SEVERE INFECTION OF FIGS BY FIG RUST PATHOGEN

In late summer and early fall of 2014, both in productive plantations and in nurseries in Montenegro, an important disease of figs was recorded. The leaves of diseased trees became twisted upwards with rusty and necrotic areas and then dried. Numerous yellow to brown coloured spots on the upper side and reddish-brown pustules on the lower side of the leaves were noticed. Almost all leaves with those symptoms prematurely fell down, leaving bare branches and unripe fruits. Microscopic observations in laboratory revealed that the disease is caused by the phytopathogenic fungus Cerotelium fici . The disease is favoured by humid and warm summer conditions as it was in 2014.


INTRODUCTION
) originates from Near East and now is mostly grown in Mediterranean region. Turkey is the largest world producer of figs (30% of overall world production) followed by Egypt, Morocco, Spain, Greece, USA, Italy, Algeria, Syria etc. (Cizmovic et al., 2005).
Fig has been traditionally grown in the southern and central part of Montenegro for a long time. After Second World War in the southern parts of Montenegro, according to number of trees, fig was on the second place after olive. Since then, due to expansion of citrus and actinidia, its economic importance gradually decreased (Mijuskovic, 1999). Based on data from 1999, there were 225.390 yielding trees, with total year production of 2.434 t and average yield of 10.7 kg/capita in Montenegro (Cizmovic et al., 2005). Until recently, in Montenegro fig was not grown on large areas, mainly near houses and in gardens, so the intensity of certain diseases was not of extreme importance. However, in recent years fig plantations were set up (from several hundreds to over 1000 trees), and several diseases have been observed whose intensity threatens the cultivation of this crop and jeopardize the yield.
In 2014 economically significant fig disease was recorded in Montenegro. Based on symptoms manifestation and microscopic observations in the laboratory it was revealed that the disease is fig rust caused by the phytopathogenic fungus Cerotelium fici (E.J. Butler) Arthur. The disease is favored by humid and warm summer conditions as it was in 2014.
Fig rust was already recorded a few times in last century in Montenegro (Mijuskovic, 1963).

MATERIAL AND METHODS
Several fig orchards and nurseries in Montenegro were visited during summer and fall of 2014. Since a lot of prematurely fallen leaves were noticed on the ground, we observed the trees and collected the diseased leaves. Samples were placed in plastic bags and transported to laboratory of phytopathology at the Biotechnical Faculty in Podgorica. After symptoms' observation and description, microscopic analysis of noticed pustules on leaves has been done using conventional techniques in order to reveal morphological features of the pathogen.
A hundred of the found spores were measured and observed in order to define their shape, color and dimensions. Their photos were made as well. For this purpose, Axioskop 2 plus Zeiss and AxioCam ERc5s Zeiss were used.

RESULTS AND DISCUSSION
During field trips to fig orchards and nurseries in Montenegro in 2014, a severe dropping of leaves from fig trees were noticed in late summer and early fall. Symptoms have manifested on the upper leaf surface as small yellowish spots at the beginning. As the disease progress they turn a reddish-brown color and become angular. However, upper surface of the leaves remains smooth (Fig.  1). Opposite of these spots, on the lower leaf surface a lot of dirty-orange, rusty to reddish-brown raised pustules were visible (Fig. 2). Angular spots often merge and form necrotic areas usually near the edges that make leaf curling upwards (Fig 3). This curling of leaves cause the reduction of assimilative surface required for optimal photosynthetic activity thus influencing on yield. In some cases it looked like the tree get burned (Fig. 4). Almost all leaves with those symptoms prematurely fell down, leaving bare branches and unripe fruits.  Microscopic analysis revealed that the pustules on the lower leaf surface were actually uredinia that contain abundance of urediniospores. Urediniospores (Fig. 6) usually have wide-ellipsoid to polygonal or rounded shape. Interior of the spores is granulated and yellowish to faintly orange, framed with the thick, light brown, denticulate membrane. Size of uredioniospores varies 19.6 -31.9 × 14.7 -24.5 μm (average 24.5 × 20.0 μm). This description corresponds to those given by Mijuskovic (1963) and McKenzie (1986). According to Huseyin & Selcuk (2004), spermogonia and aecia are unknown, while, besides uredinia and urediniospores, telia appear as well on lower leaf surface (recorded on leaves of Ficus carica in Turkey). Telia are very small, whitish and scattered with teliospores in chains of 2-7 spores, angular-spherical or broadly-ellipsoid, 19-22 x 10-17 μm; spore wall is 1-1,5 μm thick, hyaline and smooth.  (Ficus carica L.). Rust on Ficus elastica has been discovered for the first time in 1961 in France and the disease was attributed to Cerotelium fici (Grouet, 1962). In Montenegro Cerotelium fici was recorded on ornamental nursery plants of Ficus elastica Roxb. in greenhouses during 2004and 2005(Vucinic et al., 2006. Other host plants from the family Moraceae are also susceptible to C. fici such as plants from genera Maclura, Morus and Broussonetia papyrifera (paper mulberry) (McKenzie, 2013).
Fig rust is widespread in tropical and subtropical areas throughout the world. It has been recorded in the southeastern U.S., in Bermuda, West Indies, Central America, Oceania etc. (Verga & Nelson, 2014;McKenzie, 2013). The disease has been known in Australia since 1904 while it has been recorded in New Zealand on Ficus carica in 1986 (McKenzie, 1986). It is also present in Turkey (Huseyin & Selcuk, 2004) and India (Desai, 1998). According to Mijuskovic (1963), fig rust usually doesn't cause significant damages in Mediterranean, but its appearance isn't rare however even in countries with arid climate, such as Tunis, Morocco, Israel, Italy, south France, Mediterranean islands etc.
In The rust spores can be spread by wind and rain drops to other plants. Introduction of the disease in New Zealand has been related to its spread by windborne urediniospores from Australia (McKenzie, 1986). According to McKenzie (2013), when rust spores land on the surface of leaves they require at least 14 hours of continuous wetness to germinate. Several days after germination of spores and penetration of the fungus into leaf, small yellowish spots appear on the upper leaf surface as the first symptoms of the disease. When the vegetation ends, rust spores on fallen leaves overwinter and serve as a source of inoculum for the next season (Verga & Nelson, 2014).
The disease can cause significant damages in areas with rainy summer conditions. It develops usually late in the summer when the infected trees can defoliate in a few weeks due to the disease fast spreading and short incubation period. Sometimes fig rust can appear early in the summer when it can be especially destructive since premature defoliation induce new growth on trees. This new growth can beat out the plant and cause that it come into winter unprepared and susceptible to low temperatures (Mijuskovic, 1963;Ferrin & Overstreet, 2010).
Control measures against fig rust should integrate cultural practices and, if required, chemical control. Cultural practices foresee gathering and destroying of infected leaves together with such a pruning of shoots that allows airflow through the canopy and drying the foliage. It is recommended to avoid sprinkler irrigation that wets the leaves. Irrigation water should be applied at the ground level directly to the soil in the morning (to avoid humidity and leaf wetness during the night). Weed control must be regularly done to reduce relative humidity in fig orchard. If defoliation appears, the trees should be additionally fertilized to stimulate new leaves as soon as possible. These measures are recommended by Verga & Nelson (2014) and Ferrin & Overstreet (2010) and can be recommended to fig growers in Montenegro. Fungicidal control usually is not necessary, especially in Montenegro where rainy summers are exceptional. However, if the disease is present every year, chemical control needs to be applied. Treatment with protective fungicide must be done before the disease appears. Bordeaux mixture, sulphur, zineb or maneb can be used (McKenzie, 1986). Results obtained by Desai (1998) in Karnataka, India showed that, among five applied fungicides, mancozeb (0.2%) was the most effective in controlling fig rust, but also the other fungicides such as tridemorph, wettable sulphur and chlorothalonil.