Several conifer aphids of the family Adelgidae were probably introduced on nursery stock from Asia to Europe in the nineteenth century on imported fir (Abies spp.) and most of them were unknown before reaching Europe (Kenis et al., 2007). D. nordmannianae was introduced in Europe in the 1840s on imported Nordmann fir (Abies nordmanniana) and moved onto a new host, the European silver fir, Abies alba, where it has since caused important damage on young silver fir trees and Nordmann fir plantations (Bejer, 1981; Nierhaus-Wunderwald and Forster, 1999; Kenis et al., 2007).

Outside its natural range (the Northern hemisphere boreal and temperate climate environments; more precisely the higher regions of the west Caucasus), D. nordmannianae is found with silver and Nordmann fir plantations in Europe (Nierhaus-Wunderwald and Forster, 1999). D. nordmannianae has the potential to invade all areas where the host(s) are grown. The distribution area of firs is limited to the mountainous regions of eastern, western, southern and central Europe. This area ranges from 52°N in the north (Poland) to 40°N in the south (northern border of Greece) and from 5°E in the west (western Alps) to 27°E in the east (Romania, Bulgaria). Isolated occurrences can be found in France in Central Massif and the Pyrenees, and in northern Spain (Pyrenees extending the western limit to 1°W). Some specimens can be found in central and southern Italy (Calabria) extending the southern limit to 38°N. In the distribution area northeast of the river Danube, silver fir can be found at altitudes from 135 m above sea level in Poland to 1350 m in the eastern Carpathians (Romania). Southwest of the Danube, it grows from 325 m in the Apennines (Italy) to 2100 m in the western Alps, and extending up to 2900 m in the Pirin Mountains (Bulgaria). Within the main distribution area, the species forms a belt 500-600 m (800 m) wide, which moves to higher altitudes from north to south (from Wolf, 2003).

There is a high risk of introduction via infested nursery stock anywhere that Abies spp. and Picea orientalis hosts are grown commercially or as ornamentals.

Adelgids are highly host-specific; D. nordmannianae only attacks secondary hosts in the genus Abies (Havill and Foottit, 2007).

Abies nordmanniana and Picea orientalis originate from Caucasus where they grow in stands with Fagus orientalis. The distribution areas of these species are associated with altitudes 1000-2000 m above sea levels (Løfting, 1973). In Northern Europe forestry, P. orientalis is absent. Another Picea spp. is present in Northern Europe, Picea abies, but D. nordmannianae could not adapt to this host (Nierhaus-Wunderwald and Forster, 1999). The sexual part of the D. nordmanniane life cycle is therefore absent and Abies spp. is the only host available to this pest.

 Adelgidae display cyclical parthenogenesis and have complex, multigeneration, polymorphic life cycles. The Adelgidae differ from the Aphidiae by the absence of siphunculi (the pair of protruding organs found on the dorsal side of the last segment of the abdomen and also called cornicles, through which a sugary secretion is extruded) and the retention of oviparity in all generations. Adelgids feed on gymnosperms and only on certain genera in the Pinaceae (Heie, 1987; Havill and Foottit, 2007). D. nordmannianae performs a holocycle with host alternation between Picea orientalis (its primary host) and Abies (secondary host). Sexual reproduction takes place on the primary host, Picea orientalis.

Reproductive Biology

The following section is from Kirkeby-Thomsen (1998).

In the country of origin (the Pontus massive in Caucasus and northern Turkey), the life cycle of D. nordmannianae takes 2 years. In the summer, females lay eggs (sexuales) in between the Caucasian spruce needles. In August, the eggs hatch into fundatrix crawlers, which wander on the host and settle near a bud. After settling, the fundatrix undergoes diapause and overwinters as a first-instar larva. In the spring, the fundatrix moults through 2^nd and 3^rd stage larvae to imago and starts to lay eggs (from 300 to 500 eggs). The fundatrix induces the galls from the bud of P. orientalis on which it feeds. The bud swells and after bud break the needles swell at the bases (Varty, 1956). The gallicola hatch from eggs laid by the fundatrix, and these crawlers settle at the swollen needle base in the bud. Their feeding completes the gall formation. In the gall cavities, the gallicola develops through four larval stages. The gall is terminal, unlike other Adelges (Adelges cooleyi and Adelges viridis). Shoot growth does not go beyond the gall. Adult gallicola are alate and migrate to the secondary (or intermediate) host (Abies spp.). On the secondary host, gallicola migrants settle on the needles and produce up to 40 eggs. Neosistens crawlers hatch from these eggs, settle on the twig and overwinter as first-instar larvae. In the spring, they moult through three instars into the adult stage. Sistens means the generation that stops. Sistens have three larval instars (Eichhorn, 1970). Eggs laid by gallicola, hiemosistens, aestivosistens and progrediens aptera can all hatch into sistens. The sistens can either be a hiemosistens (hiemo = winter) or an aestivosistens (eastivo = summer). After hatching and locating a suitable feeding site on the newly-developed twig, the hiemosistens stops its development and spends the summer as a first-instar larva. Late in summer or early autumn, it moults from second to third instar and overwinters. In spring, just prior to bud break, the development is finished and parthenogenetic egg production is initiated. Aestivosistens is a summer generation that will reproduce once over midsummer. This generation is rare and is usually not considered (Varty, 1956).

Progrediens is the generation that continues or progresses. Progression after hatching establishes it on the abaxial surface of the newly-formed needles. If for some reason the progrediens do not have access to new needles, they may start feeding on one-year-old needles. If the feeding site is not suitable the progrediens will die without reproducing. According to Varty (1956), the progrediens is negative geotactic and positive phototactic, preferring the upper branches on infested trees. Progrediens that settle on the new needles will moult through four larval instars into adults, becoming waxy, and starting to produce eggs. The fecundity of progrediens is low; only 10-15 eggs are produced per female (Varty, 1956; Eichhorn, 1970). A fraction of the progrediens that settle on the new needles differentiate morphologically to become alate. This is the sexupara generation that will migrate to locate the primary host (P. orientalis) again. It is not possible to distinguish between the progrediens apetra and the sexuapara in the first larval instars at the time of establishing on the needles. In the last larval instar, the wings are visible. The sexupara does not produce wax on Abies spp. Sexupara migrate to P. orientalis, where it settles and overwinters. It produces a light wax, and in the spring, egg laying starts. As with apterous progrediens, the fecundity is low (Varty, 1956). The sexuales is the sexual generation where both females and males are present. Varty (1956) describes young P. orientalis shoots that retain their bud scale during flushing, and it is under this scale that the sexuales crawlers gather and establish. Larval mortality is very high in this generation.

Physiology and Phenology

In the yearly anholocycle that relates to Northern European conditions, where the primary host, P. orientalis is absent, only sistens are produced in the winter; they then transform into progrediens aptera or sexupara in the spring with no sexual reproduction into alate sexuales, and back to the sistens in the winter. In this case, the gallicolae are very rare both due to the absence of the primary host and the failure of the sexuales. The sexupara is produced and migrates to locate P. orientalis, but no or very few gallicola return to Abies spp. to contribute to population growth. In the anholocycle under North European conditions, sistens overwinter as third-instar larvae, finish their development in the spring prior to bud break and start egg laying. From the eggs, sistens hatch that establish on twigs; progrediens aptera settle on new needles; and sexupara alate migrate to a primary host that does not exist. Sistens hatch from the progrediens generation, which settle on the twigs. Sistens moult into third instars in the late summer and overwinter.

Kenis et al. (2007) report that a natural enemy of D. nordmannianae, first reported in Turkey and also found in Russia and Georgia, could be a good candidate for biological control. This chamaemyiid fly, Leucopis sp., has been reported to kill 50% of D. nordmannianae eggs in Turkey in the spring. L. hennigrapta appears to be an important predator of D. nordmannianae in Turkey and possibly the Caucasus. Small populations of D. nordmannianae in Turkey seemed to correlate with high levels of predation by L. hennigrapta. Other potential candidates have been found in the area including undetermined dipterans from the Syrphidae and Cecidomyiidae families and coleopterans from the families Coccinellidae and Derodontidae.

Environmental

• Agroforestry

General

• Botanical garden/zoo

Silver firs with lush green needles are more attractive to D. nordmannianae than older, yellowish trees with short shoots. The first attack usually occurs as the trees are young and up to 1.5 m in height. As the trees reach 2 m and more, the chances of attack decrease. D. nordmannianae are light- and warm temperature-loving insects and need sunny exposition for their development. The first signs of infestation will be found on young, free-standing firs at thicket or plantation edges and exposed to the sun. The general symptoms described in this datasheet are the ones found on fir (from Nierhaus-Wunderwald and Forster, 1999) and not Picea orientalis, the Caucasian spruce.

The overwintering, dark larvae develop into egg-producing females early, which then lay their eggs close to the buds in the spring. As the eggs hatch on spring shoots, fir needles infected with dark D. nordmannianae larvae curl back and get deformed into a 'bottle brush' shape as the larvae feed on them. Infestation with the harmless twig aphid (Mindarus abietinus) causes the needles to curl up, exposing the white, waxy stripes outside, whereas D. nordmannianae curls the needles the other way. The larvae eventually migrate to the abaxial surface of the needles. A few months later, white, waxy secretions are found on the abaxial surface of the needles and fresh clutches of D. nordmannianae are also found on shoots and needles. On the abaxial surface of the youngest needles, sucking young larvae can reach high population densities. At high attack densities, the fir tips eventually turn yellow, the needles drop and the whole tip will die down. On the stem, dark spots surrounded by whiter, woolly and fluffy material can be found as the adults are feeding on the sap of the stems. The bark of the older stems eventually cracks into pox-like chips. The shoot will swell at its base and the buds will no longer burst and die. The tree will be weakened by the feeding activity of D. nordmannianae and is susceptible to secondary attacks and infections by pathogens and other pests.

Note that galls can be formed by the sexual morphs, but only on the primary host (P. orientalis) so galls are not found on firs.

Morphological characteristics for identification under anholocyclic conditions (no sexual cycle, only found with Abies spp. hosts)

This relates to the description of neoprogrediens only (see Biology and Ecology text section for a detailed life cycle and names of the different morphs).

The first-instar sistens larvae are used to determine species. The genus is characterized by the presence of five pairs of lateral abdominal spiracles. All stages have an elongated form. There is much variation in chitinization and wax gland distribution between morphs, but both characteristics are constant for one morph of any one species (Carter, 1971). The number of wax pores within the spinal-plates of the meso- and meta-thorax and the first three abdominal segments on the first-instar sistens larvae can be used to distinguish between European species of Adelgidea (see Eichhorn, 1967). D. nordmannianae looks like a scale and has the shape of a turtle with dorsal plates. It is brownish yellow when it settles on bark for feeding, but soon turns black. All the way around the body margin and in a row across the dorsal side, wax is produced by a series of wax glands (Blackman and Eastop, 1994; Kirkeby-Thomsen, 1998).

D. nordmannianae is very similar to Dreyfusia piceae, at the time referred as to Adelges nordmiannae and Adelges piceae (Eichhorn, 1967). Havill et al. (2007) later demonstrated that the sequence divergence between these two species is only small (0.18–0.36%).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control and Sanitary Measures

Cutting and burning (on site) of severely-attacked trees during the winter is a cultural control measure used in forested areas where no chemicals are used. Firs should be propagated and grown underneath a slightly thinned mature stand or mixed with young alder or European rowan (Nierhaus-Wunderwald and Forster, 1999). Firs with little damage to the top shoots should be spared as resistance to D. nordmannianae will increase with age.

Movement Control

Do not pull uprooted trees heavily infested with D. nordmannianae through a plantation; the aphids could spread to healthy firs by contact.

Biological Control

Some options proposed by Kenis et al. (2007) include a chamaemyiid fly, Leucopis sp., some dipterans from the Syrphidae and Cecidomyiidae families and coleopterans from the families Coccinellidae and Derodontidae. Ravn et al. (2013) found L. hennigrata to be the most promising biological agent. L. hennigrapta appears to be an important naturally-occuring predator of D. nordmannianae in Turkey and possibly the Caucasus. Small populations of D. nordmannianae in Turkey seemed to correlate with high levels of predation by L. hennigrapta

Chemical Control

Chemical control is used in Christmas tree plantations and might be necessary during the growing season to protect the trees from 'bottle brush' deformation. Compounds used include synthetic pyrethroids, nicotinoids, organophosphates and carbamates (Demolis et al., 1991, 1999; Palmer, 2009).

Host Resistance (incl. vaccination)

Ongoing breeding and research in quantitative genetics of Nordmann fir Christmas trees are taking place in Denmark, and results indicate substantial economic gains (Nielsen and Hansen, 2000). Natural resistance had been observed in the past in Abies nordmanniana and Abies alba by Varty (1956), Løfting (1973), Larsen et al.(1984) and others. Natural resistance was then confirmed by Kirkeby-Thomsen (1998). Since then some molecular projects have been initiated such as the development of microsatellite markers in A. nordmanniana (Hansen et al., 2005). The breeding programme uses clonal seed orchards (CSOs) and testing of open-pollinated families (half-sib families) (Hansen and Kjær, 2006).

27/07/10 Original text by:

CRCNPB Australia, CRC for National Plant Biosecurity, Canberra, Australia