Diseases and pests of clematis from the collection of the Botanical Garden-Institute of VSUT (Yoshkar-Ola)

Golomidova Tatyana Mikhailovna Graduate student, Department of Landscape Gardening, Botany and Dendrology, Volga State University of Technology 424000, Russia, Republic of Mari El, Yoshkar-Ola, Lenin Square, 3, room 245 tanygolomidova@gmail.com Mukhametova Svetlana Valeryevna ORCID: 0000-0001-7892-6450 PhD in Agriculture Associate Professor at the Department of Garden and Park Design, Botany and Dendrology of Volga State University of Technology 424000, Russia, Mari El Republic, Yoshkar-Ola, Lenin Square, 3, aud. 245 MuhametovaSV@volgatech.net Other publications by this author     Kurnenkova Irina Pavlovna PhD in Agriculture Associate Professor, Department of Ecology, Soil Science and Nature Management, Volga State University of Technology 424000, Russia, Mari El Republic, Yoshkar-Ola, Lenin Square, 3, aud. 302 KurninkovaIP@volgatech.net

Sukhareva Lyudmila Vitalievna Head of the Department of Woody Plants Introduction and Acclimatization of Botanical Garden-Institute, Volga State University of Technology Mari El Republic, Yoshkar-Ola, Mira street, 2 "B" SuharevaLV@volgatech.net Other publications by this author

Introduction. Clematis (Clematis L.) from the Buttercup family (Ranunculaceae Juss.) is a highly decorative perennial flower crop. Due to their abundant and long-lasting flowering, a wide variety of colors and flower shapes, life forms, they belong to the leading cultures of the world's industrial floriculture ^[1].  In natural conditions, clematis are cosmopolitan – they are common on almost all continents of the Earth, excluding Antarctica, but most of them are in Eurasia, up to 200 species ^[2].

Vertical gardening is one of the most popular and promising areas of landscape design. A rather meager range of ornamental climbing plants is used in the landscaping of public places in the settlements of Central Russia, so clematis can become an actual crop for widespread use in vertical gardening ^[3]. Despite its high decorative value, clematis are not widespread in many regions of our country, with the exception of the Crimea, Volgograd Region, Bashkiria, the Urals, and the Far East, where active research is being carried out on the introduction of species and varieties of this genus. The reason is the complexity of growing clematis plants and insufficient study of most varieties that are bred in a mild humid climate. When grown in a more continental and arid climate, plants suffer from overheating of the soil and dry air: their leaves burn, shoots dry up, flowers become smaller and burn out strongly, and the flowering time is shortened ^[4]. Such abiotic factors, along with biotic ones, contribute to the development of phyto-diseases. Therefore, one of the important problems in growing clematis is their damage by diseases and pests, which reduces the decorative effect of plants. The pathogenic microflora of clematis includes more than 30 pathogens of fungal and bacterial diseases common in Europe, North America and Southeast Asia. The most common diseases in our country are powdery mildew, rust, brown spot, gray rot, fusarium, septoria, ascochitosis, cylindrosporosis, alternariasis, phomopsis ^{[5, 6]}. It is worth noting that small-flowered clematis species are more resistant to diseases and pests compared to large-flowered varieties ^{[7, 8]}.

The purpose of this study is to review the diseases and pests characteristic of the genus Clematis and to identify them on clematis from the collection of the Botanical Garden of the Institute of the Volga State Technological University (Yoshkar–Ola, Republic of Mari El).

The research methodology included searching for descriptions of diseases in literary and Internet sources, as well as visual inspection of collection plants for signs of damage. The study was conducted in 2022.

Diseases. All types and varieties of clematis are susceptible to diseases caused by phytopathogenic fungi. The most dangerous disease is wilting. The disease manifests itself during budding and flowering in the sudden withering of one or more shoots of an apparently perfectly healthy plant. The damaged shoot turns black and shrinks. The disease occurs unexpectedly, proceeds quickly (within 1-2 days). It is impossible to take any urgent measures. The disease is caused by soil fungi of the genera Phomopsis, Fusarium, Verticillium ^{[9, 5]}. Fungi, as a rule, affect the base of the stem. The hyphae of the fungus penetrate into the tissue of the plant, and, growing, the mycelium clogs the vascular-fibrous bundles. Water access stops, which leads to rapid drying of leaves and flowers. The disease occurs unexpectedly and proceeds rapidly, so the only reliable way of protection is preventive methods of destroying pathogens. At the earliest stages of plant development, various fungicides are used ^{[9, 10]}.

Wilt or verticillous wilt in a narrow sense is caused by fungi of the genus Verticillium, but often it means any wilt of clematis lashes caused by one of the above fungi. Shoots lose turgor, wither, turn black and wither (Figure 1). This process can last from several hours to several weeks ^[11].

Figure 1 – Wilt of clematis ^[11]

Fusarium is caused by pathogenic fungi of the genus Fusarium. The disease is common in more northern, i.e. wetter, areas. It occurs mainly at the base of shoots and on the roots of annual cuttings in the form of a pale pink-tinged plaque ^[5]. The bark in the lower part of the stem turns black, the affected parts look swollen. After a while, the growing mycelium of the fungus clogs the vessels, which leads to rapid withering and death of the shoot (Figure 2). This happens more often in the summer months ^[12].

Figure 2 – Fusarium ^[11]

Phomopsis is caused by pathogenic fungi of the genus Phomopsis. The disease manifests itself in the spring after the formation of a significant amount of green mass, when there is still little heat and a lot of moisture. Initially, yellow-brown spots appear on the lower leaves, their size gradually increases, the leaf darkens completely and withers (Figure 3). The bases of the shoots are affected in the form of strips of dark dots ^[12].

Figure 3 – Phomopsis ^[12]

Ascochytosis is caused by pathogenic fungi of the genus Ascochyta (A. dolomitica, A. clematidina, A. vitalbicola are most common). At the base of the shoots and on the leaves, brown to black spots of irregular shape with a clear contour appear. The affected area of the tissue dies and falls out, a hole remains in place of the spot (Figure 4). The disease manifests itself in the second half of summer ^{[5, 13]}.

Figure 4 – Ascochitosis ^[13]

Cylindrosporiosis is caused by pathogenic fungi of the genus Cylindrosporium. Oblong ochre-yellow or brown spots appear on the leaves, usually between the veins. At first it may seem that the leaves are simply burnt out in the sun, this makes it difficult to detect infection early. The spots have an oblong shape, are surrounded by a brown border and are limited by leaf veins. Over time, the affected tissue cracks and falls out, brown dry spots and holes appear (Figure 5). The shoots are deformed, the bush itself slows down in growth. At high humidity, the spots are covered with a white coating. The source of infection is plant residues ^[5].

Figure 5 – Cylindrosporiosis ^[11]

Brown spotting is caused by pathogenic fungi of the genus Cladosporium. It sometimes occurs in the form of a dark plaque on the leaves and shoots of clematis in places affected by other fungi ^[5].

Alternariasis is caused by pathogenic fungi of the genus Alternaria. It appears on the tips of the leaves in the form of large blurry brown-black spots (Figure 6). Over time, the spots grow, and the leaves dry up prematurely. At high humidity, a dense olive-black mycelium forms on them, the spores of which are the distributors of infection and quickly infect the leaves around. Affected plants overwinter poorly ^[14].

Figure 6 – Alternariosis ^[11]

Septoria is caused by fungi from the genus Septoria. Affects many types of clematis, causing brown leaf spotting (Figure 7). Light, rounded, purple-bordered spots form on the leaves, which eventually fall out. The disease progresses in conditions of high humidity at a temperature of 20-25 ° C ^[5]. Thus, for Septoria clematis-flammulae, the most optimal environmental conditions are 25 °C and 100% relative humidity ^[15].

Figure 7 – Septoria ^[16]

Gray rot is caused by pathogenic fungi of the genus Botrytis. It is expressed in the appearance of a velvety plaque on the leaves and flowers, brown spots are surrounded by a gray fluffy rim (Figure 8). It manifests itself in cold, rainy summers or with excessive watering, as well as with thickening of plantings and an overabundance of nitrogen in the soil ^[16].

Figure 8 – Gray rot ^[16]

Rust is caused by the pathogenic fungus Aecidium clematidis DC. It affects leaves, shoots and peduncles, on which reddish-yellow or bright orange loose spots are formed, later covered with a powdery orange mass consisting of eciospores (Figure 9). The shoots deform, the leaves turn brown and curl, shrink and fall off ^[5].

Figure 9 – Rust ^[12]

Powdery mildew affects all aboveground parts of clematis (shoots, leaves, flowers and seeds). At first they are covered with a white powdery coating (Figure 10), then the plaque darkens a little, and dark dots of the fruit bodies of mushrooms appear on it. The tissues under the coating darken and eventually die off. With strong development, powdery mildew inhibits the growth of clematis, they stop developing and stop blooming. Powdery mildew on clematis is most often observed in the hot season – mainly in July and August ^[17]. The greatest danger of the disease is in the southern regions, where in the middle of summer, with hot weather with sufficient humidity, it develops most intensively ^[18]. Most clematis in the middle belt and more northern regions, for example, in the Moscow and Leningrad regions, are usually damaged much less or are not affected at all ^{[5, 18]}. In Western and especially Southern Europe, powdery mildew is much more common and is considered quite dangerous. Pathogens of powdery mildew of clematis are pathogenic fungi Leveillula ranunculacearum f. clematidis, Erysiphe communis f. clematidis, Erysiphe aquilegiae, Erysiphe polygoni ^[17].

Figure 10 – Powdery mildew ^[17]

Yellow mosaic is a viral disease of clematis, manifested by the mosaic color of the leaves, on which light yellow spots, stripes and streaks appear (Figure 11). In the future, the same signs appear on flowers that look colorful and decorative, which is why many gardeners consider this effect a varietal feature. The plant itself does not wither and seems healthy. The disease progresses slowly, the plant does not die. But gradually the vine is depleted, loses its varietal qualities and becomes unsuitable for reproduction. There is no treatment for yellow mosaic, as well as other viral diseases of plants. Clematis infected with the virus should be uprooted and burned. Prevention consists in the fight against insects (aphids, ticks, worms), which are carriers of the virus. In addition, it is necessary to try to plant clematis away from such herbaceous perennials subject to yellow mosaic as phlox, tulips, delphiniums ^[12].

Figure 11 – Yellow mosaic ^[12]

Pests. There are more than 25 species of pests that parasitize various types and varieties of clematis. The gall nematode (Meloidogyne marioni) parasitizes on the roots. Its presence is manifested in the fact that thickenings (galls) of various sizes are formed on the roots (Figure 12). There are also leaf nematodes that affect the aboveground part of clematis. Such plants lag behind in growth, stop blooming ^[5].

Figure 12 – Gallic nematode ^[16]

The bases of the shoots of clematis are often damaged by mealybug (Pseudococcus adonidum), whose body is covered with white filamentous waxy secretions (Figure 13). The pest lives mainly in greenhouses and greenhouses, as well as in the south in the open ground ^[5].

Figure 13 – Mealybug ^[11]

Often, clematis are damaged by such pests as mining fly, leaf weevil, cruciferous flea, earwigs, scabies, mites, bears, slugs, aphids, etc. (figure 14). In winter, clematis shoots can be damaged by mice, rats and hares. If the plants are covered with lapnik for the winter, then it protects the bases of the shoots from rodents. Many gardeners often use poisoned baits against them, as well as from bears, but at the same time it is required to strictly observe all precautions so as not to cause the death of useful animals. If proper agricultural techniques are followed, the harmful effect of fungal and other diseases can be minimized ^[5].

Figure 14 – Pests of clematis: a) aphid Aphidoidea; b) spider mite Tetranychus urticae; c) green bug Palomena prasina; d) caterpillar sem. Spadenidae Geometridae ^[16]

In addition to insect pests, clematis are visited by insects that feed on nectar and pollen of flowers.  So, in the Moscow region, 27 species of insects belonging to 13 families and 3 orders were collected on the plants of K. Virginsky. Regardless of the type of food, the vast majority of insect species, including such well-known bloodsuckers as the autumn zhigalka Stomoxys calcitrans and midges, as well as predators of the genus Scatophaga use plant pollen as a food source. In addition, feeding of some insect pollinators of the most important fruit crops was noted on clematis: apple, pear, rowan, aronia, viburnum (Halictus albipes, Bellardia pusilla, species of the Syrphidae family) ^[19]. In the conditions of the Ufa Botanical Garden, 12 clematis species were visited by bees, bumblebees, wasps, ants, various flies and beetles attracted by plant pollen ^[20].

Table 1 provides information on the prevention and control of major diseases and pests.

Table 1 – Popular chemical and biological fungicides for the treatment of clematis (according to ^[12])

Table 2 shows signs of weakening of non-infectious clematis.

Table 2 – Signs of weakening of non-infectious clematis (based on ^[21])

In the Botanical Garden-Institute of PSTU, clematis grow on a section of lianas that is part of the "Fruticetum" exposition. Metal supports with a height of 1.5–3 m are equipped with a plastic mesh with a cell size of 4 ? 4 cm. The genus Clematis is represented in the collection by 7 species and 44 varieties ^[22]. Agrotechnical measures include weeding and loosening of plants, in hot weather, abundant watering is performed. Fertilizing of clematis with fertilizers is carried out 4 times a season: in spring, in summer before flowering, in late summer and in autumn. In the spring, fertilizers with a predominance of nitrogen are applied, before budding – a complex mineral fertilizer. At the end of summer, phosphorus-potassium fertilizers are used, ash is used before winter shelter. Every year in November, the plants are sheltered for the winter with spruce spruce branches.

For diseases in the exposition, treatments are carried out twice a season (in spring in April-May and in autumn at the end of September) with Bordeaux liquid or copper sulfate, as well as with a solution of the drugs "Gamair" and "Alirin". Some varietal clematis have small leaves, the cause of which has not yet been clarified. Presumably, it is associated with a large age of plants or the presence of nematodes ^[22].

Inspection of collectible clematis showed that most of them have signs of spotting (Figure 15). The fight against them consists in spraying plants with a solution of the drug "Fundazol".

Figure 15 – Clematis spotting

Also, a wilt was detected on the site, which affects the leaves and vines of plants older than 20 years. Wilt was found in about 1/3 of the plants in the collection (Figure 16). When a wilt is detected, the affected shoots are cut out, followed by a mixture of ash and sand in a ratio of 1:1 under the root neck.

 Figure 16 – Wilt of clematis

Mechanical damage from hail, rain, as well as damage by mice and leaf-eating insects were detected in a small amount (Figure 17).

Figure 17 – Mechanical damage: a) the plant completely, b) the flower

The presence of diseases in clematis plants is noted in the works of many researchers in various countries and regions. So, in the south of Western Siberia, at the Lisavenko Research Institute of Horticulture of Siberia (Barnaul), it was found that hot dry summers with additional watering were easier to tolerate clematis than cool rainy ones. Excess moisture in the second half of summer contributes to the development of the disease, which causes the complete death of shoots on large-flowered varieties. The authors provide a list of varieties with no signs of wilting ^[4].

In the Stavropol Botanical Garden (Stavropol), according to the results of an immunological assessment of the collection species and forms of clematis, their sufficiently high resistance to diseases and pests was revealed, with rare exceptions. Thus, in some years, C. integrifolia and C. recta f. atropurpurea had moderate damage to powdery mildew (Erysiphaceae) during budding and flowering, which significantly affected the condition of plants and their decorativeness ^[7].

In the conditions of the Belgorod region, it was revealed that the most common diseases of clematis were gray rot and alternariasis. In addition to it, there are 5 more types of diseases expressed in leaf spotting: tracheomycosis, gray rot, ascochytosis, fomosis, phylostictosis. These diseases were especially strongly detected on the leaves of the lower tier and less pronounced on the leaves of the middle tier. The leaves in the upper tier were mostly damaged by alternariosis. Tracheomycosis causes particular damage to plants, which has a detrimental effect on the entire plant ^[6].

In the Main Botanical Garden named after N. V. Tsitsin of the Russian Academy of Sciences (Moscow), the powdery mildew pathogen Erysiphe aquilegiae var. ranunculi, affecting clematis, was identified, but in general, the collection's incidence is low. Infection of 13 of the 60 examined clematis varieties was confirmed visually and by cryoSEM. In most varieties of the collection, the defeat of the powdery mildew pathogen was noted on the upper side of the leaf, but in some varieties mycelium was also found on the stems. The most susceptible and pathogen-resistant varieties of the collection have been identified ^[18].

In Jeonju (Korea), in a public park, symptoms of rust disease were found in 80% of Clematis patens plants, the severity of the disease in each affected plant varied from 60 to 90%. Symptoms were manifested in the form of light green chlorotic spots, limited by veins, on the upper surface of infected leaves, and yellow or orange rust pustules formed on the corresponding lower surface of the leaves ^[23].

In the Czech Republic, it has been established that spotting and wilting of clematis leaves is a serious disease in Czech nurseries. Clematis were found with symptoms of a fungal disease caused by Calophoma clematidina. On infected plants, irregular brown-black spots appeared on the leaves, which later turned into large necrosis, usually leading to wilting. The pathogen was present in the leaves, stems and roots of plants ^[24].

In Australia, when growing Clematis pubescens plants for the restoration of mine lands, a high degree of their damage by the wound pathogen Phoma clematidina was revealed. After transplanting plants, an outbreak of leaf spotting and wilting was noted, which the authors attribute to pruning, which increased the risk of infection of plants through damaged tissues ^[25].

Conclusion. Clematis are one of the most decorative plants used in vertical gardening. But the manifestation of their maximum decorative effect is associated with the growing conditions, including phytobeases, to which they are often susceptible. Among the diseases, wilt is especially dangerous, which leads to a sharp and rapid withering of plants. In the Botanical Garden-Institute of PSTU (Yoshkar-Ola), damage to the collection plants was also found by wilt, as well as spotting. Preventive plant treatments are carried out to combat diseases. The obtained data can be used in the practice of growing clematis at the landscaping facilities of settlements in the region.