This review continues the series of our publications on the seasonal adaptations of plant bugs (Heteroptera: Miridae) (Saulich and Musolin, 2019, 2020, 2021) and is devoted to species of the subfamily Phylinae, one of the largest in this family. The subfamily Phylinae unites 6 globally distributed tribes with a total of over 440 genera. Its highest species diversity is observed in areas with a Mediterranean climate and also in deserts and semi-deserts. Besides the Mediterranean proper, Asia Minor, and Central Asia in the Palaearctic, these are climatically similar territories in the south of North America in the Nearctic, South Africa, and southern and central Australia. The fauna of the temperate zone mainly includes species of three tribes: Pilophorini (16 genera), Hallodapini (56 genera), and Phylini (over 230 genera) (Schuh and Schwartz, 1988; Cassis and Schuh, 2012; Schuh and Weirauch, 2020).

This review is based on our own database of publications on the seasonal adaptations in Heteroptera and the online database The Planetary Biodiversity Inventory (PBI) for Plant Bugs (Schuh, 2012, 2021; Konstantinov and Namyatova, 2019) containing data on distribution and trophic specialization of plant bug species and on the specimens kept in museum collections (data as of May 2021). The review includes 39 species for which at least basic information on phenology and voltinism is available.

Tribe PILOPHORINI Douglas et Scott, 1876

The tribe Pilophorini is represented in the Holarctic by about 150 species in 16 genera. All the studied species are zoophytophages, i.e., predators that additionally feed on plants. They are often associated with certain species of plants or types of vegetation (Schuh, 1991; Cassis and Schuh, 2012; Schuh and Weirauch, 2020).

Genus Pilophorus Hahn, 1826

The genus Pilophorus comprises about 130 species distributed in different zoogeographic regions, mostly in the Holarctic and Oriental regions. The bugs are zoophytophages feeding on aphids and other small insects; many species are myrmecomorphic (Southwood and Leston, 1959; Cassis and Schuh, 2012; Yasunaga et al., 2021).

Pilophorus cinnamopterus (Kirschbaum, 1856)

A Euro-Siberian species, widespread in the Palaearctic (Vinokurov et al., 2010) and unintentionally introduced to North America (Newfoundland) (Wheeler and Henry, 1992).

The bugs occur on pines (Pinus spp.) and larch trees (Larix spp.) (Southwood and Leston, 1959; Wheeler et al., 2006; Schuh, 2021). They are zoophytophages feeding on aphids (mainly of the tribe Cinarini), immature cones, needles, and resinous secretions of conifers (Kullenberg, 1944; Southwood and Leston, 1959; Wheeler, 2001). The bugs not only externally resemble ants but also mimic their behavior, which is characteristic of true mimicry (Wheeler et al., 2006).

The species is univoltine and overwinters at the egg stage. In Sweden, England, and France adults emerge in the second half of July and usually survive until early October (Kullenberg, 1944; Southwood and Leston, 1959; Ehanno, 1987). According to the label data of museum specimens, adults are predominantly recorded in nature from June to September (Table 1; Schuh, 2021).

Table 1. The main parameters of seasonal development of plant bugs of the subfamily Phylinae
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Pilophorus clavatus (Linnaeus, 1767)

A Holarctic species (Vinokurov et al., 2010).

Both in European Russia and in the Russian Far East, the species has been recorded on a large number of broad-leaved trees and on shrubs, especially often on willows (Salix spp.) (Kerzhner, 1988). In Canada and the US, the species is known on willows (Kelton, 1980; Wheeler et al., 2006), oaks (Quercus spp.), and dogwoods (Cornus spp.) (Schuh and Schwartz, 1988).

The species is univoltine and overwinters at the egg stage. In England, nymphs occur in June–July, and adults, from July to September (Southwood and Leston, 1959; Schuh, 2021). The same timing of seasonal development was recorded for the Russian Far East (Kerzhner, 1988). Adults are predominantly recorded from July to September (see Table 1; Schuh, 2021).

Pilophorus confusus (Kirschbaum, 1856)

A Euro-Siberian species, unintentionally introduced to North America (Wheeler and Henry, 1992; Vinokurov et al., 2010).

The bugs usually occur on deciduous trees and shrubs (Schuh, 2021).

Diapausing eggs overwinter in young branches of various woody plants. In England, adult bugs commonly occur in July–August (Southwood and Leston, 1959). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

The seasonal cycle of P. confusus was studied in the south of Europe (Ramirez-Soria et al., 2018, 2019; as P. gallicus Remane, 1954), where this species plays an important role in control of the pear psyllid Cacopsylla pyri (L.) (Homoptera: Psyllidae) and other small arthropods damaging pear trees (Rosaceae: Pyrus communis L.). In Spain (Murcia Province: 38.4°N, 1.1°W), P. confusus completes three overlapping generations a year. Its active stages can be found on pear trees from March to early November (Sanchez and Ortin-Angulo, 2012). The species overwinters at the egg stage. Three years of observations have shown that the earliest nymphs appear from late March to late April, and adults of the first generation emerge in mid-May. These adults account for the first (spring) population peak that occurs at moderate temperatures and an increasing day length. The second (summer) peak is the most pronounced and occurs during the period of the highest air temperatures and the longest day. The third (autumn) population peak coincides with a decrease in temperature and day length, and the bugs gradually disappear in nature since midOctober (Ramirez-Soria et al., 2018).

In a laboratory study, all the stages developed actively when kept under long-day (LD) conditions of 16 h of light and 8 h of darkness per day, whereas the embryonic diapause was induced under short-day (SD) conditions of 9 h of light and 15 h of darkness per day. In contrast to many other insects hibernating at the egg stage, the temperature (18 and 23°C) had a weak effect on embryonic diapause induction in P. confusus. Females laid two types of eggs: non-diapausing and diapausing. Nymphs hatched from non-diapausing eggs in 15 days at a temperature of 25°C and LD. When diapausing eggs were reactivated for 90 days at a low temperature of 6°C and LD and transferred to the conditions suitable for incubation (25°C and LD), nymphs started hatching on average in 22.3 ± 0.5 days (Ramirez-Soria et al., 2019).

This pattern was also observed under the natural conditions of southeastern Spain. The percentage of actively developing (i.e., non-diapausing) eggs was the greatest in the first generation of P. confusus and the lowest in the third generation, whereas that of diapausing eggs was greater in the last generation. Three categories of females were found: females of the first category laid only actively developing (non-diapausing) eggs, those of the second category laid only diapausing eggs, and females of the third category laid both types of eggs simultaneously. The proportion of females laying mixed egg batches only slightly varied between the generations: from 14.3 to 25.0%. In contrast, the proportions of females laying actively developing eggs and diapausing eggs varied strongly between the generations: females of the first category prevailed in the spring generation (66.7%) and their proportion strongly decreased in the autumn generation, while females of the second category were few in the spring generation and their proportion increased in the autumn generation (85.7%) (Fig. 1; Ramirez-Soria et al., 2018).

Fig. 1.
figure 1

Fractions of females of Pilophorus confusus (Kirschbaum) that produced diapausing eggs, non-diapausing eggs, and both types of eggs (in one batch) under natural conditions in Murcia Province, Spain, 38.4°N, 1.1°W (after Ramirez-Soria et al., 2018; as Pilophorus gallicus Remane). The mean temperature (°C) and day length (light : darkness; L : D) for the week preceding the collection of females in nature are indicated under each bar.

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Pilophorus perplexus Douglas et Scott, 1875

The species is distributed in Europe, North Africa (Madeira, Algeria, Morocco, Tunisia), and Asia (Georgia, Armenia, Azerbaijan, Iran), and was unintentionally introduced to North America (Wheeler and Henry, 1992; Kerzhner and Josifov, 1999; Schuh, 2021).

The bugs usually occur on deciduous trees and shrubs (Schuh, 2021).

The species was studied in the south of England, where it is commonly found on oaks (Quercus spp.). Adults occur in nature from July to October; they feed on aphids (especially of the subfamily Lachninae), eggs and early-instar larvae of the codling moth, spider mites, and other small invertebrates. Eggs are laid in young twigs of the host plants. Nymphs hatch from the overwintered eggs in May–June of the following year. The species has one generation a year (Southwood and Leston, 1959). Adults are predominantly recorded from June to September (see Table 1; Schuh, 2021).

Pilophorus typicus (Distant, 1909)

The species is distributed in Southeast Asia (Kerzhner and Josifov, 1999; Yasunaga et al., 2014, 2021; Schuh, 2021).

The bugs feed on various herbaceous plants, including such vegetable crops as cucumbers, eggplants, red peppers, pumpkins, etc., and often act as greenhouse pests. Nymphs occur on plants of the families Acanthaceae, Asteraceae, Convolvulaceae, Ericaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Rutaceae, Solanaceae, and Urticaceae. This is a zoophytophagous species attacking thrips, whiteflies, leafhoppers, and spider mites, and ecologically closely associated with ants (Yasunaga et al., 2021).

In the south of Japan (Kyushu and Ryukyu islands), P. typicus is active almost year-round, all the stages of development occurring throughout the year. According to many-year observation data, in Nagasaki (32.8°N, 129.9°E) the species completes four generations a year (Yasunaga et al., 2021). Adults are mainly recorded from May to December (see Table 1; Schuh, 2021).

Pilophorus typicus was studied in Japan (Shikoku Island: Nankoku, Kochi Prefecture, 33.6°N, 133.6°E) as a promising control agent to be used against the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), the main pest of tobacco in Southeast Asia. In the laboratory the bugs were fed on leaves of Sedum rubrotinctum (Saxifragales: Crassulaceae) and frozen eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae), and the developmental parameters of all the stages from egg to adult were studied within a wide range of temperatures: from 17.5 to 30.0°C (Nishikawa et al., 2010). It was found out that the developmental time of individual stages strongly depended on the temperature but was close in different sexes. The duration of development from egg to adult was 72.0 ± 4.5 days at 17.5°C and 20.7 ± 1.1 days at 30.0°C (mean ± SD) (Nishikawa et al., 2010).

The following regression equations for the development rate were determined within the temperature range 17.5–30.0°C: 1/Y = −0.0337 + 0.0028T, r2 = 0.9953 for females and 1/Y = −0.0340 + 0.0028T, r2 = 0.9854 for males, where Y is the developmental time and T is the temperature. The lower temperature thresholds and the sums of effective temperatures required for completion of development from egg to adult were also determined: 12.0°C and 357.1 degree-days for females; 12.1°C and 357.1 degree-days for males. The cited researchers concluded that the most favorable temperatures for rearing P. typicus were close to 25.0–27.5°C. At the same time, since the food used in rearing the bugs under the experimental conditions was too expensive, an alternative food source should be found before P. typicus can be effectively used as a biological control agent (Nishikawa et al., 2010).

Tribe HALLODAPINI Van Duzee, 1916

This is a relatively small, globally distributed tribe including 64 genera (Cassis and Schuh, 2012). Most of its species are associated with ants, and many are myrmecomorphic.

Genus Hallodapus Fieber, 1858

Hallodapus montandoni Reuter, 1895

The species is distributed in Europe, the Caucasus, and Central Asia, as far eastward as Mongolia and Northwest China (Kerzhner and Josifov, 1999; Konstantinov and Vinokurov, 2011).

In England the bugs can be found in meadows, usually on bare ground between grass sods. They attack the ants Myrmica scabrinodis Nylander (Hymenoptera: Formicidae), with which they usually co-occur. Long-winged individuals are extremely rare.

The species is univoltine and overwinters at the egg stage. Nymphs appear in early June; adults emerge in late July and usually survive until September (Southwood and Leston, 1959). Judging by the museum collections, adults are predominantly recorded from May to August (see Table 1; Schuh, 2021).

Hallodapus rufescens (Burmeister, 1835)

A Euro-Siberian species (Vinokurov et al., 2010).

These bugs are typical inhabitants of the soil surface, preferring open, well heated biotopes; in particular, in Siberia they are common in meadows (Vinokurov and Kanyukova, 1995). In England, they occur in heathlands. The short-winged form predominates in the populations, while long-winged individuals are rare (Southwood and Leston, 1959).

The species is univoltine. In England, adults emerge in early July and survive until September. Hibernation occurs at the egg stage (Southwood and Leston, 1959). Adults are recorded from June to August (see Table 1; Schuh, 2021).

Genus Systellonotus Fieber, 1858

Systellonotus triguttatus (Linnaeus, 1767)

The species is distributed in Europe; within Asia, it has been recorded in Armenia, Kazakhstan, and Tyumen Province of Russia (Vinokurov and Kanyukova, 1995; Kerzhner and Josifov, 1999; Konstantinov and Namyatova, 2008).

In England, the bugs inhabit open sandy areas overgrown with heather, usually co-occurring with the ants Formica fusca L. or Lasius niger (L.) which they externally resemble. Nymphs and adults are zoophytophages that consume both plant and animal food but never attack living ants. Their plant diet includes sap from the buds, young shoots, and immature fruits of heather and sheep fescue Festuca ovina; the bugs also suck honeydew and can feed on galls on willows. Their animal food consists mainly of aphids. Males are always long-winged; the myrmecomorphic females are usually short-winged (Southwood and Leston, 1959).

The species is univoltine and overwinters at the egg stage. Eggs are laid in bark fissures, in particular, of the creeping willow Salix repens. Nymphs hatch in the spring of the following year, and adults can be found in nature from late May to mid-August. Adults are predominantly recorded from May to August (see Table 1; Schuh, 2021).

Tribe PHYLINI Douglas et Scott, 1865

This is one of the largest tribes of the subfamily Phylinae, comprising over 136 Palaearctic genera and over 100 Nearctic genera (Cassis and Schuh, 2012; Schuh and Weirauch, 2020).

Genus Atomoscelis Reuter, 1875

Atomoscelis onusta (Fieber, 1861)

A West-Central Palaearctic species, unintentionally introduced to North America (Wheeler and Henry, 1992; Vinokurov et al., 2010).

The bugs are trophically associated with wild chenopods (Amaranthaceae) and also damage many crops: beets, corn, pumpkins, and melons (Asanova and Iskakov, 1977; Vinokurov and Kanyukova, 1995; Schuh, 2021).

The species overwinters at the egg stage. In Kazakhstan, it has three generations a year, with pre-adult development taking about one month (Asanova and Iskakov, 1977). Adults are commonly recorded from March to October (see Table 1; Schuh, 2021).

Genus Atractotomus Fieber, 1858

Atractotomus magnicornis (Fallén, 1807)

A European species, unintentionally introduced to North America (Wheeler and Henry, 1992; Kerzhner and Josifov, 1999).

According to observations in England, the bugs usually live on spruces (Picea spp.) and rarely occur on other conifers (Southwood and Leston, 1959). They have been found on many species of pines (Pinus spp.) (Schuh, 2021).

The species overwinters at the egg stage. Adults emerge in late June or early July and survive until September. Eggs are laid on the host plants, and nymphs hatch in the following spring. The species is univoltine (Southwood and Leston, 1959). Adults are predominantly recorded in nature from June to August (Table 1; Schuh, 2021).

Atractotomus mali (Meyer-Dür, 1843)

A Palaearctic species, unintentionally introduced to North America (Wheeler and Henry, 1992; Kerzhner and Josifov, 1999).

The bugs are phytozoophages feeding on spider mites, aphids and their sugary secretions, lepidopteran larvae and pupae, and other small insects. In Kazakhstan they are known as predators destroying apple ermine larvae in their nests (Asanova and Iskakov, 1977). They may also feed by cannibalism (Collyer, 1953). The main host plants are trees and shrubs of the family Rosaceae, though the bugs have been found on plants of many other families, including conifers (Schuh, 2021).

The seasonal cycle is univoltine in Europe and the northern regions of North America (Canada) (Kullenberg, 1944; Jonsson, 1985; Ehanno, 1987). According to observations in England, the species also has one generation a year; eggs overwinter, and adults occur in nature from late June to early August (Southwood and Leston, 1959). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

Genus Campylomma Reuter, 1878

Campylomma verbasci (Meyer-Dür, 1843) (mullein plant bug)

A West-Palaearctic species, distributed in the entire North Africa, Europe, Transcaucasia, Turkey, Central Asia, and northeastern China (Konstantinov and Vinokurov, 2011). It was discovered on the British Isles as late as the 1930s (Wheeler and Henry, 1992). This is an adventive species in North America (Kerzhner and Josifov, 1999).

In Europe, the species used to be considered of no importance to agriculture, but in 1990 significant damage was reported in apple orchards in the Netherlands, Belgium, and Bulgaria (Wheeler, 2000a, 2000b). The bugs are phytozoophages feeding on small insects: thrips, whiteflies, aphids, and small lepidopteran larvae. In Kazakhstan, they reach high densities on cotton plants where they feed on spider mites (Asanova and Iskakov, 1977). The species has been found on many deciduous trees (Schuh, 2021).

The species completes 2 generations a year over most of its European range (Southwood and Leston, 1959; Niemczyk, 1978; Torres et al., 1999), 1 generation in Norway (60°N) (Skanland, 1980; Jonsson, 1983, 1985), and 3 generations in Iran (Pourhadji, 2001). Eggs overwinter in diapause (Thistlewood and Smith, 1996). Adults are predominantly recorded from May to September (see Table 1; Schuh, 2021).

This species is characterized by a change of host plants during the season. Nymphs of the first (overwintered) generation feed on woody plants. Adults of this generation emerge in June–July and migrate to herbaceous plants, more often to the great mullein Verbascum thapsus, where they give rise to the second generation that develops entirely on herbaceous plants. In August–October, adults of the second generation return from grasses to woody plants, mainly to apple and pear trees, where they lay eggs to overwinter in the young stems (Southwood and Leston, 1959).

The seasonal development of C. verbasci was extensively studied in Canada, because after naturalization of this species in North America it became an important pest of orchard trees. The punctures made by the feeding early-instar nymphs in the setting apple and pear fruits appear later as dark corky scars, reducing the quality and commercial value of fruit. The nymphs of C. verbasci also feed as predators and destroy small insects; however, in the overall balance the damage caused by nymphs feeding on apple trees outweighs their utility as predators. In contrast, on pear trees C. verbasci is the most important predator of the pear psyllid Psylla pyri L.; therefore, it was recommended to preserve this bug in pear crops (Thistlewood and Smith, 1996).

In Canada (Richmond, British Columbia, 49.2°N, 123.1°W; Ontario, Quebec, 46.8°N, 71.2°W), the species usually produces 2 or 3, and rarely even 4 generations a year. Nymphs of the first generation hatch from overwintered eggs in early May, when apple and pear trees start blossoming. In some years, up to 50% of the nymphs hatch within 3–4 days. The nymphs live in inflorescences or in silky nests of lepidopteran larvae. In early June, most of the emerging adults migrate to herbaceous plants and form several generations there; adults of the last generation return to fruit trees in September–October and lay overwintering eggs (Thistlewood et al., 1990; Thistlewood and Smith, 1996).

The developmental time of C. verbasci nymphs was estimated by different authors under laboratory conditions. The nymphal stage was completed in 23 days at 21°C (McMullen and Jong, 1970), in 21 days at 22°C (Smith and Borden, 1991), and in 16 days at 23°C (Niemczyk, 1978). Animal food is required for nymphal development, although pollen can partly compensate for the lack of proteins (Bartlett, 1996).

The results of laboratory studies at different constant temperatures were used in developing a model to predict the timing of nymphs hatching from overwintered eggs under natural conditions (Judd and McBrien, 1994).

Genus Chlamydatus Curtis, 1833

Chlamydatus allii V.G. Putshkov, 1959

A Eurasian steppe species (Vinokurov et al., 2010).

In European Russia, the bugs have been recorded on wild garlic (Allium spp.), and they are known to damage the leek Allium porrum L. (Vinokurov et al., 2010).

The species overwinters at the adult stage (Asanova and Iskakov, 1977). In Russia adults are recorded in July and September, and sporadically in other months (see Table 1; Schuh, 2021).

Chlamydatus evanescens (Boheman, 1852)

A Eurasian species (Kerzhner and Josifov, 1999)

The bugs feed on Lepidium spp., less commonly on Sedum spp. (Southwood and Leston, 1959).

In England, the species completes two generations a year. Adults of the summer generation emerge in June and early July, those of the autumn generation, in late August and September and even in October; they overwinter and reactivate in May of the following year. Eggs are laid on the leaves of the host plant. The color of the hatching nymphs matches that of the young leaves (Southwood and Leston, 1959). Overwintering of the species at the adult stage was also observed in Sweden (Kullenberg, 1944). Adults are commonly recorded in August (see Table 1; Schuh, 2021).

Chlamydatus pulicarius (Fallén, 1807)

A Holarctic species (Schuh and Schwartz, 2005; Schuh, 2021).

In Siberia, the bugs are more often found in meadows (Vinokurov and Kanyukova, 1995). Similar to Ch. pullus, Ch. pulicarius is a polyphagous species (Putshkov, 1972; Schuh, 2021). In Kazakhstan, the bugs also occur on corn, beets, and buckwheat.

The species is bivoltine and overwinters at the egg stage (Asanova and Iskakov, 1977). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

Chlamydatus pullus (Reuter, 1870)

A Holarctic species (Schuh and Schwartz, 2005; Vinokurov et al., 2010).

The bugs damage many field and vegetable crops, being more common on alfalfa, sainfoin, and clover.

The species largely produces 2 generations a year in Kazakhstan, and 3 generations in the southern regions. It overwinters at the egg stage. Adults occur from late May to late autumn (Asanova and Iskakov, 1977).

The species was studied in England, where the bugs can often be found on sorrels (Rumex spp.) and the common knotgrass Polygonum aviculare L., though their main host plants are the white clover Trifolium repens L. and the hop clover Medicago lupulina L. Two generations are completed in a year. Adults of the first generation emerge in late May and early June, those of the second generation, in late July, and some of them survive until late September. The species overwinters at the egg stage. Adults of both sexes are always long-winged (Southwood and Leston, 1959).

Adults are predominantly recorded from May to August (see Table 1; Schuh, 2021).

Chlamydatus wilkinsoni (Douglas et Scott, 1866)

A Holarctic circumpolar species (Vinokurov et al., 2010; Schuh, 2021).

In Siberia, the bugs occur on goosefoots, often in wetlands and mountain tundra (Vinokurov and Kanyukova, 1995).

In England, adults can be found from May to August. They are usually short-winged, while long-winged individuals of both sexes are very rare (Southwood and Leston, 1959). Adults are most commonly recorded in July and August in different parts of the species’ range (see Table 1; Schuh, 2021).

Genus Compsidolon Reuter, 1899

Compsidolon salicellum (Herrich-Schaeffer, 1841)

A Euro-Siberian species, unintentionally introduced to North America (Wheeler and Henry, 1992; Vinokurov et al., 2010).

The bugs live on blackberries and other herbaceous and woody plants, including the common hazel Corylus avellana (L.) H. Karst., willows (Salix spp.), alders (Alnus spp.), and apple trees (Malus spp.) (Schuh, 2021). They are zoophytophages feeding on small insects and mites.

In England, the species can be found from late July to October. It overwinters at the egg stage (Southwood and Leston, 1959).

Genus Europiella Reuter, 1909

Europiella artemisiae (Becker, 1864)

A Holarctic species (Schuh, 2004; Vinokurov et al., 2010).

The bugs damage vegetable and field crops. In the wild they are trophically associated only with various wormwoods (Artemisia spp.) (Asanova and Iskakov, 1977).

The species is multivoltine and overwinters at the egg stage. It produces 1 or 2 generations a year in the northern regions of Kazakhstan, and 3 or 4 generations in the south (Asanova and Iskakov, 1977). The species was studied in England, where it also has two generations a year. Adults of the first generation appear in late June and July, those of the second generation, from late August to October (Southwood and Leston, 1959). Adults are predominantly recorded from April to October in different parts of the species’ range (see Table 1; Schuh, 2021).

Europiella decolor (Uhler, 1893)

A Holarctic species (Schuh, 2004; Vinokurov et al., 2010).

The main host plants belong to the genera Artemisia and Chrysothamnus (Asteraceae), although in the Palaearctic the bugs also feed on Lamiaceae. Unlike most species of the subfamily Phylinae, these bugs are commonly found on plants that are not yet in bloom (Schuh, 2004).

In England, adults emerge in late June and early July and become already rare in early August. The species produces one generation a year, with eggs overwintering and nymphs hatching in May of the following year (Southwood and Leston, 1959). These observations are not quite consistent with the label data of museum specimens, according to which adults are predominantly recorded from February to October, with a peak of occurrence in June–August (see Table 1; Schuh, 2021).

Genus Megalocoleus Reuter, 1890

Megalocoleus molliculus (Fallén, 1807)

A trans-Palaearctic species, unintentionally introduced to North America (Wheeler and Henry, 1992; Vinokurov et al., 2010).

The bugs are common on yarrows (Achillea spp.) and other composites (Southwood and Leston, 1959; Vinokurov and Kanyukova, 1995; Matocq, 2004).

The seasonal cycle of the species was studied in England, where it overwinters at the egg stage; nymphs hatch in early June, and adults emerge in early July and can be found until September. One generation a year is produced (Southwood and Leston, 1959). Adults are predominantly recorded from May to August (Table 1; Schuh, 2021).

Megalocoleus tanaceti (Fallén, 1807)

A Euro-Siberian species (Matocq, 2004; Vinokurov et al., 2010).

In England, the bugs commonly occur on buds, flowers, and immature fruits of tansy (Tanacetum spp.; Asteraceae).

Adults can be found from mid-July to early September. Females lay overwintering eggs in the stems of blossoming plants, usually at the base of the secondary corymbs. Nymphs hatch the following summer. One generation a year is produced (Southwood and Leston, 1959). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

Genus Monosynamma Scott, 1864

Monosynamma bohemanni (Fallén, 1829)

A Holarctic species (Vinokurov et al., 2010; Schuh, 2021).

In Siberia, the bugs live on willows (Salix spp.) (Vinokurov and Kanyukova, 1995); in England, they also inhabit willows, but only those growing on coastal sand dunes. The species is also known from legumes, composites, and other herbaceous and some woody plants (Schuh, 2021).

Adults occur from late June to early August. The species is univoltine and overwinters at the egg stage (Southwood and Leston, 1959). Adults are predominantly recorded from June to September (see Table 1; Schuh, 2021).

Genus Parapsallus Wagner, 1952

Parapsallus vitellinus (Scholtz, 1847)

A trans-Eurasian species, unintentionally introduced to North America (Wheeler and Henry, 1992; Vinokurov et al., 2010).

The bugs commonly occur on conifers, often on larch trees (Larix spp.).

In England, adults occur from late June to early August. The species is univoltine and overwinters at the egg stage (Southwood and Leston, 1959).

Genus Phoenicocoris Reuter, 1875

Phoenicocoris obscurellus (Fallén, 1829)

A Euro-Siberian species, widespread from the west of Europe, including the British Isles, Portugal, and Italy, to the Russian Far East (Kerzhner and Josifov, 1999; Schwartz and Stonedahl, 2004; Vinokurov et al., 2010).

The bugs commonly occur on the Scots pine Pinus sylvestris L.; in France, also on the common juniper Juniperus communis L. (Schwartz and Stonedahl, 2004).

In England, the earliest adults appear in mid-June and can be found until the end of August. The species is univoltine and overwinters at the egg stage (Butler, 1923; Southwood and Leston, 1959). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

Genus Phylus Hahn, 1831

Phylus coryli (Linnaeus, 1758)

A species widespread in Europe, recorded in Transcaucasia and Turkey, and unintentionally introduced to North America (Wheeler and Henry, 1992; Kerzhner and Josifov, 1999; Aukema et al., 2013).

The bugs usually live on hazel and feed on aphids, psyllids (Psyllidae), and other small insects (Southwood and Leston, 1959).

Eggs are laid in the young shoots near the stipules. Nymphs hatch in late May and early June. The earliest adults emerge in late June, and only a few of them survive until mid-August or early September. The species is univoltine (Butler, 1923; Southwood and Leston, 1959). Adults are predominantly recorded from June to August (Table 1; Schuh, 2021).

Phylus melanocephalus (Linnaeus 1767)

A European species; within Asia, it was recorded in Georgia, Armenia, and Turkey (Kerzhner and Josifov, 1999; Aukema et al., 2013).

The bugs commonly occur on oaks (Quercus spp.). They are phytozoophages feeding on aphids and other small insects.

Adults appear in the first half of June and survive until early August. Overwintering eggs are laid near the buds of young oaks. Nymphs hatch in mid-May. The species is univoltine (Southwood and Leston, 1959). Adults are predominantly recorded in June and July (see Table 1; Schuh, 2021).

Genus Plagiognathus Fieber, 1858

Plagiognathus arbustorum (Fabricius, 1794)

A Holarctic species (Schuh, 2001; Vinokurov et al., 2010). This is one of the commonest species of the family Miridae in England.

The bugs occur on various herbaceous plants, especially often on nettles (Urtica spp.) (Southwood and Leston, 1959; Schuh, 2021). In Kazakhstan, they prefer humid habitats. The species is phyzootophagous (Southwood and Leston, 1959) and polyphagous. The bugs damage peas and alfalfa (Asanova and Iskakov, 1977).

According to observations in England, nymphs hatch in May, and the earliest adults emerge in early July; in Kazakhstan, adults appear in mid-June and die off by the end of September. The species is univoltine and overwinters at the egg stage (Southwood and Leston, 1959; Asanova and Iskakov, 1977). Adults are predominantly recorded from May to September (Table 1; Schuh, 2021).

Plagiognathus chrysanthemi (Wolff, 1804)

A trans-Palaearctic species, unintentionally introduced to North America (Wheeler and Henry, 1992; Schuh, 2001; Vinokurov et al., 2010).

At high densities the bugs damage alfalfa, clover, and sainfoin crops; the species is regarded as a minor pest of herbaceous legumes (Putshkov, 1972; Asanova and Iskakov, 1977). In Canada, the bugs strongly damage legumes, especially the deervetch Lotus corniculatus L. that is usually grown for seeds (Guppy, 1963). In England, the species can be found in wastelands on ragworts (Senecio spp.), mayweeds (Anthemis spp.), yarrows (Achillea spp.), and other composites (Southwood and Leston, 1959).

According to observations in England, nymphs hatch in late May. The earliest adults emerge in late June, and some adults survive until October. Eggs are laid in July–August and overwinter, so that nymphs hatch in the spring of the following year. The species is known to be univoltine both in England (Southwood and Leston, 1959) and in the northern regions of North America (Canada) (Guppy, 1963).

Genus Plesiodema Reuter, 1875

Plesiodema pinetella (Zetterstedt, 1828)

A West-Central Palaearctic species (Schwartz, 2006; Vinokurov et al., 2010).

Adults can be found on various conifers (Pinus spp., Picea spp., Larix spp.) (Schwartz, 2006) from mid-June to late July (Southwood and Leston, 1959).

There is no exact information about the overwintering stage, though other species of this genus are known to overwinter as eggs (Yasunaga, 2003). Adults are predominantly recorded from May to July (see Table 1; Schuh, 2021).

Plesiodema stlaniki Kerzhner, 1979

The species is distributed in Siberia and the Russian Far East (Kerzhner and Josifov, 1999; Vinokurov et al., 2010), and also in Japan (the islands of Hokkaido and Honshu: Yasunaga, 2003).

In Japan, the bugs were found in the alpine belt on Pinus pumila Regel (Kerzhner, 1978, 1979).

The species is univoltine and overwinters at the egg stage. Nymphs occur in June and July (see Table 1; Yasunaga, 2003; Schuh, 2021).

Genus Psallus Fieber, 1858

Psallus ambiguus Fallén, 1807

A European-East Mediterranean species that is known, besides Europe, also from Georgia, Azerbaijan, Turkey, and Iran (Kerzhner and Josifov, 1999; Aukema et al., 2013).

The species was studied in detail in England, where it is widespread. The bugs commonly occur on apple trees (Malus spp.), hawthorns (Crataegus spp.), willows (Salix spp.), and other, predominantly woody plants. They are phytozoophages, both nymphs and adults consuming not only plant food but also aphids and other small insects (Southwood and Leston, 1959; Schuh, 2021).

Adults occur from late May to August in England and from mid-June to mid-July in Norway. Eggs are laid in young twigs of trees; nymphs hatch in May of the following year. The species is univoltine (Southwood and Leston, 1959; Jonsson, 1985). Adults are predominantly recorded in June and July (see Table 1; Schuh, 2021).

Psallus betuleti (Fallén, 1826)

A Holarctic species (Vinokurov et al., 2010; Schuh, 2021).

The bugs have been found on Betulaceae, mainly on birches (Betula spp.) and alders (Alnus spp.) (Kerzhner, 1978; Schuh, 2021). They are phytozoophages feeding on small insects, including aphids (Butler, 1923; Southwood and Leston, 1959).

In England, nymphs hatch in late April and early May. Adults emerge in late May and the first half of June and can be found until August (Southwood and Leston, 1959). Similar dates of adult emergence were recorded in the Netherlands (Aukema, 2008). Eggs are laid in young shoots of birch trees and overwinter. The species is univoltine (Southwood and Leston, 1959). Adults are predominantly recorded from May to September (see Table 1; Schuh, 2021).

Psallus falleni Reuter, 1883

A Holarctic species (Vinokurov et al., 2010).

The bugs occur on plants of the family Betulaceae (Kerzhner, 1978; Yasunaga and Vinokurov, 2000; Schuh, 2021).

In England, adults are especially numerous from late July to September, and occasional nymphs can be found even in early August. The species probably overwinters at the egg stage (Butler, 1923; Southwood and Leston, 1959). Adults are predominantly recorded from May to September (see Table 1; Schuh, 2021).

Psallus lepidus Fieber, 1858

The species is distributed in Europe and North Africa; within Asia it is known from Armenia and Azerbaijan. It was unintentionally introduced to North America (Wheeler and Henry, 1992; Kerzhner and Josifov, 1999).

In England, adults occur on ash trees (Fraxinus spp.) from mid-June to early September, and nymphs can be found even as late as August. In the opinion of Southwood and Leston (1959), the species probably produces two generations a year. Adults are mostly recorded from May to September (see Table 1; Schuh, 2021).

Psallus luridus Reuter, 1878

A Euro-Siberian species (Vinokurov et al., 2010).

In England, the bugs inhabit young trees of European larch Larix decidua. Adults can be found from mid-June to early August. The species is univoltine and overwinters at the egg stage (Southwood and Leston, 1959). Adults are predominantly recorded in July and August (see Table 1; Schuh, 2021).

Genus Pseudatomoscelis Poppius, 1911

Pseudatomoscelis seriatus (Reuter, 1876) (cotton fleahopper)

A Nearctic species (Schuh, 2021).

The bugs damage cotton plants in the USA. They are polyphages feeding on over 35 plant species and preferring species of the genus Croton (Snodgrass et al., 1984).

The species is multivoltine (Gaylor and Sterling, 1977). The seasonal development of its population was studied in Texas, USA (30.6°N, 96.3°W). From September to November females concentrate on blossoming hogworts Croton capitatus Michx. and lay diapausing eggs in their stems. Nymphs hatch in March and April, and newly emerged adults of the first generation migrate to various species of early-spring ephemeroid plants. As these plants become less attractive to bugs, the adults migrate to cotton fields and produce several generations there. In autumn the bugs migrate back to hogwort plants (Gaylor and Sterling, 1977; Breene et al., 1989).

The onset of facultative embryonic diapause in this species was found to depend on the living conditions of nymphs of the maternal generation. The highest sensitivity to day length was observed in early-instar nymphs (up to the III instar). The production of diapausing egg was controlled by the photoperiodic response of a long-day type with a threshold between 12 and 13 h at 26.7°C. If early-instar nymphs developed at a photophase shorter than the threshold one, the females laid diapausing eggs (Fig. 2; Gaylor and Sterling, 1977).

Fig. 2.
figure 2

Photoperiodic induction of embryonic diapause in Pseudatomoscelis seriatus (Reuter) at 26.7°C (Texas, USA, 30.6°N, 96.3°W; after Gaylor and Sterling, 1977). Bugs of the maternal generation were kept at constant day lengths and temperatures.

Full size image

The embryonic diapause was terminated under the influence of low temperatures. The greatest proportion of nymphs hatched from the diapausing eggs stored at about +4°C (Gaylor and Sterling, 1977).

Adults are predominantly recorded from March to October (Table 1; Schuh, 2021).

Genus Solenoxyphus Reuter, 1875

Solenoxyphus artemisiae Putshkov, 1978

The species is distributed in Turkmenistan and Uzbekistan (Konstantinov, 2008).

The species was originally described by Putshkov (1978) based on specimens collected from Artemisia badghysi Krasch. et Lincz. ex Poljakov (Asteraceae). According to observations in the eastern part of the Kara-Kum Desert (Kaplin, 1993), its main host plants are Kochia odontoptera Schrenk, Londesia eriantha Fisch. et C.A. Mey., Salsola sclerantha (C.A. Mey.) Akhani et Roalson, and S. carinata C.A. Mey. (Chenopodiaceae).

Two generations are produced annually; nymphs of the second generation can be found until late June, and adults that develop from them, in early July (Kaplin, 1993). The few adults kept in museums were collected in May (see Table 1; Schuh, 2021).

Genus Tytthus Fieber, 1864

Tytthus pygmaeus (Zetterstedt, 1838)

A Holarctic species (Vinokurov et al., 2010; Schuh, 2021).

The bugs live on sedges in humid biotopes in Siberia (Vinokurov and Kanyukova, 1995). The same information was reported for Canada (Kelton, 1980).

Adults emerge since mid-July and usually survive until early September. The species overwinters at the egg stage. Adults are always long-winged. Both nymphs and adults are predators feeding on eggs and small nymphs of leafhoppers (Cicadellidae) (Southwood and Leston, 1959). Adults are predominantly recorded from June to August (see Table 1; Schuh, 2021).

DISCUSSION

Analysis of the currently available data on voltinism and phenology of the 39 most studied species of the subfamily Phylinae in the Holarctic fauna show that most of the studied species are those of economic importance: either biological control agents or pests of economically important crops. The ecophysiological responses controlling the seasonal development of bugs, e.g., the pre-adult development rate, diapause induction and termination, and wing dimorphism, remain practically unstudied even in such a species-rich subfamily as Phylinae.

Five Holarctic species of the tribe Pilophorini have been studied in this respect. Three of them, distributed in the temperate zone, complete one generation a year and hibernate at the egg stage. This is clearly confirmed by their phenology: adults are the last to appear during the season, and only nymphs but not adults are present in the spring of the following year. However, there is still no reason to believe that their annual cycles are obligatorily univoltine, because the obligate nature of their diapause has not been proven experimentally and there is no data indicating that the species remain univoltine under the climatic conditions that allow more than one generation a year. The seasonal cycle of these species was studied only in regions with a boreal climate, where the sum of effective temperatures above the developmental threshold seems to be sufficient for only one generation per season.

The seasonal cycles of Pilophorus confusus and P. typicus have been studied in regions with a warmer climate: Spain and Japan, respectively. These species are multivoltine; depending on environmental conditions, they produce a greater number of generations (P. confusus) or are active all the year round, i.e., homodynamic (P. typicus).

The three studied species of the tribe Hallodapini have similar seasonal cycles with one generation per year and overwintering at the egg stage. However, the available data are insufficient to characterize the ecophysiological basis of univoltinism for the entire tribe.

The tribe Phylini is the largest in the subfamily Phylinae; some of its genera, such as Psallus and Campylomma, comprise up to 140 species each (Duwal et al., 2012; Konstantinov et al., 2015). This tribe also shows a higher diversity of seasonal patterns. Although overwintering at the egg stage is generally characteristic of the family Miridae, two species of the genus Chlamydatus of the tribe Phylini are known to overwinter as adults: Ch. allii in Kazakhstan (Asanova and Iskakov, 1977) and Ch. evanescens in England (Southwood and Leston, 1959) and Sweden (Kullenberg, 1944). Three out of five studied Chlamydatus species have a multivoltine seasonal cycle, and no data are available on the voltinism and overwintering stage of two other species, Ch. allii and Ch. wilkinsoni.

Of the remaining 26 species of the tribe Phylini listed in Table 1, six species have multivoltine seasonal cycles and complete from 2 to 4 generations a year in different climatic zones.

Species of this tribe also demonstrate a seasonal adaptation quite unusual for true bugs, namely the shift of host plants during the season. As described above, nymphs of the first (overwintering at the egg stage) generation of Campylomma verbasci feed on woody plants, and the emerging adults of this generation migrate to herbaceous plants, on which the second generation develops. Adults of the second generation return from herbaceous vegetation to woody plants in late summer or early autumn and lay overwintering eggs in the young stems (Southwood and Leston, 1959). Such a seasonal cycle is more typical of Homoptera than of Heteroptera, although it is also known in Lygocoris pabulinus from the tribe Mirini of the subfamily Mirinae (Saulich and Musolin, 2020).

In conclusion, it should be noted that the large subfamily Phylinae shows a considerable diversity of ecophysiological characteristics, such as trophic specialization, seasonal shift of host plants, voltinism, and the overwintering stage. The subfamily includes many agricultural pests and also species whose economic status and invasion potentials may change following climate warming and transformation of agricultural practices.