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ACTA AGROBOTANICA Vol. 65 (1): 11-20 2012

COMMERCIALLY IMPORTANT PROPERTIES OF OF THE

1Elżbieta Weryszko-Chmielewska, 2Anna Matysik-Woźniak, 1Aneta Sulborska, 2Robert Rejdak

1Department of Botany, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland 2Department of General Ophtalmology, Medical University of Lublin, Chmielna 1, 20-079 Lublin, Poland e-mail: [email protected]

Received: 10.10.2011

Abstract THE HISTORY OF USE OF Plantago PLANTS The centuries-old experience of folk medicine, nutritio- nal traditions, and the results of numerous research studies show Various Plantago have been used as that plants of the genus Plantago can be used for medicinal, food for humans and animals as well as medicinal, co- cosmetic, dietetic, and ritual purposes. smetic, and ritual plants. The traditional and multiple In the composition of Plantago, the- uses of these plants are confirmed by ethnobotanical re is an abundance of biologically active substances (among and ethnopharmacological research (Samuelsen, others, glycosides, flavonoids, polysaccharides, and vitamins) 2000; Ł uczaj, 2004; Cornara et al. 2009). exhibiting beneficial effects and, simultaneously, there is a low The medicinal properties of Plantago lanceola- content of compounds that may exert a toxic effect. Scientific ta have been known since ancient times. This species research has confirmed that Plantago plants have antioxidative, was used in China already 3000 years ago. In ancient apoptosis-inhibiting, protective, healing-enhancing, spasmoly- tic, anthelmintic, and properties; they inhibit the Rome Pliny the Elder recommended plantain as a me- development of some tumours, reduce the level of lipids in blo- dicine for 24 diseases. In folk medicine of many coun- od and inhibit tissue glycation. In phytotherapy, , stems, tries, the aerial parts of P. lanceolata are used external- and/or seeds of different plantain species are used. ly and internally to treat different ailments (Nowiń - Plantago leaves and seeds are also used to manufac- ski, 1983; Nishibe, 2002). In Italy the resin of ture creams, lotions, and face masks. Different parts of these P. lanceolata was used as a substitute for incense smo- plants (fresh material, extracts, or isolated substances) ke in church rituals. of this plantain, are also used in human and animal nutrition. Plantain leaves mixed with stems of other plants (Helichrysum, Thy- can be eaten like lettuce or added to salads, fried in pastry, used mus), were burnt to perfume clothes and rooms with to prepare a tea, juice, or wine. Its seeds are added to cakes, the smell of smoke (C ornara et al. 2009). bread, breakfast , ice cream, and drinks, or they are co- was included among the most oked like groats. Animals fed with plantain can live longer and important in the Chinese herbarium dated from are healthier, while meat derived from such animals is tastier the 1st century A.D. It was also used in ancient Gre- and healthier to humans. Plantago seeds are readily eaten by ece and Rome. Dioscorides, Pliny the Elder, and Galen cage birds. recommended it against and scorpion bites. It Plantain , produced in large amounts (up to 20,000 was also used in therapy during the Middle Ages (N o - pollen grains per 1 of P. lancolata), can cause allergies in sensitive people. Due to a long flowering period of plants of wiń ski, 1983; Samuelsen, 2000; Strzelec- the genus Plantago, the effect of the allergenic factor persists k a and Kowalski, 2000). Seeds of P. major were for many weeks. In Poland days with the maximum concentra- placed in the tombs of pharaohs, while its leaves were tion of airborne plantain pollen most often occur in July. used as a vegetable by the Chinese. Plantain was called White Man’s Foot by North American Indians, since it grew everywhere where the white man appeared. The Key words: Plantago, medicinal uses, cosmetics, edible Shoshone Indians applied heated leaves of this species plants, animal feed, allergenic pollen. to wounds (C lark, 1977). 12 Elżbieta Weryszko-Chmielewska, Anna Matysik-Woźniak, Aneta Sulborska, Robert Rejdak

THE CHARACTERISTICS OF The leaves of plants of the genus Plantago form THE GENUS Plantago a ground rosette. The blades are entire or denti- culate. The are small, bisexual, most frequen- The family comprises about tly borne in spike-like inflorescences (Fig. 1A). They 265 species widespread in temperate climate areas. produce a delicate scent in some species. The perianth The genus Plantago includes about 260 species of pe- consists of a 3-sepalled calyx and a 4-petalled corolla rennials, annuals and, exceptionally, shrubs (Szwey- forming a tube and 4 membranous lobes (Reardon kowscy, 2003). In Poland 17 species of the genus et al. 2009). The androecium comprises 4 fu- Plantago are found growing in the wild, among others, sed to the corolla tube which are several times longer P. lanceolata L., P. major L., P. media L., P. arena- than the (Fig. 1A). In these flowers, the stamens ria Waldst. and Kit., P. maritima L., P. altissima L., perform the role of the attractant. In P. media, they are P. patagonica Jacq., P. intermedia Gilib., P. corono- lily coloured and attract numerous insects (Lipiń - pus L., P. atrata Hoppe, P. serpentina All., and P. win- ski, 2010). The stamens have a rare feature of closing teri Wintg. (Mirek et al. 2002). The first four above- their anthers at high air humidity, which protects pol- -mentioned taxa belong to medicinal plants. Moreover, len against water (Maurizio and Grafl, 1969). other plantain species are included among plants used Plantago flowers represent an intermediate degree in therapy, inter alia, the ones growing in the Mediter- between anemophily and entomophily; for instance, ranean area: P. afra L. (= P. ), P. ovata Forsk., under favourable weather conditions perform the P. asiatica L., and P. depressa Willd. (Andrze- while collecting the pollen of P. lanceola- jewska-Golec, 1994). These plants can reprodu- ta, whereas in adverse weather its flowers are pollina- ce from seed or vegetatively from buds formed on their ted by the wind. These flowers do not produce nectar roots (M aurizio and Grafl, 1969). (Kugler, 1970).

Fig. 1. of (×3). B-D. Pollen grains of P. media (B) (×670), P. major (C) (×700), P. lanceolata (D) (×530). Commercially important properties of plants of the genus Plantago 13

A (fruit), which opens by a lid, develops and closes when dry (Weberling, 1992). In the fruit, from the pistil of the superior, mostly bilocular ovary there are usually 2 seeds and their coat can have diffe- (Podhajská and Rivola, 1992; Szweykow- rent shades of brown. The seeds are elliptically-shaped scy, 2003). The existing research shows that fruits ori- and their surface is smooth and shiny. In the seed coat, ginating from different populations of Plantago lance- there are cells accumulating and, as a result of olata significantly differ in size and shape (Truchan, that, soaked seeds swell up quickly and stick to the me- 2005). The fruit of Plantago has a special feature, since it dium (Maurizio and Grafl, 1969; Podhajská dehisces and releases seeds when it is wet (hygrochasy) and Rivola, 1992; Ś widziń ska, 1998).

Tab. 1. Characteristics of some species of Plantago and their traditional medicinal uses

No. Species Occurrence Morphological features Traditional medicinal use References

1. Plantago , north Plant height 10-60 cm. Herbal infusion – Strzelecka and lanceolata L. , Middle Lanceolate leaves form compresses for wounds, Kowalski, 2000; Asia. a ground rosette; brown burns; leaf juice used for Podbielkowski and flowers borne in spikes 1-3 ulcers and eye diseases. Sudnik-Wójcikowska, cm long. 2003. 2. Plantago Europe, Asia. Plant height up to 40 cm. Compresses from fresh Strzelecka and major L. Ovate, entire leaves form leaves for wounds and Kowalski, 2000; a ground rosette. Small ulcers; irrigation of Podbielkowski and greenish flowers borne in a wounds with leaf infusion; Sudnik-Wójcikowska, long, cylindrical spike. an antitussive agent. 2003. 3. Plantago Europe. Plant height 10-50 cm. Anti-inflammatory, Anioł-Kwiatkowska media L. Elliptical leaves borne in a astringent, expectorant et al., 1993; rosette. Fragrant flowers with activity. Podbielkowski and a whitish corolla form short Sudnik-Wójcikowska, spikes. 2003. 4. Plantago arenaria Europe, west Plant height up to 40 cm. Its Mild purgative. Strzelecka and Waldst. and Kit. Asia, west linear leaves are arranged Kowalski, 2000; (= P. indica) . oppositely. Whitish flowers Podbielkowski and form globular spikes growing Sudnik-Wójcikowska, from the axils of the highest 2003. leaves. 5. Plantago South Plant height ca. 30 cm. Purgative. Strzelecka and psyllium L. Europe. Linear, opposite leaves, Kowalski, 2000; (= P. afra) stems branched. Flowers with Podbielkowski and a brown corolla grow from Sudnik-Wójcikowska, the leaf axils. 2003. 6. South Europe, Plant height 20-40 cm. Mild purgative. Senderski, 2007; Forsk. south-west Linear, woolly haired leaves Podbielkowski and Asia, South form one or several ground Sudnik-Wójcikowska, America, North rosettes. The inflorescence is 2003. America. a spike. 7. Plantago Japan, Korea, Plant height 30-50 cm. The is a detoxicating, Andrzejewska – Golec asiatica L. China, Entire leaves with a parallel purgative, antipyretic and Makowczyńska, Indochina, venation forming a ground agent; it improves 2005. Malaysia, rosette. Small flowers borne eyesight; compress for Taiwan, east in a spike-like inflorescence. wounds. Siberia. Seeds – used in stomach ulcer disease and rhinoconjunctivitis; compress for snakebites. 8. Plantago depressa Asia – from the Plant height >10 cm. Purgative. Kletter snd Willd. Ural Mountains Elliptical leaves, elliptical Kriechbaum, 2001; to China and – lanceolate to oval, erect; www.eFloras.org Japan. they grow from a short stem. Small, white flowers. 14 Elżbieta Weryszko-Chmielewska, Anna Matysik-Woźniak, Aneta Sulborska, Robert Rejdak

Leaf anatomical characters ceolata 22.3-27.8 μm, Plantago major 19.5-27.0 μm, The leaves of P. lanceolata show the isolateral 27.0-32.0 μm. The pore diameter in structure. Diacytic stomata are distributed in the upper pollen grains of the above-mentioned species ranges and lower epidermis. The mesophyll consists of 1-3 from 2.0 to 6.0 μm. Pollen grains of P. major have layers of palisade parenchyma, located on both sides of a small number of pores (5-8), whereas this number the epidermis, and a multi-layered spongy parenchy- is much higher for P. media (7-11) and P. lanceolata ma situated in the central part of the lamella (Kohl- (9-15) (B eug, 2004). münzer, 1998; Gostin, 2009). In other plantain Species of the genus Plantago are included in species, e.g. P. lessingii, the spongy parenchyma is the list of plants producing allergenic pollen (Baldo poorly developed (Yukun, 1994). The largest spon- et al. 1982; D’Amato et al. 1991). Symptoms of gy parenchyma cells in the leaves of P. lanceolata are allergy induced by the effects of P. lanceolata pollen found in the inner layers of the mesophyll, and their have been recorded in North America, Europe, and diameter decreases in the direction of the epidermis . Since the flowering period of all represen- (Gostin, 2009). Vascular bundles and mucilage- tatives of this family lasts several months and plants -accumulating cells are distributed in the mesophyll produce significant amounts of pollen, the risk of pol- (Maurizio and Grafl, 1969). len allergy in sensitive people can continue for many Contrary to the previously mentioned species, weeks (Watson and Constable, 1991). the leaves of P. major have a structure typical for le- First pollen grains of Plantago are recorded in aves of dicotyledons. They are characterized by 3 lay- the air in particular regions of Poland at different times. ers of palisade parenchyma on the side of the upper They have been recorded earliest, already in the third epidermis and several layers of spongy parenchyma on decade of April, in Poznań and Łódź (Majkowska- the side of the lower epidermis (O noda et al. 2008). -Wojciechowska et al. 2006; Stach, 2006), and Glandular and non-glandular hairs occur on the latest (the second decade of May) in Szczecin and Lu- leaf surface in representatives of the genus Plantago. blin (Puc, 2006; Weryszko-Chmielewska The glandular trichomes can be club-shaped and they and Piotrowska, 2006). Maximum concentrations have a unicellular head or the head is divided vertical- of Plantago pollen grains in aeroplankton of different ly into two cells. The non-glandular trichomes located regions of Poland during the period 2001-2005 ranged 3 on the leaves of Plantago have different shapes and 3-33 pollen grains per 1 m of air; these values were structures. They can be very short, 1-3-celled, slightly the highest in Sosnowiec, Rzeszów and Lublin, and the longer, consisting of 2-9 cells, or multicellular, com- lowest in Poznań, Wrocław, and Łódź. Days with the posed of 14-40 cells. These hairs are characterized by maximum concentration were most frequently noted a smooth or papillose cuticle (Andrzejewska- in different decades of July, less frequently in June or -Golec and Ś wię tosł awski, 1993, 1998; A n - August (Weryszko-Chmielewska, 2006). drzejewska-Golec, 2000, 2003). P. lanceolata has the greatest allergenic impor- tance. The most often described is designated Pla l 1 and it has a weight of 16-20 kDa. It shows cross ALLERGENIC PROPERTIES OF reactions with the olive allergen Ole e 1 (Calabozo Plantago POLLEN et al. 2001). Likewise in many anemophilous plants, all Plantago species produce large amounts of pollen. It MEDICINAL USES has been calculated that one stamen of P. lanceolata Numerous species of the genus Plantago owe releases 7 700 – 20 000 pollen grains, in P. media it is their properties to the presence of many biologically 6 000 – 14 000 pollen grains, while in P. major 5 870 active substances, inter alia, glycosides, flavonoids, grains. One inflorescence of these species produces, re- polysaccharides, and vitamins. spectively, 2 million, 3.3 million, and 6.3 million pol- len grains (Kugler, 1970; Ś widziń ska, 1998; Plantago lanceolata Piotrowska, 2008). The research also shows that The leaf of ribwort plantain (Plantaginis lan- one of Plantago produces on average 1 mg of ceolatae folium) is raw material recognised in Polish pollen (M aurizio and Grafl, 1969). Pharmacopoeia VI and European Pharmacopoeia 5. Pollen grains of Plantago are spherical and Raw material products are recommended for internal multiporate with small verrucae on the exine surface use in airway infections as well as mucosal inflamma- (Beug, 2004) (Figs. 1B-D). Their diameter is in the tory changes of the oral cavity and throat; externally, range of 16-35 μm (Watson and Constable, it is used in dermatitis. Biologically active substances 1991), while according to Beug (2004) this value is found in ribwort plantain include, among others, irido- the following for the respective species: Plantagolan- id glycosides, flavonoids, polysaccharides in the form Commercially important properties of plants of the genus Plantago 15 of water soluble , and (Kohlmün- noids found in plantain is baicalein which causes the zer, 1998). death of cancer cells and inhibits the growth of human The level of iridoid glycosides, which include hepatoma cell lines (Motoo and Sawabu, 1994) aucubin and catalpol, in a natural population of P. lan- as well as exhibits strong antiproliferative effects on ceolata can reach even 9% of dry weight. Aucubin is a rat liver cancer cultures (Inoue and Jackson, precursor in catalpol biosynthesis (Bowers, 1991). 1999). Numerous studies have shown that extracts of Other studies show that the level of aucubin and ca- P. major have cytotoxic effects on cultures of diffe- talpol in the leaves of seven Plantago species was up rent human cancer cell lines and human leukaemic to, respectively, 0.27% and 1.81% of leaf dry weight cells (Matsukawa et al. 1993; L e Bail et al. (Jurišić et al. 2004). 1998; Gálvez et al. 2005). Samuelsen (2000) Aucubin exhibits numerous pharmacological reports about the antitumor use of P. major by folk activities: antibacterial, anti-inflammatory, and it also medicine in the Canary Islands, Venezuela, Chile and facilitates healing of skin wounds. It can be useful in Panama. local treatment of oral wounds (Shim et al. 2007). In the case of three other species: Plantago Aucubin is a specific inhibitor of NF-kB in mast cells, psyllium, P. arenaria, and P. ovata, medicinal raw ma- which may have a beneficial effect in the treatment of terial is the seed called Plantaginis semen. The seed chronic allergic conditions (Jeong et al. 2002). This coat contains mucilage and hemicellulose which cause glycoside has been shown to have an antiproliferative a strong swelling of seeds. Mucilaginous compounds effect on cancer cells (small-cell lung carcinoma), in- found in medicinal raw material contain xylose, rham- ducing their apoptosis (H ung et al. 2008). nose, arabinose, galactose, and uronic acids as well as Ground leaves or juice from fresh leaves of P. sugars (planteose, glucose, and fructose), oil, phyto- lanceolata are used to control external animal skin pa- sterols, aucubin, monoterpene, and triterpene alkalo- rasites. Both ethanol and aqueous extracts from leaves ids. Seeds of the aforementioned species are used as of this plant species have shown antihelminthic activi- a protective and coating drug and also as a purgative. ty in mice (K ozan et al. 2006). P. arenaria and P. ovata seeds have also been found Ribwort plantain is also used in the treatment of to reduce the level of cholesterol (Strzelecka and burns, insect bites, and stomach ulcers (Strzelecka Kowalski, 2000; Senderski, 2007). Seed hu- and Kowalski, 2000; Sarwa, 2001). Leaf extracts sks of P. ovata and P. psyllium are currently used in the have expectorant and antitussive effects as well as they pharmaceutical industry (Chan and Wypyszyk, exhibit immunotropic, adaptogenic, and acti- 1988; Dhar et al. 2000; 2005). vity (Andrzejewska-Golec, 1994). They are Rozaeipoor et al. (2000) showed that an extract also used for eye irrigation in rhinoconjunctivitis (S a - of P. ovata seeds significantly affected the immune muelsen, 2000; Sarwa, 2001). system of rabbits. It caused a reduction in anti-HD an- tibodies as well as an increase in the number of white Plantago major blood cells and spleen leukocytes. The aqueous extract Medicinal raw material is the leaf of common of P. ovata seeds reduced hyperglycaemia in type 1 plantain (Plantaginis maioris folium) which contains and 2 diabetes in rats. These properties show that this iridoid glycosides, flavonoids, mucilaginous compo- extract can be used in diabetes treatment (Kordošo- unds, phenolic acids, tannins, triterpene compounds, v á and Machová, 2006). vitamins C and K as well as mineral compounds Treatment with P. ovata seed coat preparations (Kohlmünzer, 1998; Strzelecka and K o - increases and stabilises the level of HDL – cholesterol, walski, 2000). thereby reducing the risk factors of cardiovascular sys- Leaf extracts exhibit protective and anti-inflam- tem diseases (S o l à et al. 2007). matory effects in digestive tract diseases, bronchitis, and pharyngitis (Strzelecka and Kowalski, 2000). APPLICATION IN COSMETICS Plantago major is a popular plant that has been used by Chinese medicine for many years to treat viral Plantago lanceolata and P. major are included diseases, from common colds to viral hepatitis. Phe- in the list of cosmetic plants. Aqueous infusions and nolic compounds (caffeic acid) isolated from the leaf stabilised fresh juice from leaves of these both plantain extract of this plantain show strong antiviral activity, in species are used in cosmetics. Antiseptic, antibacterial, particular against HIV-1 as well as HIV-2 and ADV-3 and astringent effects of their leaves are utilised (Pod- at multiplication stages (C hiang et al. 2002). bielkowski and Sudnik-Wójcikowska, P. major has properties stimulating the immu- 2003; Czerpak and J a b ł o ń ska-Trypuć , ne system. At specific doses, it causes proliferation of 2008). The extract from the leaves of P. lanceolata lymphocyte cultures. Seeds of this taxon show anti- is used to produce different cosmetics, among others, diarrhoeal activity (Lans et al. 2007). One of flavo- creams, lotions as well as face masks for oily and acne 16 Elżbieta Weryszko-Chmielewska, Anna Matysik-Woźniak, Aneta Sulborska, Robert Rejdak skin (Podbielkowski, 1992; J ę drzejko et al. stics of meat and fat desired by the consumer (Grela, 2007). 1995). Other authors (Hlava et al. 1984) recommend Plantago lanceolata is a plant that is official- the use of crushed fresh leaves of P. lanceolata in face ly allowed in animal nutrition (Grela, 1997). It was masks. These researchers also mention the species of demonstrated that the addition of herbal mixture con- P. psyllium whose seeds contain up to 10% of muci- taining P. lanceolata in the feeding of porkers impro- lage and are used to prepare a macerate in cold water ved meat taste and increased the amount of unsatura- and subsequently to produce nourishing creams and ted acids, which is a desired feature in human nutrition lotions. The literature confirms that seed husks of P. (Grela and Baranowska, 1999). P. lanceolata ovata and P. psyllium have found application in the stems are recommended as a food integrator for rab- cosmetics industry (D har et al. 2005). bits and other animals (Cornara et al. 2009). On the other hand, seeds dried, roasted, or milled for flour are Plantago AS AN EDIBLE PLANT used as food for cage birds. Seeds of this plantain are a delicacy for canaries (Clark, 1977; Fijał kowski Plantago major was used as a vegetable in Chi- and C hojnacka-Fijał kowska, 2009). na and by North American Indians, for example, from the Cherokee and Mohican tribes (Ł uczaj, 2004). Acknowledgements Leaves of different Plantago species are eaten raw or cooked, and their taste is compared to that of Research supported by the Ministry of Science chard. Only young leaves are consumed in the form of and Higher Education of Poland as the part of statutory salads, since older ones are fibrous and bitter (Clark, activities of Department of Botany, University of Life 1977; Ł uczaj, 2004). In Italy Plantago lanceolata Sciences in Lublin. leaves are used as an addition to salads or are eaten like lettuce (Samuelsen, 2000; Heimler et al. REFERENCES 2007). Plantain leaves are also used as an addition to A n d r z e j e w s k a - G o l e c E . , 1994. Ontogeny of trichomes soups and as a cooked vegetable. 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(ed). Katedra i Zakład Farmakognozji z Pracownią jące, przyspieszające procesy gojenia, spazmolityczne, Roślin Leczniczych Wydziału Farmaceutycznego przeciwrobacze, przeciwdrobnoustrojowe, hamujące Akademii Medycznej im. Prof. Feliksa Skubiszewskie- rozwój niektórych nowotworów, a także obniżające po- go, Lublin (in Polish). ziom lipidów we krwi oraz hamujące procesy glikacji Yu k u n R . , 1994. A study on the anatomy and environment w tkankach. W fitoterapii stosuje się liście, pędy lub/i of leaves of Plantago lessingii Pisch et wey. Jour- nasiona różnych gatunków babki. nal of Ningxia Agricultural College. CNKI: SUN: Liście i nasiona Plantago znajdują także za- LXLX.O.1994-04-007 (in Chinese). stosowanie do wyrobu kremów, lotionów i maseczek. www.eFloras.org Różne części tych roślin (świeży surowiec, ekstrakty lub wyizolowane substancje) wykorzystywane są rów- nież w żywieniu ludzi i zwierząt. Liście babki można Właściwości użytkowe roślin spożywać jak sałatę, smażyć w cieście, przyrządzać z rodzaju Plantago z nich herbatę, sok czy wino. Nasiona dodawane są do ciastek, chleba, płatków śniadaniowych, lodów, napo- Streszczenie jów lub gotowane są jak kasza. Zwierzęta karmione babką mogą żyć dłużej i są zdrowsze, zaś mięso z nich Wielowiekowe doświadczenia medycyny ludo- pochodzące jest smaczniejsze i zdrowsze dla ludzi. wej, tradycje żywieniowe oraz wyniki licznych badań Nasiona Plantago są chętnie zjadane przez ptaki utrzy- naukowych wskazują, że rośliny z rodzaju Plantago mywane w klatach. mogą być wykorzystywane w celach leczniczych, ko- Natomiast pyłek babki ma właściwości alergi- smetycznych, dietetycznych oraz rytualnych. zujące. Produkowany w dużych ilościach (do 20 tys. W składzie fitochemicznym Plantago występu- ziaren pyłku/1 pręcik P. lancolata) może wywoływać je bogactwo substancji biologicznie czynnych (m. in., alergie u osób wrażliwych. Z uwagi na długi okres glikozydy, flawonoidy, polisacharydy i witaminy) o ko- rzystnym działaniu, przy jednoczesnej niewielkiej za- kwitnienia roślin z rodzaju Plantago, działanie czyn- wartości związków o właściwościach toksycznych. nika alergizującego utrzymuje się przez wiele tygodni. Badania naukowe potwierdziły, że rośliny te mają wła- W Polsce dni z maksymalną koncentracją ziaren pyłku ściwości antyoksydacyjne, hamujące apoptozę, osłania- babki w powietrzu najczęściej występują w lipcu.