The taxonomy of crop pests: The aphids

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1 Chapter 20 The taxonomy of crop pests: The aphids Gary L. Miller 1 and Robert G. Foottit 2 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 Insect Biodiversity: Science and Society, 1st edition. Edited by R. Foottit and P. Adler 2009 Blackwell Publishing, ISBN

2 There is a perception that certain insect pests of crops are well-studied biologically and that their taxonomy is in good order. This perception might lead to the impression by those who are unfamiliar with the intricacies of acquiring taxonomic understanding of biological diversity that we know all there is to know. In fact, science is a discipline that continually builds on its previous discoveries and technologies as it advances our knowledge. Much research is needed even in economically important insect groups whose taxonomy might be regarded as advanced. In this chapter, using the Aphidoidea as an example and, in particular, using the early works of North American aphidology as background, we explore various dimensions of taxonomic knowledge in this pest group. HISTORICAL BACKGROUND Plants have been cultivated and traded since perhaps 8000 BC (Huxley 1978) and insect pests have long plagued humans and their crops. Ancient civilizations recorded swarms of locusts and other insect pestilence (Harpaz 1973, Konishi and Ito 1973). As humans expanded crop cultivation, associated insect problems soon followed. The European colonists of the New World faced their own set of insect-related problems with the cultivation of both native and introduced crops. For example, tobacco, which is native to the New World, experienced insect damage from hornworms and flea-beetles from the outset of its cultivation (Garner 1946). The introduction of new plants also began early during European colonization. Sugarcane was transported from the Canary Islands to Hispaniola on Columbus s second voyage in 1493 (Deerr 1949). Some of these early introduced plants also had their associated pests, including aphids. The close association of aphids with their hosts meant those insects and their eggs were being transported through commerce as well (Howard 1898). The cabbage aphid, Brevicoryne brassicae (Linnaeus), was noted in North America as early as 1791 (Miller et al. 2006). Early entomologists were well aware that commerce and travel were responsible for the transport of some of these pests. In 1856, Asa Fitch speculated that B. brassicae was brought along with cabbage plants on shipboard cargo (Miller et al. 2006). ECONOMIC IMPORTANCE AND EARLY TAXONOMY Aphids are small, soft-bodied insects mostly ranging between 1.5 and 3.5 mm in length (Blackman and Eastop 2000); they feed on plants with piercingsucking mouthparts. Besides the mechanical damage they cause by this action, aphids also serve as the largest group of vectors of plant viruses (Eastop 1977, Chan et al. 1991). The damage is further compounded by fouling of the host plant with honeydew. Noted as long ago as in Réaumur s (1737) work, honeydew is excreted from the anus and is high in plant sugars and other compounds. Besides having an influence on predators (Glen 1973) and parasitoids (Faria 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 plants, sooty mold reduces a plant s aesthetic market value (Worf et al. 1995). More than 250 species of the Aphidoidea (in the families Adelgidae, Phylloxeridae, and Aphididae) feed on agricultural or horticultural crops (Blackman and Eastop 2000). While this figure only represents approximately 5% of the world aphid fauna, the economic consequences of aphid damage are huge. For example, Wellings et al. (1989) estimated for 13 selected crops that aphids contribute about 2% of the total losses attributed to insects and believed that figure was a gross underestimate. Aphids are one of the important vegetable pests (Capinera 2002). Of the 80 groups of vascular plants in the world only 8 lack aphids, and those groups represent only 3% of the plant species (Eastop 1978). Most aphid references refer to economic impact and some of the very earliest works of the sixteenth and seventeenth centuries have been noted by Blackman and Eastop (2000). Although aphids have extraordinary damaging horticultural effects, some of society s early interest involved their beneficial or positive attributes. Galls of certain aphid species (e.g., Baizongia pistaciae [Linnaeus] and Schlechtendalia chinensis [Bell]) have been used for centuries in medicine, tanning, and dyeing (Fagan 1918). Woodcuts as early as 1570 illustrate galls of B. pistaciae on Pistacia (Blackman and Eastop 1994) and by 1596 Chinese galls of Melaphis chinensis [= S. chinensis] onrhus javanica (a sumac) were noted as insect induced (Eastop 1979).

3 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 Fig (a) (top). Some of the early aphid work produced by Réaumur (1737) included his woodcuts, which were used for identification. Linnaeus (1758) referenced both of the aphid species in his work. (Figs Aphis rosae (= Macrosiphum rosae). Figs Aphis sambuci.) (b) (bottom). Nearly three centuries later, short DNA sequences 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 the papers concerning aphids had little taxonomic value. A notable exception is Réaumur s (1737) Mémoires pour servir à l histore des insectes. This work included information on aphid life history and biology as Some of the earliest, if not the earliest, systematic work on North American aphids was that of Rafinesque 1 (1817, 1818), who described 36 species and 4 subgenera. 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, Harris (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 specializing in the study of aphids. Difficulty in distinguishing aphids was noted as early as Linnaeus (Walsh 1863) and early workers in North America also lamented the lack of study and knowledge of the aphids. Walsh (1863), in Illinois, complained about the need for Public Scientific Libraries that his more fortunate Eastern brethren had. He added that the specific distinctions of the aphids themselves were generally evanescent in the dried specimen. Thomas (1879) reiterated Walsh s comments and believed the reasons for the neglected study of aphids rested on 1 Hottes (1963) proposed to suppress Rafinesques s aphid names and subsequent workers (e.g., Remaudière and Remaudière 1997) have recorded his names as unavailable.

4 466 Gary L. Miller and Robert G. Foottit two issues, the difficulty in preserving specimens and the paucity of systematic works, most of which were European. With delays of months to years to procure a reference work (Oestlund 1886), the situation for some was daunting. In 1886, Oestlund still considered the systematics of the aphids unsatisfactory but regarded the lack of literature as the greatest want for the frontier naturalist. Later, Oestlund s (1919) tone changed when his concern focused on the then- recent aphid classification difficulties on account of the great number of new genera and species made known. Especially noteworthy with Oestlund s (1886) earlier concern about the state of aphid study is his failure to mention the difficulty of preserving specimens. By the 1860s, North Americans, along with their European counterparts, were making progress in preserving pinned insect specimens in cabinets (Sorensen 1995). Instead of being pinned or glued on small boards, aphids were routinely preserved on microscope slides. 2 Changes in the way aphids were being studied and preserved were accompanied by changes and improvements in species descriptions and tools for identification. The earliest North American aphid descriptions (e.g., Rafinesque 1817, 1818; Haldemann 1844) were based almost entirely on coloration, general appearance, and host association. Subsequent workers (e.g., Walsh 1863, Riley 1879, see also Miller et al. 2006) relied on descriptions of general appearance but also routinely included measurements of body length and wing length in their species descriptions. Walsh s (1863) generic descriptions added comparisons to other morphological structures (e.g., relative length of siphunculi in comparison to tarsal length), a practice that was uncommon at the time. By the late 2 Pergande s ledger and card file at the United States Aphidoidea Collection, Beltsville, Maryland, provides an excellent record of the progression of preserved aphid specimens. His earliest ledger entries, while he was in St. Louis, Missouri (1877), record collected aphid specimens as being pinned, mounted on boards, or preserved in alcohol. By 1878 in Washington, DC, he noted aphids as being mounted in balsam and preserved in alcohol. Other aphidologists were also using balsam-mounted specimens, as Pergande noted the receipt of Pemphigus aceris n. sp. from aphidologist Monell that were mounted on slide in At the USNM, Pergande was evidently still gluing specimens to pieces of board as late as 1880 but he also mounted some on a slide. In 1903, Pergande recorded that he examined the old Fitch collection of Aphides for Aphis mali Fitch, which were pinned and then mounted all of them in balsam. Slide mounting had indeed become a standard way to study and preserve the aphids by the turn of the century. 1880s, a new dimension was added to the descriptions of aphid morphology. Relative descriptors of antennal segment length, such as about half as long as the preceding (e.g., Monell 1879) or subequal (e.g., Oestlund 1886), were being replaced with discrete measurements in one-hundredth of a millimeter (e.g., Oestlund 1887). These changes generally corresponded with major advances that were being made in microscopy, especially the development and design of microscope objectives and lenses that maximized both magnification and resolution. Other changes were taking place in aphid taxonomy in North America. Earliest works reflected Linnaeus s (1758) simple classification (e.g., Haldemann 1844). The list of aphid species referable to Linnaeus s single genus, Aphis, was being expanded. The taxonomic works of European aphidologists such as Kaltenbach (1843), Koch (1854), Passerini (1860), and Buckton (1876) influenced the early taxonomic studies of the North American workers (Walsh 1863, Thomas 1877, 1878, 1879). While these works included keys to genera and tribes, species treatments consisted of simple descriptions and lists. Monell s (1879) contribution is worth mentioning because he also developed identification keys for related species of select genera. The use of species keys advanced the ability to identify aphids. Oestlund s (1887) study of Minnesota aphids provided detailed keys to subfamilies, genera, and species of select genera. In what was a synthesis of the knowledge of North American aphids, he also included detailed species descriptions, an up-to-date literature review of North American authors, and a host plant list. It was also a reflection of the fruits of government-sponsored entomology at that time (Sorensen 1995). Of the 65 publications listed in Oestlund s (1887) aphid bibliography, nearly 75% of the works reflect government-sponsored or government-associated entomology. A major work published at the beginning of the twentieth century, Hunter s (1901) catalog The Aphididae of North America, provided much of the pertinent literature on and taxonomy of North American aphids. Various authors had published lists of described species but Hunter (1901) not only contributed an expanded species list but also included the known systematic and economic literature referable to the species, along with host plant information. Knowledge of North American aphids had grown from 36 species proposed by Rafinesque (1817, 1818) to 166 species identified by Monell (1879), an increase of nearly five

5 The taxonomy of crop pests: the aphids 467 times, to 325 species identified by Hunter (1901), an increase of more than nine times. The compilation of the North American aphid fauna would continue to grow to 1416 species (Foottit et al. 2006). RECOGNIZING APHID SPECIES As the number of recognized aphid species has grown since Linnaeus (1758) (Fig. 20.2), there have been difficulties in recognizing or even defining an aphid species (e.g., Shaposhnikov 1987). The conceptual and operational use of species concepts and definitions in aphid taxonomy throughout the world is complicated by their reproductive biology. Aphids are characterized by cyclical parthenogenesis, but there may also be purely anholocyclic populations not manifesting the sexual phase of the life cycle. Recommendations have been made for the taxonomic treatment of aphid populations that are permanently parthenogenetic; formal species status could be given to a biologically recognizable anholocyclic group derived from a sexual ancestor (Blackman and Brown 1991, Foottit 1997, Havill and Foottit 2007). One way to observe trends in aphid systematics is to compare the rates of synonymy and the accumulation of new taxa; as more research is done, more species are described and new synonymies are discovered (Fig. 20.2). From 1758 (when Linnaeus s work was published) until 1840, the number of described valid aphid species (sensu lato) and cumulative aphid names was only 109 and the difference between the two parameters remained relatively small. Starting around 1841, shortly before Kaltenbach s (1843) work, the difference between cumulative aphid names and cumulative valid names over time began to increase, albeit gradually, until about the late 1910s. The number of valid species increased nearly eightfold from 129 to 1011 species between 1841 and Between 1840 and 1949, there were nearly twice as many Fig (Inset). Cumulative aphid names proposed versus cumulative currently valid aphid names from 1758 to (Main). Number of proposed aphid names versus valid aphid names from 1758 to 2000

6 468 Gary L. Miller and Robert G. Foottit proposed names as valid names (3891 vs. 2000). During the twentieth century, a steady and dramatic rise in both cumulative and valid names was realized, with the exception of the period of World War II. From 1920 to the present, the number of valid aphid names has increased from 1026 to 4885, an increase of almost five times. Activities slowed in the last several decades of the twentieth century and early twenty-first century showed a slowing of activity. From 1950 to 2000 there were 1.3 times the number of proposed names versus valid names (3495 vs. 2721) (Fig main). This trend might reflect a slowing of activity but it could also reflect a lack of opportunity to reassess previous work. Taxonomic study continues on the Aphidoidea with description of new species and reassessment of old synonymies (Eastop and Blackman 2005). Historically and even recently, the number of aphid species (sensu lato) has been 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., Remaudière and Remaudière 1997), more remains to be done. Data on the synonymies of aphid species can be further extracted from the most recent world aphid catalogs. Eastop and Hille Ris Lambers s (1976) catalog listed 21 species with 10 or more synonyms (Ilharco and Van Harten 1987). Remaudière and Remaudière s (1997) catalog recorded 28 species with 10 or more synonyms. The five species with the highest number of synonyms, as listed in Remaudière and Remaudière s (1997) catalog, include polyphagous, economically important species: Brachycaudus helichrysi (Kaltenbach) (47 synonyms), Aphis gossypii Glover (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 by polyphagy and morphological variation on different hosts (Hunter 1901, Ilharco and Van Harten 1987) or by poor communication between aphid workers (Ilharco and Van Harten 1987). Because aphid morphology is strongly influenced by environmental factors, establishing valid species boundaries and determining synonymies remain problematic (Eastop and Blackman 2005). Other reasons for synonymy could include a lack of funding for follow-up investigations on samples of limited geographic range previously collected or the publish or perish syndrome that might pressure taxonomists into describing new species from small samples (Eastop and Blackman 2005). THE FOCUS BECOMES FINER Technological advances in nineteenth-century microscopy were followed by equally significant advances in twentieth-century microbiology and statistical analyses. An early pioneer in aphid genetic work was Nobel Laureate Thomas Hunt Morgan, who is better known for his later work with Drosophila melanogaster and establishment of the chromosome theory of heredity. Some of Morgan s (1906) earlier studies included karyological drawings of various phylloxerids. Unfortunately, of the earliest studies on aphid karyology, many are suspect due to uncertainties in proper identification of the respective aphid species (Kuznetsova and Shaposhnikov 1973) and lack of voucher material. Subsequent karyotype studies of aphids have been used at various taxonomic levels. For example, the karyotype is often stable at the generic level, although exceptions do occur (e.g., Amphorophora), and in several genera, differences in gross chromosomal morphology are taxonomically important (Blackman 1980a). Importance of the aphid (sensu lato) karyotype and chromosomal numbers has been addressed in detailed reviews by several authors (e.g., Kuznetsova and Shaposhnikov 1973; Blackman 1980a, 1980b, 1985; Hales et al., 1997). By the early to mid-1980s, aphid karyotype analysis had moved toward measuring the density of the stained nucleus as a tool for determining DNA content (Blackman 1985). Molecular genetic techniques however were shifting in the late 1980s. DNA restriction fragment length polymorphisms (RFLP) were being applied to aphid taxonomy and systematics (Foottit et al. 1990). The early to mid-1990s saw aphid systematics further benefiting from the use of polymerase chain reaction (PCR) and sequencing techniques (e.g., Sorensen et al. 1995, von Dohlen and Moran 1995). These techniques continue to be refined today (e.g., von Dohlen et al. 2006, Havill et al. 2007, Coeur d acier et al. 2008). Morphometrics, the quantitative characterization, analysis, and comparison of biological form (Roth and Mercer 2000), have been used to examine morphological variation in aphids and adelgids and have influenced taxonomic decision making. Several such studies have examined geographic variation and morphological

7 The taxonomy of crop pests: the aphids 469 character variation in aphids (e.g., Pemphigus spp. by Sokal (1962), Sokal et al. (1980); Adelges piceae (Ratzeburg) by Foottit and Mackauer (1980); and Cinara spp. by Foottit and Mackauer (1990), Foottit (1992), and Favret and Voegtlin (2004)). Morphometric approaches have been increasingly used to analyze morphological patterns in complexes of pest species combined with analysis of other types of data (e.g., Myzus spp. by Blackman (1987), Rhopalosiphum maidis (Fitch) by Blackman and Brown (1991), and Myzus antirrhinii (Macchiati) by Hales et al. (2000)). Increasingly, molecular approaches are being used to resolve taxonomic problems throughout the Aphidoidea at all taxonomic levels. The rapid and recent historical development in the use of these techniques includes RFLP (Foottit et al. 1990; Valenzuela et al. 2007), sequencing of nuclear and mitochondrial markers (Havill et al. 2007), microsatellites (Hales et al. 2000), DNA barcoding (Foottit et al. in press; Fig. 20.1b), and other molecular markers (Hales et al. 1997). The resolution is finer using molecular techniques (Fig.20.1b) but workers are still uncovering problems that require even newer approaches. Evidence suggests that phytophagous insects such as aphids acquire new plant hosts and adapt rapidly to new conditions (Raymond et al. 2001). This results in genetic diversity among aphid populations and even in sibling species making it difficult, if not impossible, to determine this diversity using comparative morphological techniques alone (Eastop and Blackman 2005). A combination of classical approaches and new molecular genetic applications likely will prove necessary to determine the extent of diversity in aphid populations and species complexes (e.g., Lozier et al. 2008). Morphologically indistinguishable species that are differentiated genetically will require a reevaluation of species concepts and the handling of clonal lineages (Foottit 1997). These situations may require a workable nomenclatural system of indexable names for infraspecific taxa (Kim and McPheron 1993). ADVENTIVE APHID SPECIES Society depends on agronomic, horticultural, and forest plants for its survival, growth, and development. As phytophagous insects, aphids are intimately tied to their host plants and cause significant economic crop losses through direct feeding damage and transmission of plant viruses. With increased international trade and the consequent increased movement of commodities, the connection between aphids and their hosts has resulted in increased rates of introductions (Foottit et al. 2006). In the absence of natural control measures, some of these aphids have had a major economic impact. In North America alone, in recent years, the establishment of the soy bean aphid, Aphis glycines Matsumura, the brown citrus aphid, Toxoptera citricidus (Kirkaldy) and the Russian wheat aphid, Diuraphis noxia (Kurdjumov), has resulted in millions of dollars in crop losses (Foottit et al. 2006). Although some notable world treatments address adventive aphids (e.g., Blackman and Eastop 1994, Blackman and Eastop 2000, Blackman and Eastop 2006) as do recent regional taxonomic inventories (e.g., Teulon et al. 2003, Foottit et al. 2006, Mondor et al. 2007), thorough taxonomic analyses of other regional faunas are needed. Where aphid faunas have been developed, the proportion of adventive species is high. For example, percentages of adventive species range from 19% of the North America aphid fauna (Foottit et al. 2006) to 100% of the Hawaiian aphid fauna as adventive (Mondor et al. 2007). Adventive aphids represent an increasing threat in most regions of the world; their detection will require new approaches such as DNA barcoding (Armstrong and Ball 2005). Historically, questions concerning the taxonomic determination of conspecific aphid species from different biogeographic regions has concerned aphid taxonomists (e.g., Hunter 1901, Foottit et al. 2006). The biogeographic origins of some adventive aphids can be complicated or ill defined. An example of these, among many (Foottit et al. 2006), is that of the woolly apple aphid, Eriosoma lanigerum (Hausman). Also known as the American blight, it gained notoriety as an apple pest in Europe where it was considered as originating from America. Although generally considered native to North America (e.g., Smith 1985), its reported origin 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 relies on accurate taxonomic information. We need extensive sampling to encompass the range of aphid variability from different hosts in different regions. To make predictions for possible future introductions and formulate necessary regulations, timely identifications based on sound taxonomic science is critical.

8 470 Gary L. Miller and Robert G. Foottit CONCLUSIONS From examination of the taxonomic history of the Aphidoidea, several conclusions can be drawn. Extensive study at all levels, including faunal studies, revisionary work, and development of a stable classification system for species and genera is needed. Given the complex life cycles of aphids and their parthenogenetic mode of reproduction, taxonomy has to be developed at the infraspecific level. Society has increasing needs, particularly in understanding processes involving adventive species, managing and protecting crops, and assessing the effects of climate change. Given these needs, it is important to deliver timely and accurate taxonomic information. This delivery can be accomplished most efficiently through an accessible Web-based system. While aphids might be considered a well-studied pest group, much work remains to be done. Those aphids that garnered Réaumur s (Fig 20.1) attention nearly three centuries ago remain a group in need of study, albeit in finer detail. REFERENCES Anonymous ARS Crop Protection and Quarantine National Program (304). Action Plan. code= 304&docid=355&up [Accessed 22 June 2006]. Armstrong, K. F. and S. L. Ball DNA barcodes for biosecurity: Invasive species identification. Philosophical Transactions of the Royal Society B.(Biological Sciences), 360, Barnes, J. K Asa Fitch and the emergence of American entomology, with an entomological bibliography and a catalog of taxonomic names and type specimens. New York State Museum Bulletin 461: Blackman, R. L. 1980a. Chromosome numbers in the Aphididae and their taxonomic significance. Systematic Entomology 5: Blackman, R. L. 1980b. Chromosomes and parthenogenesis in aphids. Pp In R. L. Blackman, G. M. Hewitt, and M. Ashburner (eds). Insect Cytogenetics. Symposium of the Royal Entomological Society of London Blackwell Scientific Publications, Oxford, Pp. 10. Blackman, R. L Aphid cytology and genetics. Pp In H. Szel giewicz (ed). Evolution and Biosystematics of Aphids. Proceedings of the International Aphidological Symposium at Jablonna, 5 11 April Polska Akademia Nauk Instytut Zoologii. 510 pp. Blackman, R. L Morphological discrimination of a tobacco-feeding form from Myzus persicae (Sulzer) (Hemiptera: Aphididae), and a key to New World Myzus (Nectarosiphon) species. Bulletin of Entomological Research 77: Blackman, R. L. and P. A. Brown Morphometric variation within and between populations of Rhopalosiphum maidis with a discussion of the taxonomic treatment of permanently parthenogenetic aphids (Homoptera: Aphididae). Entomologia Generalis 16: Blackman, R. L. and V. F. Eastop Aphids on the World s Trees: An Identification and Information Guide. CAB International, Wallingford, UK pp. Blackman, R. L. and V. F. Eastop Aphids on the World s Crops: An Identification and Information Guide. Second Edition. John Wiley & Sons, England. 466 pp. Blackman, R. L. and V. F. Eastop Aphids on the world s herbaceous plants and shrubs. 2 Vols. John Wiley & Sons Ltd., England pp. Buckton, G. B Monograph of the British Aphides. Ray Society, London 1: Capinera, J. L North American vegetable pests: the pattern of invasion. American Entomologist 48: Chan, C. K., A. R. Forbes, and D. A. Raworth Aphid-transmitted viruses and their vectors of the world. Agriculture Canada Technical Bulletin E: Coeur d acier, A., G. Cocuzza, E. Jousselin, V. Cavalieri, and S. Barbagallo Molecular phylogeny and systematics in the genus Brachycaudus (Homoptera: Aphididae): insights from a combined analysis of nuclear and mitochondrial genes. Zoologica Scripta 37: Deerr, N The History of Sugar. Volume 1. Chapman and Hall, London. 258 pp. Eastop, V. F Aphids and psyllids. Pp In Viruses and Invertebrates. North-Holland Research Monographs. Frontiers of Biology. North Holland Publishing, Amsterdam-London. 31. Eastop, V. F Worldwide importance of aphids as virus vectors. Pp In K. F. Harris and K. Maramorosh (eds). Aphids as Virus Vectors. Academic Press, New York. 559 pp. Eastop, V. F Diversity of the Sternorryncha within major climatic zones. Pp In L. A. Mound and N. Waloff (eds). Diversity of Insect Faunas. Symposia of the Royal Entomological Society of London Blackwell Scientific Publications, Oxford, Pp. 9. Eastop, V. F Sternorrhyncha as angiosperm taxonomists. Symbolae Botanicae Upsaliensis 22(4): Eastop, V. F. and R. L. Blackman Some new synonyms in Aphididae (Hemiptera: Sternorrhyncha). Zootaxa 1089: Eastop, V. F. and D. Hille Ris Lambers Survey of the World s Aphids. Dr. W. Junk, Publishers, The Hague. 573 pp. Fagan, M. M The uses of insect galls. American Naturalist 52:

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