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Phylloxeridae is a small family of plant-parasitic
hemiptera Hemiptera (; ) is an order of insects, commonly called true bugs, comprising over 80,000 species within groups such as the cicadas, aphids, planthoppers, leafhoppers, assassin bugs, bed bugs, and shield bugs. They range in size from to arou ...
ns closely related to aphids with only 75 described species. This group comprises two subfamilies (Phylloxerininae and Phylloxerinae) and 11
genera Genus ( plural genera ) is a taxonomic rank used in the biological classification of living and fossil organisms as well as viruses. In the hierarchy of biological classification, genus comes above species and below family. In binomial nomenclat ...
with one that is fossil. The genus type is ''
Phylloxera Grape phylloxera is an insect pest of commercial grapevines worldwide, originally native to eastern North America. Grape phylloxera (''Daktulosphaira vitifoliae'' (Fitch 1855) belong to the family Phylloxeridae, within the order Hemiptera, bu ...
''. The Phylloxeridae species are usually called phylloxerans or phylloxerids.


History and distribution

The first record of species of the family was in
Aphid Aphids are small sap-sucking insects and members of the superfamily Aphidoidea. Common names include greenfly and blackfly, although individuals within a species can vary widely in color. The group includes the fluffy white woolly aphids. A t ...
oidea by Latreille, 1802. In 1857 Herrich-Schaeffer described the family and named this group 'Phylloxeriden'. Lichtenstein was the first to use the word 'Phylloxeridae' in 1883. They have a worldwide distribution but seem to have originated from a moderate climate since they are more diverse in temperate climates and their adaptation to tropical life probably is of a secondary nature.


Behavior and ecology

Phylloxerans are aphid-like insects that are parasitic hemipterans on
deciduous In the fields of horticulture and Botany, the term ''deciduous'' () means "falling off at maturity" and "tending to fall off", in reference to trees and shrubs that seasonally shed leaves, usually in the autumn; to the shedding of petals, ...
trees and perennial fruit crops. They feed on leaves and roots and are cecidogenic, which means they induce
gall Galls (from the Latin , 'oak-apple') or ''cecidia'' (from the Greek , anything gushing out) are a kind of swelling growth on the external tissues of plants, fungi, or animals. Plant galls are abnormal outgrowths of plant tissues, similar to be ...
s to form. They have very complex life cycles with cyclical
parthenogenesis Parthenogenesis (; from the Greek grc, παρθένος, translit=parthénos, lit=virgin, label=none + grc, γένεσις, translit=génesis, lit=creation, label=none) is a natural form of asexual reproduction in which growth and developmen ...
and host alternation. In outline, a female fundatrix hatches from an overwintering egg on the primary host which is usually a woody plant before bud burst stimulating a gall to form on the young leaves. Winged offspring in the following or third generation migrate in spring to the secondary host (usually an herbaceous). Then, many winged and wingless generations may be produced on the secondary host before winged migrants return to the primary host in autumn. Males and mating females mate on the winter host and produce overwintering eggs. In the family Phylloxeridae, some species are holocyclic (meaning they produce both asexual and sexual generations) while some are anholocyclic (producing only asexual generations). Species of this family live within the galls on the host plants and also in the crevices of barks.


Economic importance

Phylloxerids can transmit diseases to plants. Their importance is even more perceptible historically. In fact, '' Daktulosphaira vitifoliae'' (grape phylloxera) is considered as the most economically important insect pest of commercial grapevines ''
Vitis ''Vitis'' (grapevine) is a genus of 79 accepted species of vining plants in the flowering plant family Vitaceae. The genus is made up of species predominantly from the Northern Hemisphere. It is economically important as the source of grapes, ...
'' worldwide. In the late 19th century, the phylloxera epidemic destroyed almost all the European grapes and they could only fix the problem by planting grapevines from the US, then grafting European grapevines onto American roots.


Morphology

The phylloxeran species are very small to minute insects. Besides, there is a high polymorphism in the family Phylloxeridae making it at times difficult to identify its members. Also, they can quite easily be confused with related insects such as adelgids and true aphids. The most important features used to tell them apart from their relatives and from other insects are the wings' venation, the
ovipositor The ovipositor is a tube-like organ used by some animals, especially insects, for the laying of eggs. In insects, an ovipositor consists of a maximum of three pairs of appendages. The details and morphology of the ovipositor vary, but typical ...
and some characteristics of their antennae. Phylloxerans have a three-segmented antenna in all forms (both adults and immature). The wings are held flat over the body at rest and the Cu1 and Cu2 of the front wings are stalked at the base. The
flagellum A flagellum (; ) is a hairlike appendage that protrudes from certain plant and animal sperm cells, and from a wide range of microorganisms to provide motility. Many protists with flagella are termed as flagellates. A microorganism may have f ...
always ends in a sensorium (or rhinaria) and adult females can have one or two additional sensorial on the flagellum. Egg laying females and males have
vestigial Vestigiality is the retention, during the process of evolution, of genetically determined structures or attributes that have lost some or all of the ancestral function in a given species. Assessment of the vestigiality must generally rely on co ...
mouthparts and are wingless. Concerning the immature, the nymphs resemble adults but never have the secondary sensorium. Also the immature of the sexuales have a unique non-feeding pupiform larva. Phylloxerans can be distinguished from adelgids by the fact that they have a vulva instead of a sclerotized ovipositor, and usually lack the wax glands or plates found in adelgids. They can also be distinguished from aphids because they have 3 veins while aphids have 4-6 veins.


Taxonomy/phylogeny

Phylloxeridae is part of the order Hemiptera and suborder Sternorrhyncha. But there is a lot of controversy when it comes to its position and
phylogeny A phylogenetic tree (also phylogeny or evolutionary tree Felsenstein J. (2004). ''Inferring Phylogenies'' Sinauer Associates: Sunderland, MA.) is a branching diagram or a tree showing the evolutionary relationships among various biological s ...
within this lineage, especially in regard to its relatives namely the adelgids (Adelgidae) and aphids (Aphididae). The following quote is an illustration: "Almost as many classifications of aphids have been proposed as there have been practicing taxonomists". "Aphids" here include Adelgidae, Aphididae and Phylloxeridae. In the past these three families mentioned above have been placed together in the same superfamily Aphidoidea. Generally, Phylloxeridae is placed together with Adelgidae in the superfamily Phylloxeroidea. In fact, bionomical similarity such as the
oviparous Oviparous animals are animals that lay their eggs, with little or no other embryonic development within the mother. This is the reproductive method of most fish, amphibians, most reptiles, and all pterosaurs, dinosaurs (including birds), and m ...
parthenogenetic females observed in these two groups and morphological characters (e.g. reduction of forewing venation, reduction of antennal segments) have been used in the study of their phylogeny, suggesting that they are closely related and leading to their placing as sister groups in Phylloxeroidea. Phylloxeridae together with Adelgidae form the oviparous aphids group which is
monophyletic In cladistics for a group of organisms, monophyly is the condition of being a clade—that is, a group of taxa composed only of a common ancestor (or more precisely an ancestral population) and all of its lineal descendants. Monophyletic gr ...
and is the sister group to Aphidoidea (other aphids). However, more recent studies using both morphological and molecular data to discuss the phylogeny and evolutionary history within Sternorrhyncha suggest that representatives of Adelgidae, Aphididae and Phylloxeridae have evolved independently and should not be combined in superfamilies. The debate is still open and more research is needed to clear up the Sternorrhyncha phylogeny.


References

*Blackman, R. L. 1978. Early development of the parthenogenetic egg in three species of aphids (Homoptera: Aphididae). – International Journal of Insect Morphology and Embryology 7: 33–44. *Blackman, R. L. and Eastop, V. F. 1994. Aphids on the world's trees. An identification and information guide. – CAB International, Wallingford. *Bonhag, P. 1955. Histochemical studies of the ovarian nurse tissue and oocytes of the milkweed bug, Oncopeltus fasciatus (Dallas). I. Cytology, nuclei acids, and carbohydrates. – Journal of Morphology 93: 177–230. *Evans, J. W. 1963. The phylogeny of the Homoptera. Annu. Rev. Entomol. 8: 77-94 *Gullan, P.J. and Cook, L.G. 2007. Phylogeny and higher classification of the scale insects (Hemiptera: Sternorrhyncha: Cocoidea). Zootaxa. 1668: 413-425 *Heie, O. E. 1987. Paleontology and phylogeny. In Minks, A. K. and Harrewijn, P. (Eds): Aphids, Their Biology, Natural Enemies and Control, Vol. 2, pp. 367–391. *Powell, S.K., Cooper, D.P. and Forneck, A. 2013. The biology, physiology and host-plant interactions of grappe phylloxera Daktulosphaira vitifoliae. Advances in Insect Physiology. 45: 159-218 *Von Dohlen, C.D. and Moran, N.A. 1995. Molecular phylogeny of the Homoptera: A paraphyletic taxon.. J.Mol. Evol. 41: 211-213 *Von Dohlen, C. D. and Moran, N. A. 2000. Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. – Biological Journal of the Linnean Society 71:689–717. *Stoetzel, M.B. 1998. Antennal and other characters useful in identification of the Aphidoidea (Homoptera). Proc. Entomol. Soc. Wash. 100(3). pp. 588–593 *Szklarzewicz, T., Jankowska, W., Wieczorek, K. and Wegierek, P. 2009.Structure of the ovaries of the primitive aphids Phylloxera glabra and Phylloxera coccinea (Hemiptera, Aphidinea: Phylloxeridae). — Acta Zoologica (Stockholm) 90: 123–131 *Wegierek, P. 2002. Relationships within Aphidomorpha on the basis of thorax morphology. – Prace Naukowe Uniwersytetu 9lÅskiego w Katowicach 2101: 106. *http://www.tolweb.org/Sternorrhyncha/10800 *http://research.amnh.org/pbi/bugs/true_bugs.html

*http://aphid.speciesfile.org/Common/editTaxon/Distribution/ShowDistribution.aspx?TaxonNamD=1170904 {{Taxonbar, from=Q2671139 Phylloxeridae, Agricultural pest insects Hemiptera families