The development of Erysiphe alphitoides and E. hypophylla in the urban environment EWA SUCHARZEWSKA Department of Mycology, University of Warmia and Mazury in Olsztyn Oczapowskiego 1A, PL-10-719 Olsztyn-Kortowo, ewko@uwm.edu.pl Sucharzewska E.: The development of Erysiphe alphitoides and E. hypophylla in the urban environment. Acta Mycol. 44 (1): 109–123, 2009. Differentiated responses of Erysiphe alphitoides and E. hypophylla in urban conditions are described. The influence of transport pollution on the morphology of the mycelium, chasmotecium development and individual stages of the developmental cycle is discussed. Key words: Erysiphales, developmental cycle, transport pollution, Olsztyn INTRODUCTION Erysiphe alphitoides Griff et Maubl. and E. hypophylla Nevod. are common obligate parasites of the order Erysiphales. They infect representatives of the genera Quercus and Fagus as well as sporadically Aesculus and Castanea. Paeonia lutea has been identified as a new host of Erysiphe hypophylla (Takamatsu et al. 2006). The two phytopathogens are widespread in entire Europe, Asia, America, Australia and New Zealand. The occurrence of Erysiphe alphitoides has been documented in Poland since 1909, initially in the conidial stage only (Oidium quercinum Thüm). The sexual stage of E. alphitoides was first observed in France in 1911 and recorded in Poland in 1922 (Braun 1995; Sałata 1985). It has since been recorded in the teleomorphic stage as Microsphaera alphitoides very often (Adamska et al. 1999; Czerniawska 2001; Dynowska et al. 1999; Kalinowska‑Kucharska, Kadłubowska 1993; Kućmierz 1967, 1971, 1973; Majewski 1970, 1971; Mułenko 1981, 1988; Mułenko, Wojdyło 2002; Ruszkiewicz‑Michalska 2006; Sałata et al. 1993). Erysiphe alphitoides is a dangerous oak pathogen. It attacks trees of various age classes causing a reduction in annual growth (Minkievič et al. 1993). ACTA MYCOLOGICA Vol. 44 (1): 109–123 2009 110 E. Sucharzewska Erysiphe hypophylla was first observed in Poland in 1952 (Sałata 1985). It has been recorded sporadically in different parts of Poland (Dynowska et al. 1999; Ma‑ jewski 1971; Mułenko 1988; Sałata, Majewski 1976). In contrast to Erysiphe alphitoides, the systematic position of E. hypophylla was not clear until recently (Braun, Takamatsu 2000). The species was considered by many mycologists to be a synonym of Erysiphe alphitoides (Microsphaera alphitoides) based on biometric studies. Braun et al. (2003) finally distinguished two separate species using molecular studies: Erysiphe alphitoides and Erysiphe hypophylla. The two fungi, mostly Erysiphe alphitoides and less frequently E. hypophylla, has been reported in studies investigating their presence in floristically or phytosocio‑ logically interesting communities and ecosystems characterised by a low level of an‑ thropopressure. As they were often inventories or phytopathological examinations, these studies usually provided systematic and geographical analyses of species rich‑ ness or an assessment of taxonomic differentiation in relation to plant associations in a given area (Adamska et al. 1999; Czerniawska 2001; Majewski 1971; Mułenko 1996, 1998; Kućmierz 1971, 1973). However, the ecology Erysiphe alphitoides and E. hypophylla and their life strategies in environments exposed to strong anthropopres‑ sure have been discussed in few studies. The aim of this study was to analyse the occurrence of Erysiphe alphitoides and E. hypophylla and to examine basic life reactions of the parasites in urban conditions. MATERIAL AND METHODS Examinations (2000‑2002) were conducted in the city of Olsztyn and its vicinity at 63 sites (17 sites with young plants and 46 sites with mature Quercus robur L. plants) situated at a range of distances from main transport routes: up to 50 m, up to 100 m, up to 300 m and >300 m. Distances were selected using studies by Lorenc‑Plucińska and Byczyńska (1997) which show that the greatest value of exhaust gas concentra‑ tion is recorded at a distance of 30‑50 m away from the road and is at a constant level of 30%. The exhaust gas level drops to 10% at 200 m away from transport routes. Sites located >300 m were used as controls. Material was obtained from the middle of the vegetative period when first chas‑ mothecia began to occur on the powdery mycelium. One sample was defined as a total of 25 leaves collected randomly from each host plant. The infection rate of host plants, mycelium development and morphology as well as chasmothecium development were examined in the macro‑ and microscopic analysis of the material. 1. The disease rating was calculated for each sample on a 5°‑scale using McKin‑ ney’s formula. It shows the degree of infection of host plants and is a criterion of pathogen sensitivity (Dynowska 1993, 1994) to changes in the optimum environment conditions: Σ (a x b) x 100% R = -------------------- N x 4 Erysiphe alphitoides and E. hypophylla 111 R – disease coefficient in percent (index); Σ (a x b) x 100% – the sum of the products obtained by multiplying the number of plant organs (a) by the degree of infection (b); N – total number of plants (alternatively leaves, fruits) examined in the study; 4 – the highest degree of infection in a five‑grade scale (0 – no infection; 1 – up to 10%; 2‑11 – 25%; 3‑26 – 50%; 4‑51 – 100%). The final value R used in the results analysis was calculated based on the arithmetic mean for each fungal species on a specific host plant = mean degree of infection. 2. The developmental stage of the parasite was identified: asexual stage, sexual stage. 3. The number of chasmothecia, both mature and immature, per 1 cm2 of the sur‑ face of each infected leaf was established. Ten randomly collected morphologically mature chasmothecia were selected and analysed under a microscope. The following were assessed: a) developmental degree of appendages in a three‑grade scale: 0 – chasmothecia without appendages, I – chasmothecia with appendages not fully developed, II – chasmothecia with fully developed appendages; b) maturity of chasmothecia in a three‑grade scale: 0 – chasmothecia without asci and spores; I – chasmothecia with asci without formed ascospores; II – chasmothecia with asci containing spores; c) morphological variability of chasmothecia, the size and diameter of chasmoth‑ ecia, appendages. The number of chasmothecia discussed in the results was calculated based on the arithmetic mean for each fugal species. Fungi were determined using keys by Braun (1987, 1995) and Sałata (1985). Spe‑ cies were identified using morphological traits of chasmothecia (size and diameter, number of appendages, appendages branching). The nomenclature was accepted after Braun and Takamatsu (2000) and Braun et al. (2003). Host plants were determined using studies by Szafer et al. (1988) and Rutkowski (1998). Statistical calculations were conducted using the data analysis software system STATISTICA (StatSoft, Inc.) version 6 (2003) by variance analysis. Significant differ‑ ences among the means were declared at a significance level of p=0.05. The means were then classified in homogenous groups for selected factors using Duncan’s test. Letter symbols (a, b, c…) were used and values to which the same letters were as‑ signed do not differ significantly at p=0.05. RESULTS Erysiphe alphitoides and E. hypophylla were observed on both mature and young Quercus robur plants in all the years of the study period: at 40 sites in 2000 (63%), at 47 sites in 2001 (75%) and at 48 sites in 2002 (77%) (Fig.1). The analysis of the degree of infection of the host plant in relation to the distance from transport routes shows noticeable, statistically significant differences. The high‑ est mean disease index was recorded at sites located up to 100 m and 50 m (52% and 112 E. Sucharzewska 44%, respectively). The lowest mean infection was observed at sites located up to 300 m and >300 m, which is confirmed by the statistical analysis (Fig. 2). The two parasites either occurred separately or co‑occurred on the same plant and even on the same leaf. The upper leaf surface was usually colonised by E. al- phitoides and the lower leaf surface by E. hypophylla. Chasmothecia of E. alphitoides were recorded beside chasmothecia of E. hypophylla on the lower leaf surface in a few cases. A relatively high participation of the species’ co‑occurrence on the same leaves was recorded in each study year. Changes in the prevalence of the two fungi were also observed. E. alphitoides increased its occurrence at the distances examined in the study year by year. The highest participation of the species was recorded at sites located up to 50 m. E. hypophylla occurred more frequently at sites located up to 300m and >300m (Fig. 4). Two developmental stages of E. alphitoides and E. hypophylla were observed throughout the study period: the asexual stage when conidial spores occurred and the sexual stage when chasmothecia were produced. Samples containing the perfect stage of the two fungi constituted the highest percentage regardless of the distance (>70%). Fig. 1. Percentage participation of E. alphitoides and E. hypophylla in samples on Q. robur. Fig. 2. Mean degree of infection of Q. robur by E. alphitoides and E. hy- pophylla in relation to the distance from transport routes in the study period (letters a and b indicate sta‑ tistically significantly different val‑ ues at p=0.05). Fig. 3. Mean number of E. alphi- toides chasmothecia per 1cm2 of leaf surface throughout the study period. 118 E. Sucharzewska E. alphitoides in areas strongly influenced by pollution has also been observed by Boczoń (1998) and Domański et al. (1987). Divergent results of research into the occurrence of E. alphitoides is explained by Domański (1976). He attributes epiphy‑ toses to a specific system of ecological factors that favourably influence the devel‑ opment as well as aggressiveness and pathogenecity of the disease agent. A set of factors co‑interacting in different combinations most probably occurred in each of the above cases and may have influenced divergent study results. This was shown in a study by Grzebyta et al. (2005), who analysed the influence of high temperature and fluoride on the development of E. alphitodes on Q. robur: higher infection of leaves in oaks growing in an area containing fluoride than in a clean area was recorded in previous observations. This indicated a low sensitivity of the pathogen to pollution with fluoride compounds. More detailed examinations, however, showed that fluo‑ ride which acted synergistically with high temperature caused the opposite effect and led to low infection of leaves. Erysiphe hypophylla, which mostly colonised the lower leaf surface similarly to E. alphitoides, developed in all the distance zones. Its strongest development was observed at sites up to 300 m and at control sites. Interestingly, the species co‑oc‑ curred on the same leaves and the percentage of the occurrence of this type was high in the distance zones in the three study years. Information on the occurrence of biology of E. hypophylla is scarce in the available literature. It was recorded in the Białowieża National Park by Majewski (1971) and at a few localities in Poland by Sałata & Majewski (1976) and Dynowska et al. (1999). The species seems to be common and the present study shows that it often occurs along with E. alphitoides. However, the presence of the latter is recorded in many Polish studies (Adamska et al. 1999; Czerniawska 2001; Kalinowska‑Kucharska, Kadłubowska 1993; Mułenko, Wojdyło 2002). These studies are conducted mostly in environments similar to natu‑ ral ones where the degree of anthropogenecity is low. These results, however, cannot be used to define the occurrence of E. hypophylla in urbanised and natural areas. Di‑ vergent opinions on the separate position of the two parasites and their treatment as one species, Erysiphe (Microsphaera) alphitoides, may have also contributed to this. Weather conditions also influenced the development of the two species in the study period. Erysiphales can infect plants in a broad range of temperatures and humidity. Due to a considerable amount of water in the cell, spore germination in the majority of the representatives of the order takes places even in low relative air humidity. The highest degree of infection in all the species analysed in the study was observed in 2002 when the vegetative period was very warm and dry. July, Au‑ gust and September were hot while precipitation between May and September was lower than usual. Similar results were obtained by Durska (1974), who recorded an increased development of Erysiphales during a dry and hot summer. Parasites aim to close the developmental cycle in order to produce structures having the best possible resistance genes that condition the survival of a species. Therefore, a strategy aimed at increasing and improving reproduction is a char‑ acteristic trait of parasites. Organisms whose features are better adapted to their environments achieve a greater reproduction success. The sexual process may be disturbed in unfavourable conditions, such as pollution, which may result in the ab‑ sence of or a reduction in the number of ascomata or degeneration. This was ob‑ served in Lophodermium pinastrii by Grzywacz (1976) as well as by Kowalski and Erysiphe alphitoides and E. hypophylla 119 Budnik (1976). The parasite could not reach a full developmental cycle due to high concentrations of toxic compounds and altered chemism of infected needles, and did not produce ascomata. A full developmental cycle of the two powdery mildews that ended in the produc‑ tion of chasmothecia, also called cleistothecia, characteristic of this fungal group, was observed in the present study. Chasmothecia in the order Erysiphales are scle‑ rotia and their initiation occurs in unfavourable environmental conditions accord‑ ing to some researchers (Dynowska 1996a; Füzi 2001). Literature data show that the majority of powdery mildews enter the reproduction stage towards the end of the vegetative period, between August and November (Füzi 2001; Majewski 1971; Mmbaga 2002; Sałata 1985; Turnau, Czerwonka 1986). Present results corresponds with literature reports. Young chasmothecia in Erysiphe alphitoides and Erysiphe hy- pophylla were observed at most sites at the beginning of August. They began to ma‑ ture in the second half of August and mature chasmothecia were recorded in mid September. Similar results were obtained by Kadłubowska, Kalinowska‑Kucharska (1989) and Minkievič et al. (1993). However, the parasites did not always enter the generative stage. The fact that the Oidium form was recorded towards the end of the study periods suggests that the sexual stage is not obligatory in the species and the parasite also overwinters in the anamorphic form. Majewski (1971) also ob‑ served that not all powdery mildews enter the teleomorphic stage in his studies in the Białowieża National Park. Statistically significant differences in the number of chasmothecia between the zone influenced by automotive exhaust gases and the control zone were observed in Erysiphe alphitoides. Parasites formed chasmothecia more numerously at a distance up to 50 m away from transport routes and their smallest number was recorded >300 m. This may result from the differences in the degree of infection of the host plant. A similar opinion was expressed by Füzi (2001), who observed a strict correlation between the number of chasmothecia and the degree of infection: both variables were mutually dependent. Mmbaga (2002) disagrees and reports that neither the degree of infection of the host (leaves with a low infection degree often contained a high number of chasmothecia) nor the plant age influences the number of cha‑ smothecia. Significant disturbances in chasmothecium development at sites located by main transport routes were not observed in the two powdery mildews. It is interesting that differences in appendage development were observed be‑ tween the two mildews infecting Q. robur. A considerably greater number of chas‑ mothecia without appendages (0 developmental stage) and having appendages not fully developed (I developmental stage) were recorded in E. alphitoides. Chasmo‑ thecia having appendages in I and II developmental stage dominated in E. hypophylla. The lower leaf surface may have been more favourable for the development of chas‑ mothecia. This is reflected in the maturity of asci and spores. A high participation of chasmothecia without developed asci and spores was recorded in E. alphitoides while chasmothecia with asci containing spores constituted a considerably higher percentage in E. hypophylla. Untypical chasmothecia whose size was considerably smaller and which did not have developed asci and spores but had fully developed appendages and chasmothecia with untypical appendages were observed in Erysiphe alphitoides. These chasmoth‑ ecia were recorded in the zone up to 50 m in 2002. Empty chasmothecia have been 120 E. Sucharzewska described in Epichlöe typhina in athropogenic populations of Pucciniella distans and attributed to disturbances in the genetic control of the developmental cycle of E. typh- ina caused by an environmental factor (Falińska 2002). Degenerated chasmothecia of a considerably smaller size were observed in Lophodermium pinastrii in the zone of the strongest influence of pollution by Benben, Sierota (1976) and Grzywacz (1976). Empty chasmothecia as well as untypical appendages in polluted sites recorded in the present study may indicate developmental disturbances. However, such chasmoth‑ ecia constituted a very low percentage. Their occurrence may thus be caused natural disturbances resulting from the formation of a great number of chasmothecia or the influence of higher temperatures as suggested by Moore‑Landecker (1992). Ecological research into the parasites of the order Erysiphales conducted in the urban environment does not unambiguously show the influence of individual factors on the development of the fungi examined in this study. However, the two species have a broad ecological amplitude. This is connected with adaptation processes con‑ ditioned by genetic mechanisms that are activated at times of greater and more long‑ term amplitudes of environmental factors that are characteristic of urbinocenoses (Stearns 1992). 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Stanowiska w liczbie 63 zlokalizowane były wzdłuż głów‑ Erysiphe alphitoides and E. hypophylla 123 nych szlaków komunikacyjnych w odległościach do 50 m, do 100 m, do 300 m oraz >300 m (kontrolne). Materiał badawczy stanowiły losowo zebrane liście z rośliny żywicielskiej. We wszystkich latach badań E. alphitoides i E. hypophylla wystąpiły na Q. robur z dużym nasileniem. Odnotowano stosunkowo wysoki udział wspólnego występowania obydwu gatunków na tych samych liściach. Stwierdzono różnice w średnim stopniu porażenia rośliny żywicielskiej w zależności od odległości od szlaków komunikacyjnych. Wyniki te były istotne statystycznie. Nie odnotowano zakłóceń w rozwoju analizowanych pasożytów‑obserwowano stadia anamorficzne i teleomor‑ ficzne niezależnie od odległości. U Erysiphe alphitoides, odnotowano istotne statystycznie różnice w liczbie chasmotecjów pomiędzy strefą znajdującą się pod wpływem spalin samo‑ chodowych a strefą kontrolną. Interesujące wydaje się zaobserwowanie różnicy w rozwoju przyczepek. U E. alphitoides odnotowano znacznie więcej chasmotecjów bez przyczepek oraz z przyczepkami nie w pełni rozwiniętymi. Natomiast u E. hypophylla dominowały owocniki z przyczepkami w pełni rozwiniętymi. Ma to odzwierciedlenie w dojrzałości worków i zarodni‑ ków. U E. alphitoides stwierdzono wysoki udział owocników bez wykształconych worków i za‑ rodników, podczas gdy u E. hypophylla znacznie większy procent stanowiły chasmotecja z wor‑ kami wypełnionymi zarodnikami. W strefie do 50 m u Erysiphe alphitoides zarejestrowano owocniki nietypowe, o znacznie mniejszych wymiarach bez wykształconych worków i zarodników, ale z całkowicie wykształco‑ nymi przyczepkami a także owocniki ze zniekształconymi przyczepkami. 2014-01-01T11:48:59+0100 Polish Botanical Society