphids are intimately tied formulate necessary regulations, timely identifications to their host plants and cause significant economic based on sound taxonomic science is critical. 470 Gary L. Miller and Robert G. Foottit

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