Identification guide to Nordic aphids associated with mosses, horsetails and ferns (Bryophyta, Equisetophyta, Polypodiophyta) (Insecta, Hemiptera, Aphidoidea)

Keys and diagnoses of North european aphids (hemiptera, Aphidoidea) associated with mosses, horsetails and ferns are given, based on fresh and freeze-dried material. Numerous externally visible and thus informative characters, that are absent in cleared, slide-mounted specimens, such as body shape colours, wax coating and pattern etc., are utilized. Most of the species are illustrated by photographs of live specimens and drawings. root-feeding species living in the moss layer or otherwise often present in moss samples are also included, even if their hosts were spermatophytes. the combination of colour images and diagnoses, utilizing easily observed characters, allows the identification of a large number of species already in the field, and many more at home with the aid of a stereo microscope. Host plant relationships and association with ants are summarised, including new records. brief accounts on aphid life cycles, freeze-drying preparation techniques, etc. are also given to support the use of the keys.

this guide is, as far as possible, based on fresh and freeze-dried material, which maximizes the number of characters that can be used, including colouration and wax pattern. the measurements and indices available on slides are naturally also available on freeze-dried specimens, so slide-based keys can very well be used. Just as for slide-mounted material, knowledge of the host plant is of great help for the identification. Most aphids are monophagous or oligophagous, and closely related species usually feed on different plants, which makes plant-based keys fast and easy to use. A clear majority of the species are readily identifiable based on host plant data, diagnoses, colour images of live specimens, fresh or freezedried material and the aid of a good stereo microscope. Often just a glance at a photograph will appear to give the correct identification, but sibling species may be involved, so it should always be kept in mind that host plant association alone is not enough. Descriptions and figures should always be consulted before the decision is made. In some cases fine details need to be studied, and measurements may have to be taken. In most cases the necessary measurements can be taken on fresh and freeze-dried material, without any further processing. Sometimes, however, a water preparation on a slide, e.g., of a leg, is helpful, and in critical cases cleared and mounted specimens are needed. It should be borne in mind that all characters visible in slides are present also in freeze-dried material, and if not directly visible, always can be made so by clearing and mounting the specimen.
the present article is focused on the aphids associated with cryptogams of Finland and Scandinavia, including Iceland, Greenland, the Faroes and Svalbard. Included are also most of the species occurring in adjacent parts of north-eastern europe, the baltic region and northern central europe, including the british Isles. Some species feeding on spermatophytes, but often occurring in moss samples, are also included. Accounts on aphid life cycles, preservation and terminology are also given here, but they are kept short, and more or less limited to subjects needed for using the keys and diagnoses. this article is intended to be followed by papers dealing with aphids feeding on other plants, and the ultimate goal is to cover all aphids occurring in North europe. the keys, instead of being dichotomous, consist of multi-character diagnoses and synopses grouping the diagnoses into sections sharing one or a few easily observed characters. Accompanied by photographs and drawings the data given in the diagnoses should in most cases be enough to allow correct identifications, or when that is not the case, to give sufficient reason to doubt the results and seek additional information elsewhere in the literature. As a contrast to keys based on slide material, this article also aims at enabling the student to learn species in advance and to recognise them as they are encountered in the field.

Material and methods
the host records and distribution data are according to blackman & eastop (1994, 2006, 2014), heie (1980, 1986, 1992, 1994, 1995, 2004), holman (2009) and the database of the Finnish expert Group on hemiptera (http://biolcoll.utu.fi/hemi/tyoryhma/tyoryhma_eng.htm), comprising most of the aphid data recorded from Finland (predominantly by O. heikinheimo and myself), with additional records from adjacent countries. the photographs and drawings are original, unless otherwise stated. My own records of hosts are marked with asterisks (*) in the host lists of the diagnoses and in the host tables (Appendices 1 and 2), as are records by Osmo heikinheimo and other Finnish collectors whenever I have been able to confirm the relationships (e.g., from Heikinheimo's field notes).
The identifications underlying the figures, keys and diagnoses have all been confirmed by checking against keys and descriptions based on cleared specimens. the diagnoses are kept short, particularly when photographs are available, and the emphasis is on the parthenogenetic morphs, particularly aptera. In many cases, characteristics of juveniles are also included. More elaborate descriptions of all morphs are given in, e.g., heie (1980,1986,1992,1994,1995,2004) and references therein. the diagnoses are, whenever possible, based on my own observations on fresh and freeze-dried material supplemented by data from heie (1980, 1986, 1992, 1995, 2004), blackman 2010and blackman & eastop (1994, European Journal of Taxonomy 145: 1-55 (2015 2006, 2014) (generally not cited separately) or other references, cited as used. In addition, valuable information on aphid taxonomy and bibliography can be found in Favret (2015). the plant nomenclature is based on hill et al. (2006: mosses) and Karlsson & Agestam (2014: vascular plants). Data on attendant ants are mostly my own (denoted by an asterisk), the nomenclature following Abenius et al. 2012.

Preservation and labelling
For students who wish to preserve aphid material or build a reference collection without spending excessive time with the slide mounting process, here is an easy recipe for freeze-dried specimens: 1. Collect the aphids in small test tubes or other suitable vials, with or without part of the host plant. A slip of tissue paper may be inserted to absorb excess moisture. label the vial and close it, e.g., with a cotton wool stopper. Keep the vial out of direct sunshine. 2. At home, put the vials into a container with a layer of desiccant (Silica gel, rubin gel) on bottom in the freezer (-18°C is suitable) and close the container (Fig. 1A). Petri Ahlroth (pers. comm.) uses silica gel cat litter as desiccant, and his aphid specimens are excellent. More material can be added when needed. Some specimens can be pinned on micro-pins and the wings set at this stage. It may be useful to pin the specimens from below, in which case the blunt end of the micro pins may be sharpened (Fig. 1b). Pinned specimens should preferably be mounted on a piece of, e.g., foam polystyrene to support the legs during the drying process. the wings of alatae can also be set ( Fig. 1C). 3. After a few months the aphids are dry and ready for the collection, as such in tubes or other vials (Fig. 1D), pinned, or glued to cardboard. Galls usually take at least six months to dry properly. For examples of dry, pinned specimens, see Fig. 1e-G.
to speed up the drying process, vacuum equipment can be used (e.g., Albrecht 1994), but that is by no means necessary.
Please note that in addition to the basic information on the labels (place, date and collector) it is of utmost importance to add information on the aphid's position and occurrence on the plant. Just the name of the host plant is not enough to ascertain a true aphid-host relationship. "Cirsium arvense. Dense colony on upper part of stalk." is a correct host plant statement, whereas "Cirsium arvense" alone denotes a substrate or (the worst scenario) a subsequently added inferred "host" name, and its role as host is not determined. Sadly enough, museum collections consist too often of many inadequately labelled aphid samples, and many temporary substrates may have entered published host lists. An addition of attendant ants is also welcome: "Attended by Lasius niger", preferably accompanied by a couple of preserved ants. If the attending ant species cannot be identified with certainty, as is often the case with, e.g., wood ants (Formica), it is better to leave the species name out instead of implying a certain identification.

Aphid life cycles
this chapter is intentionally kept very brief. I will just try to give the information needed for using my keys. In the outer zone an ordinary monoecious holocycle in Aphididae. The fertilized egg overwinters and in spring the first viviparous parhenogenetic generation, the fundatrix (stem-mother) hatches. Upon the fundatrix follows a variable number of viviparous females (viviparae), apterous and/or alate. In autumn (sometimes earlier) sexuparae are born and in turn give birth to oviparous (sexual) females (ovipara) and males, which mate, and the oviparae lay eggs. the inner zone shows an anholocycle, with only parthenogenetic females (viviparous in Aphididae, oviparous in Adelgidae).

Fig. 3.
Dioecious one-year holocycle (Rhopalosiphum padi). the inner zone represents the primary host (bird cherry, Prunus padus and allies), the outer zone the secondary (usually graminoids). the fundatrix gives birth to apterae, which in turn give birth to alatae, most of which migrate to the secondary hosts.
In autumn males and gynoparae (viviparae giving birth to oviparae) migrate to the primary host, where mating and egg-laying take place. A small fraction of the viviparae may remain on the primary host throughout the summer.
ALBRECHT A.C., Identification guide to Nordic aphids Fig. 4. Dioecious one-year holocycle accompanied by a continuous anholocycle on the secondary host, e.g., Pachypappella lactea (leaf galls on aspen, Populus tremula; roots of spruce, Picea abies) or Tetraneura ulmi (leaf galls on elm, Ulmus; subterraneous parts of grasses, Poaceae). Zones as in Fig. 3. In some years the Finnish populations on the primary hosts (for P. lactea in South Finland) may be more or less absent, and their existence is dependent on the populations on the secondary hosts.

Fig. 5.
Dioecious two-year holocycle in Adelgidae, e.g., Adelges laricis (shoot galls on spruce, Picea; needles of larch, Larix). All females oviparous. the fundatrix (hatched from a fertilized egg) overwinters as a larva, and induces the formation of a pineapple-like gall on the primary host. All her offspring are alate (gallicolae) and migrate to the secondary host, where they lay eggs on the needles. the aphids hatching move to the twigs where they hibernate as young larvae (the 'neosistens' stage). In spring they move back to the needles and become adults (sistentes). their offspring are either alate sexuparae and migrate to spruce, or apterous 'progredientes'. In autumn the sexuparae fly to spruce and lay eggs which become sexual females and males, which mate. the females then lay eggs out of which new fundatrices hatch.
= viviparous the presence of the species in the Nordic countries is based on heie (1980,1982,1986,1992,1994,1995,2004) and my own databases. the countries are denoted by letters as follows:

Synoptic key and diagnoses for aphids on mosses, horsetails and ferns
For a summary of the host-plant relationships of aphids feeding on mosses, horsetails and ferns, see Appendix 1 and 2. In the diagnoses my own host records and relevant others from the database are denoted by an asterisk (*) after the host name. For geographical and phenological records from Finland, see Albrecht (2010).

D F N S.
Note the question of whether the moss-feeding M. escherichi represents the secondary host generations of the Sorbus-feeding M. drepanosiphoides (börner, 1939), which would make the two taxa synonymous (Blackman & Eastop 2014), has not yet been definitely resolved, and is awaiting results from molecular analyses. Until then, I prefer to continue regarding the two taxa as separate species, because they are morphologically distinctive. Among other characteristics are the siphunculi, which are generally quite constant throughout the parthenogenetic morphs. In the Sorbus-feeding fundatrix and alatae they are long, black and truncate, with a large terminal aperture. the transfer experiments of M. drepanosiphoides from Sorbus to Plagiothecium laetum performed by Stekolshchikov & Shaposhnikov (1993) would, however, give support for the synonymy.

Diagnosis
Apterae ovoid, robustly built, 0.6-1 mm, whitish, with a thin wax-dusting and exuding wax tufts from spinal and pleural wax gland plates on abdominal segments 3-6 (4 longitudinal rows of plates); marginal wax gland plates absent. legs, antennae and rostrum short and stout. Antennae 4-5-segmented. hind femur not distinctly thickened. rIV+V with a rather narrow and indistinct pale subapical zone. tarsal segments fused (the segment border depicted in fig. 66b by Blackman & Eastop (1994, 2014 looks anomalous, and may be an artefact).
Dioecious, alternating between leaf galls on aspen Populus tremula (Salicaceae) and Norway spruce Picea abies (Pinaceae), where the aphids live on thin roots within and above the mor layer (a compacted European Journal of Taxonomy 145: 1-55 (2015) Fig. 18. Pachypappella lactea (tullgren, 1909). A-E. Apt. and wax cells on terminal Picea abies roots. F-G. Apt. from Hylocomium splendens sample. two wax gland plates in F indicated by arrows.
ALBRECHT A.C., Identification guide to Nordic aphids humus layer beneath the moss layer), among moss or litter. the apterae reside in nests of dense wax wool, 1.5-2 mm across, usually one aphid in each. the nests often occur in small groups, often within the looser, wider and less distinctly delimited wax exudate of Prociphilus xylostei (deGeer, 1773) and Pachypappa species. P. lactea has a continuous anholocyclic population on spruce roots. Not associated with ants. Danielsson (1990aDanielsson ( , 1990b gives keys and descriptions of the root-feeding generations of Pachypappella, Gootiella and Pachypappa. See also Carter & Danielsson (1991).

Diagnosis
Apterae 1-2 mm, pale yellowish with wax tufts posteriorly. Cells in abdominal wax gland plates with a small central spot (Fig. 19A). Segments 1 and 2 of tarsi less distinctly separated than in P. tremulae (linnaeus, 1761) and P. vesicalis Koch, 1856. legs longer, hind femur more than 4 × its maximum width. Antennae usually 6-segmented, PT finger-like. Spines at apices of tibiae weak, not much stronger than the hairs on first tarsal segment. Hind tibia on dorsal side bearing 2-5 spine-like hairs with short, blunt apices. Dioecious. Alternating between Populus tremula (Salicaceae) and Picea abies roots (Pinaceae), where wax-covered colonies are formed. Anholocyclic hibernation occurs.

Diagnosis
Apterae 1-2 mm. resembling P. populi. Cells in abdominal wax gland plates with a larger central spot (as in Fig. 19b). Segments 1 and 2 of all tarsi distinctly separated from each other. Spines at apices of tibiae very robust, much stronger than hairs on first tarsal segment. Dorsal hairs on hind tibia with fairly short and blunt apices. life cycle as in the previous species. Anholocyclic hibernation on roots of spruce Picea is common.

Diagnosis
Diagnosis based on Carter & Danielsson (1991). resembling P. populi. Antenna usually 5-segmented, Pt extremely short. Cells in abdominal wax gland plates with a larger central spot (Fig. 19b). Spines at apices of tibiae very robust, much stronger than the hairs on first tarsal segment. Dorsal hairs on hind tibia with long, pointed apices. Dioecious. Alternates between white poplar Populus alba (Salicaceae) and Picea roots (Pinaceae) where the aphids live in wax nests similar to those of Pachypapella lactea (Carter & Danielsson 1991).

Distribution
F S.

ABDBB. Pale subapical zone on RIV+V narrow, indistinct or absent. Wax glands may be present on head
Genus Prociphilus tullgren, 1925 Prociphilus xylostei (deGeer, 1773) Fig. 21 Diagnosis Apterae 1.2-2 mm, pale green with large wax gland plates (and wax tufts unless worn off) on head and abdomen. rIV+V = 0.2 × ht2, without pale subapical zone. legs and antennae slender. Dioecious. Alternating between honeysuckle Lonicera (Caprifoliaceae) and thin, mycorrhizal Picea abies roots (Pinaceae), where the colonies are coated with wax wool and where the aphids may hibernate. P. xylostei apparently has a continuous anholocyclic population on spruce roots. Common in moss samples from spruce forests.

Distribution
D F N S.
ALBRECHT A.C., Identification guide to Nordic aphids Prociphilus pini (burmeister, 1835) Fig. 22 Diagnosis Apterae 1.2-2 mm. As P. xylostei but cream or pale pinkish rather than greenish or yellowish. rIV+V as long as ht2, with narrow and indistinct subapical zone. Dioecious. Alternating between Crataegus (rosaceae) and thin roots of Pinus (Pinaceae). May be found all the year in moss samples in pine forests, especially on rock.
Distribution D F N S.

Diagnosis
Diagnosis based on heie (2004). Apterae about 2.9 mm, wax-covered. two pairs of wax gland plates on head. Posterior plates on head better developed than anterior ones. A narrow pale subapical zone on rIV+V distinct. Dioecious, alternating between ash Fraxinus excelsior (sometimes other Oleaceae) and fir Abies (Pinaceae), where it feeds in wax-covered colonies on the roots.

Fig. 23. Aphis equiseticola
ALBRECHT A.C., Identification guide to Nordic aphids Distribution D N S.

Aphis gossypii Glover, 1877
Diagnosis Aptera 0.8-1.7 mm. Pale green to blackish green; siphunculi black. Small, pale yellow specimens occur in in crowded colonies or hot conditions. In cold temperate regions mostly in glasshouses. Dioecious with several unrelated plants as primary hosts, in europe, however, mostly anholocyclic. Very similar to A. beccabungae Koch, 1855 (Fig. 24)

Distribution
Known from NW russia only.

Recorded host
Dennstaedtiaceae: Pteridium aquilinum. ALBRECHT A.C., Identification guide to Nordic aphids alternating between peach (Prunus persica) and plants of more than 40 families. Anholocyclic in the north and in the tropics. Usually in urban environments, also a common indoor pest.

Distribution
D F N S.

Discussion
Up to now, identification keys for aphids have been based on macerated specimens on microscopic slides, much of the emphasis being laid on measurements and indices based on them; in most cases only the ranges are given, without statistical parameters. Attempting to identify fresh or freeze-dried aphids using these keys may at first thought feel troublesome, but for the present that is the way we have to go.
And it works, provided you have a good stereo microscope. Almost all of the characters described in the keys are well visible in unmacerated material, so slides need only exceptionally be made. And often a leg or antenna immersed in water on a slide is enough. One goal of this guide is to enhance the use of characters lost in the maceration process, many of which participate in the distinctiveness of the species and make it possible to identify as many of them as possible even in the field, although it is always advisable to look up the species in the literature and check the identification.
Most aphids are easily found by simply inspecting the plants, keeping the eyes open for abnormal growth, the presence of ants and other phenomena that may indicate the presence of aphids. Aphids associated with mosses are, however, generally considered rare and difficult to find. Aphids feeding on mycorrhizal conifer roots are readily revealed by the white wax wool they produce, but the genuine moss-feeders are almost impossible to spot in the field. Besides being small, they live hidden in the moss tussocks and are often cryptically coloured. In funnel samples they usually die before reaching the collection jar, which perhaps explains the seeming rarity of moss aphids. The best way of finding them is to dry all excess water from the moss, sieve it through a 1-2 mm mesh and study the sample alive under a stereo loupe. It seems quite safe to anticipate that, with the right methodology applied, moss aphids will prove to be surprisingly common throughout Northern europe.