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Sphaeropsis sapinea (Fr.) Dyko & B. Sutton in Pinus sylvestris L. stands affected by long-term drought

Sphaeropsis sapinea (Fr.) Dyko & B. Sutton in Pinus sylvestris L. stands affected by long-term... In this study, the fruit bodies (pycnidial) colonization and spore presence of Sphaeropsis sapinea (Fr.) Dyko & B. Sutton on Scots pine (Pinus sylvestris L.) trees in stands affected by long-term drought in the Czech Republic were evaluated. A total of 520 cones at four sites were evaluated every 1.5 months from June 2019 to December 2020. The pycnidia of S. sapinea in relation to colonization by subcortical insects in inner bark and wood, and wood-decaying fungi a total of 340 trunks at 17 sites during the autumn of 2020 were also evaluated. Pycnidial colonization of S. sapinea on cones was significantly higher at the site with the highest air humidity and significantly lower in the sampling periods of June 2019, August 2019, and November 2019, which were characterized by low precipitation levels. S. sapinea spore presence on cones was significantly higher at sites in Bohemia compared to those in Moravia, in sites with higher air humidity, and in three consecutive sampling periods in March 2020–June 2020. Pycnidial colonization of S. sapinea on trunks was significantly positively dependent on the colonization of subcortical insects in both inner bark and wood, but not with the colonization of wood-decaying fungi. The results of this study show a positive relationship between high humidity and colonization by subcortical insects in inner bark and wood with S. sapinea on Scots pine. Key words: Diplodia tip blight; fungal pathogens; Scots pine; subcortical insects; wood-decaying fungi Editor: Andrej Kunca µm (Swart et al. 1993). Colonization of pine cones by S. 1. Introduction sapinea increases with higher winter temperatures and Sphaeropsis sapinea (Fr.) Dyko & B. Sutton, syn. Diplo- higher summer precipitation (Fabre et al. 2011). Germi- dia sapinea (Fr.) Fuckel, is an endophytic, ascomycet- nation of S. sapinea spores increases with high humid- ous fungus, plant saprophyte, and parasite that causes ity (Capretti et al. 2013). The optimal temperature for Diplodia tip blight (Bußkamp et al. 2020). Infection mycelial growth of the pathogen is about 30 °C (Keen & with S. sapinea can result in serious damage to conifers Smith 1989). Significant factors that influence the out - (Doğmuş-Lehtijärvi et al. 2014). The most common host break of S. sapinea are temperature, altitude and land trees of S. sapinea are pines (Pinus spp.), but Abies spp., cover (Bosso et al. 2017). Subcortical insects (Whitehill Cedrus spp., Larix spp., Picea spp. Pseudotsuga spp., et al. 2007; Davydenko & Baturkin 2020) and large pine Tsuga spp., Chamaecyparis spp., Cupressus spp., Juni- weevil (Hylobius abietis L.) (Drenkhan et al. 2017) can perus spp., Platycladus spp., Fagus spp., Quercus spp., be vectors of S. sapinea spores, making it easier for this Alnus spp. and Arceuthobium spp. can also serve as host pathogen to colonize the host’s cambial tissues. (Zwo- trees (Zlatković et al. 2017; Smahi et al. 2017; Bußkamp linski et al. 1995). S. sapinea is able to survive on dead et al. 2021; CABI 2021). host tissues for at least several months up to one year S. sapinea forms fruit bodies (pycnidis) that contain (Santini et al. 2008). spores (conidia) on the trunks, branches, needles, and S. sapinea attacks cones, which reduces the amount cones of the hosts (Zhou et al. 1997). Pycnidia are dark, of seed production and germination (Doğmuş-Lehtijärvi immersed to erumpent, ovoid, and ostiolate. Conidia are et al. 2014). S. sapinea also attacks trees from the seedling ovoid to obovoid, rounded at the apex, initially hyaline stage in nurseries to mature trees in ornamental plant- to yellowish becoming dark brown, usually 0–1 septate, ing, forest plantations and natural stands (Georgieva & thick-walled, and approximately 30–45 µm × 10–16 Hlebarska 2016). S. sapinea has an endophytic life stage *Corresponding author. František Lorenc, e-mail: lorenc@vulhm.cz, phone: +420 724 352 558 © 2022 Authors. This is an open access article under the CC BY 4.0 license. F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 when it does not harm the host (Smith et al. 1996; Flow- therefore be a useful method for determining stands that ers et al. 2001; Terhonen et al. 2020; Blumenstein et al. are in danger of being afflicted with Diplodia tip blight. 2021b). However, the fungus can accumulate unnoticed The aims of this study, which was performed in forest in healthy trees before the disease breaks out, represent- pine stands affected by long-term drought in the Czech ing a sudden threat to hosts (Stanosz et al. 2001; Blumen- Republic, were to: 1) monitor the dynamics of S. sap- stein et al. 2021a). The pathogenicity of S. sapinea has inea pycnidial colonization and its spore presence on pine increased due to climate change, climate warming, and cones and assess how they are affected by air temperature longer or more frequent droughts (Desprez-Loustau et al. and air humidity; 2) assess the link between the occur- 2007; Vornam et al. 2019). S. sapinea has changed from rence of S. sapinea pycnidial colonization on pine trunks a relatively harmless species to a virulent one in many and the colonization by subcortical insects intinner bark, countries (Spathelf et al. 2014). Pathogen-induced defo- subcortical insects in wood, and wood-decaying fungi. liation can act as predisposing and inciting factors for tree death, reducing the capacity of trees to survive short- or long-term stressing events, such as bark beetle attacks 2. Material and methods (Oliva et al. 2016). After years with prolonged drought episodes culmitating The occurrence of S. sapinea has been confirmed in in 2018 (Skalák et al. 2019; ČHMÚ 2021), 4 permanent a total of 128 countries in Europe, Asia, Africa, North research sites were established in the Czech Republic America, South America, Australia and Oceania (CABI in pine forest with visible symptoms of decline due to 2021). In Europe, S. sapinea is rapidly spreading to drought in June 201t: Valtice, Příšťpo, Brodce, Vrbová the north. Now, it is commonly seen in the Baltic Sea Lhota (Table 1). Each research site was approximately region (Adamson et al. 2015), Finland (Terhonen et al. rectangular in shape and consisted of 50 live P. sylvestris 2020) and Scandinavia (CABI 2021) and is threatening trees. A temperature-humidity logger (type S3631 from to become a serious pathogen in these areas (Brodde et Comet System, s.r.o, Czech Republic) was installed on al. 2019; Adamson et al. 2021). In recent years, water the trees in the centre of each site at a height of approxi- balance disturbances in Poland have contributed to the mately 1.3 m above the ground and was protected against spread of fungal pathogens, including S. sapinea, on P. direct sunlight and rain by a plastic cup coated with dark sylvestris (Skrzecz & Perlińska 2018). In Slovakia, S. sap- adhesive tape. The loggers recorded the air temperature inea has been a serious pathogen on Austrian pine (Pinus and relative air humidity at 1-hour intervals. Data was nigra J.F. Arnold) since 2000 (Kunca & Leontovyč 2013; gathered from the sites between July 2019 and Novem- Leontovyč et al. 2020), including urban trees (Juhásová ber with the exception of the Vrbová Lhota site. Only the et al. 2006). In the Czech Republic, S. sapinea previously period between January 2020 and November 2020 was occurred mainly on non-native P. nigra (Jankovský & considered for this site, as no data was gathered outside Palovčíková 2003; Novotný et al. 2012), but since 2015, of this period (due to logger failure). The mean daily it has also begun attacking native P. sylvestris, especially air temperature was calculated from the temperatures in stands weakened by drought and high temperatures measured by the logger at 7:00, 14:00, and 21:00 Central (Pešková & Soukup 2016). European Time, according to the formula: (T + T + 2 The most important measures to control the spread 7 14 × T ) / 4. The mean daily air humidity was calculated of S. sapinea are to provide and conserve water during as the arithmetic mean from the values measured by the drought seasons (Sinclair & Lyon 2005). Pruning and logger. The mean monthly air temperature and humidity removal of excised shoots of both seedlings (Munck were calculated as the arithmetic mean from the mean & Stanosz 2008) and mature trees may improve their appearance, but a new colonization may occur because daily values. conidia are also released from diseased cones on green Every 1.5 months, 10 light-coloured pine cones branches (Sinclair & Lyon 2005). The persistence of without traces of decomposition were collected at each pine-pathogenic species, such as S. sapinea, for up to research site from the sampling sites (evenly distrib- one year in dead plant material questions the feasibil- uted throughout the sites), from July 2019 to December ity of leaving coarse woody debris (Santini et al. 2008). 2020 (40 cones in each sampling period, 13 sampling Planting of more resistant tree species and varieties can periods, for a total of 520 cones). Pycnidial colonization also be recommended (Gerhold et al. 1994; Iturritxa et of S. sapinea on each cone was evaluated using a ster- al. 2013), but non-native species can be more susceptible eomicroscope in 4 classes: 0 (no pycnidia), 1 (individual to pathogens (Lombardero et al. 2008). In forest nurser- pycnidia), 2 (many pycnidia on some parts of cones only), ies, it is recommended to apply chemical preparations and 3 (many pycnidia on the whole cone) (Fig. 1). S. during the period of spore dissemination (Georgieva & sapinea spore presence in its pycnidia on each cone was Hlebarska 2016). There is a link between the S. sapinea subsequently evaluated using a laboratory microscope in spore presence on cones and the occurrence of Diplodia two levels: 0 (no spores) and 1 (spores present). Other tip blight (Peterson et Wysong 1968). Monitoring of fruit fungi on the cones were excluded from the evaluation. bodies and sporulation of S. sapinea on pine cones could 215 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 1. The examples of pycnydial colonization of Sphaeropis sapinea classes on cones: 0 – no pycnidia, 1 – individual pycnidia, 2 – many pycnidia on some parts of cones only, 3 – many pycnidia on the whole cone. Table 1. Summary information about research sites for evalu- (crown) parts of trunk only, because the pycnidia were ations on pine cones. Altitude – values in meters above sea totally absent on the thick bark in the other parts of the level; Soil type according to CENIA (2010–2020). trunks. Colonization of wood-decaying fungi was evalu- Site GPS Altitude Soil type ated as a presence of visible symptoms of the colonization Valtice 48.7596542N, 16.8160897E 185 Arenic Cambisols of these fungi: wood rot, fruit bodies on the trunk, myc- Příšťpo 49.0505056N, 15.9360144E 450 Dystric Cambisols Brodce 49.8422722N, 14.5976958E 305 Eutric Cambisols elium, syrrocium or rhizomorphs under bark. In unclear Vrbová Lhota 50.1180942N, 15.0869150E 190 Calcic Chernozems cases, samples were taken from the trunks and examined in a laboratory using a microscope. In 2020, a one-time evaluation was carried out at 17 The obtained data was statistically tested in SPSS sites in the Czech Republic (Table 2) that had a signic fi ant software. Generalized linear models (GLM) were used proportion of pine stands (ÚHÚL 2021), on this year’s (Denis 2019). fallen P. sylvestris trunks due to windfall, windbreak or cutting (based on informations from forest owners). Trunks which fall down before 2020 were not evaluated 3. results due to high colonization of saprotrophic fungi. Twenty trunks were evaluated per site (total 340 trunks). Pyc- The dynamics of air temperature and air humidity during nidial colonization of S. sapinea on trunks, colonization the measurement period (July 2019–November 2020) by subcortical insects in inner bark, subcortical insects were similar in all 4 permanent research sites. The high- in wood, and wood-decaying fungi were evaluated, all est mean monthly temperatures were recorded at the Val- in 3 levels: 0 (absent), 1 (low occurrence in a limited tice site and then at the Vrbová Lhota site. Above-average part of the trunk), 2 (strong or widespread occurrence). temperatures (compared to the normal from 1981–2010) Pycnidial colonization of S. sapinea was related to upper were recorded in all months at all sites, except for May Table 2. All sites for evaluation of Sphaeropsis sapinea on pine trunks, their positions and mean ± standard deviation (range 0–2) of assessed variables. Number of sampled trunks for each site: 20. Site GPS S. sapinea Insect inner bark Insect wood Fungi wood Býšť 50.1519389N, 15.8684200E 0.60 ± 0.94 1.30 ± 0.98 0.00 ± 0.00 0.20 ± 0.62 Horšovský Týn 49.5410833N, 12.9355556E 1.10 ± 0.91 1.90 ± 0.45 1.00 ± 0.97 0.85 ± 0.99 Chramosty 49.6632256N, 14.3142286E 1.85 ± 0.49 2.00 ± 0.00 0.85 ± 0.93 1.35 ± 0.93 Jemčina 49.1109722N 14.8534881E 0.30 ± 0.73 1.55 ± 0.83 0.00 ± 0.00 2.00 ± 0.00 Kladruby 49.7170089N, 13.0268167E 0.55 ± 0.89 0.80 ± 0.85 0.00 ± 0.00 0.10 ± 0.45 Kryry 50.2112686N, 13.4334769E 0.45 ± 0.69 1.40 ± 0.82 0.40 ± 0.75 0.05 ± 0.22 Nový Ples 50.3105811N 15.9525286E 1.65 ± 0.49 1.55 ± 0.83 1.50 ± 0.76 1.55 ± 0.83 Přelovice 50.0657689N, 15.6119669E 1.10 ± 0.91 1.70 ± 0.73 0.90 ± 0.91 1.30 ± 0.98 Rakov 49.3475000N, 14.3336111E 0.55 ± 0.89 1.45 ± 0.83 0.15 ± 0.49 0.50 ± 0.89 Rozkoš 49.0263511N 15.9537692E 0.40 ± 0.82 2.00 ± 0.00 1.30 ± 0.86 0.00 ± 0.00 Srní u České Lípy 50.6411639N, 14.6103083E 0.50 ± 0.83 1.80 ± 0.52 0.30 ± 0.66 1.60 ± 0.82 Strážnice 48.9428686N, 17.2704803E 1.40 ± 0.82 1.50 ± 0.76 0.00 ± 0.00 0.00 ± 0.00 Třeboň 49.0021900N, 14.8220656E 0.70 ± 0.98 1.70 ± 0.66 0.40 ± 0.75 0.20 ± 0.41 Tvořihráz 48.9092297N, 16.0999289E 0.50 ± 0.89 2.00 ± 0.00 0.00 ± 0.00 0.10 ± 0.45 Valtice 48.7663567N, 16.7900678E 0.05 ± 0.22 0.65 ± 0.93 0.00 ± 0.00 0.00 ± 0.00 Vrbová Lhota 50.1139339N, 15.0938819E 0.60 ± 0.88 0.60 ± 0.94 0.50 ± 0.89 0.10 ± 0.45 Ždírec 49.4648753N, 15.6571569E 1.10 ± 1.02 1.00 ± 1.03 0.00 ± 0.00 0.00 ± 0.00 216 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 2020 (Fig. 2). The highest air humidity was recorded at successive sampling periods March 2020, April 2020, the Brodce site, which was higher compared to other and June 2020 (Table 3, Fig. 4). sites, especially during June 2020–December 2020. The On pine trunks, S. sapinea pycnidia were recorded in lowest air humidity was recorded at the Vrbová Lhota site low occurrence (level 1) on 32 trunks (9%) and in strong (in all measurement months), and in terms of the period, occurrence (level 2) on 118 trunks (35%). Pycnidial from March 2020 to May 2020 with a minimum in April colonization of S. sapinea on trunks was significantly 2020 at all sites (Fig. 3). positively dependent on the colonization by subcortical On cones, pycnidial colonization of S. sapinea was insects in inner bark (Table 3, Fig. 5) and by subcortical significantly higher at the Brodce site (Table 3, Fig. 4), insects in wood (Table 3, Fig. 5), but independent from and in the sampling periods June 2019, August 2019, and the colonization by wood-decaying fungi (Table 3, Fig. 5). November 2019 (Table 3, Fig. 4). S. sapinea spore pres- White rot on wood occurred on most trunks colonized by ence differed among all sites, ranked in decreasing order: wood-decaying fungi, along with white syrrocium and/or Brodce, Vrbové Lhota, Příšťpo, Valtice (Table 3, Fig. 4). black cord-like rhizomorphs of Armillaria sp. Pycnidial colonization was also significantly higher in -5 2019 2019 2019 2019 2019 2019 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Valtice Příšťpo Brodce Vrbová Lhota Mean 1981–2010 Fig. 2. Mean monthly air temperature at research localitiessites for the evaluation of pine cones during the research period (own data), and mean monthly temperature for the Czech Republic in 1981–2010 (ČHMÚ 2021). 100 160 0 0 2019 2019 2019 2019 2019 2019 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Valtice Příšťpo Brodce Vrbová Lhota Precipitation levels Fig. 3. Mean monthly moisture at research sites for the evaluation of pine cones during the research period (own data) and pre- cipitation levels for the Czech Republic (ČHMÚ 2021). Mooisture [%] Temperature [C] Precipitation levels [mm] F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 4. Box plots of pycnidial colonization of Sphaeropsis sapinea and its spore presence on pine cones. Centre line – mean, box – standard deviation, whiskers – 1.96 * standard deviation. 130 samples per site box, 40 samples per sampling period box. Table 3. Generalized linear models (GLMs) of pycnidial colonization of Sphaeropsis sapinea and its spore presence on pine cones, and pycnidial colonization on pine trunks. Effect – tested variables, df – degrees of freedom, Wald – value of the Wald Chi-square test; p – significance level (number non-significant * p < 0.05 ** p < 0.01 *** p < 0.001). Model N Effect Wald df P Significantly different groups Pycnidial colonization Site 9.26 3 * higher: Brodce Sampling period 70.27 12 *** lower: 2019 June, 2019 August, 2019 November on cones Spore presence Site 58.54 3 * Brodce > Vrbová Lhota > Příšťpo > Valtice Sampling period 47.02 12 *** higher: 2020 March, 2020 April, 2020 June on cones Insect inner bark 12.95 2 ** positive dependence Pycnidial colonization 340 Insect wood 12.12 2 ** positive dependence on trunks Fungi wood 4.04 2 0.13 Pycnidial colonization of S. sapinea on cones was 4. Discussion significantly higher at the Brodce site, which was char - Higher temperatures at the Valtice and Vrbová Lhota acterized by the highest air humidity (Fig. 3). Zwolin- sites were related to their lower altitude (Table 1). Dur- ski et al. (1990) recorded a higher intensity of dieback ing our study, temperatures at all sites were higher than by S. sapinea on Pinus radiata in South Africa in areas mean temperatures in all months except May 2020. with lower altitudes, enclosed valley sites, and sheltered Low humidity at the Vrbová Lhota was probably due stands that are all characterised by higher air humidity to it being located on the edge of the forest next to a and smaller temperature variation. Pycnidial coloniza- meadow, whereas the other sites were within the forest tion of S. sapinea in our study was significantly lower stand. The high humidity at the Brodce site during June in the sampling periods June 2019, August 2019, and 2020–November 2020 compared to the other sites in our November 2019, which were characterized by high study was probably due to extremely high precipitation in temperatures compared to the mean from 1981–2020 June 2020 (171% compared to the mean from 1981–2020 (Fig. 2) and by low precipitation (ČHMÚ 2021; Fig. 3). for Prague and the Central Bohemian Region) (ČHMÚ High summer precipitation has a positive effect on the 2021). A subsequent period with sufficient precipita- colonization of pine cones by S. sapinea (Fabre et al. tion (ČHMÚ 2021) and the microclimatic conditions at the site were also causes of the high humidity. 2011). In the Czech Republic, lower precipitation lev- 218 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 5. Scatterplots of pycnidial colonization of Sphaeropsis sapinea fruit body growth rate on pine trunks. Numbers next to circles – number of its samples. Total 340 samples in each scatterplot. els were recorded in 2019 compared to 2020 during our Brodce, Vrbové Lhota, Příšťpo, Valtice. The Brodce and study (ČHMÚ 2021, Fig. 3). Blumenstein et al. (2021b) Vrbová Lhota sites were in Bohemia, while the remain- recorded a significantly higher abundance of S. sapinea ing 2 sites were in Moravia. These results are consist- on P. sylvestris branches in Germany in June compared ent with surveys of the Forest Protection Service in the to September. Contrary, pycnidial colonization of S. sap- Czech Republic, where the colonization of S. sapinea in inea on cones showed seasonal dynamics in our study, dying pine stands was higher in Bohemia than in Moravia probably due to negative effect of low humidity, respec- (Liška et al. 2018), although these differences were less tively low precipitations, and high summer temperatures. pronounced in the period of our study (2019–2020) than S. sapinea spore presence on cones in our study differed in previous years (Lorenc 2021). Of the pairs of sites both signic fi antly between all sites, ranked in decreasing order: in Bohemia and Moravia, S. sapinea spore presence was 219 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 higher at those with higher altitudes, which were char- bark and wood), and Orthotomicus erosus Wollaston (in acterized by lower air temperature (Fig. 2). In contrast, wood). The colonizationof S. sapinea was also associated the intensity of S. sapinea colonization (presence) (Fabre with infestation from the genus Dioryctia in P. resinosa et al. 2011) as so as infection (as a pathogen) (Zwolinski (Feci et al. 2003) and from pine cone bugs (Gastrodes et al. 1990) on pines decreased with increasing altitude grossipes De Geer) in P. nigra (Feci et al. 2002), which in previous studies (Zwolinski et al. 1990; Fabre et al. indicates the role of various groups of insects in spreading 2011). In Bohemia, the lower S. sapinea spore presence this fungus. Therefore, subcortical insects in both inner at the Vrbová Lhota site could be due to lower air humid- bark and wood could contribute to S. sapinea coloniza- ity (Fig. 3). In Moravia, the differences in air humidity tion of pine trunks in our study. S. sapinea pycnidial measurements between sites were small. According to colonization on trunks in our study was not depend- ČHMÚ (2021), precipitation levels in the same period ent on the colonization of wood-decaying fungi. White were 967 mm in the South Moravian Region (Valtice) wood rot was observed on most of the colonized trunks, and 1120 mm in the Vysočina region (Příšťpo). Thus, along with white syrrocium and/or black cord-like rhi- increased precipitation could be the reason for the higher zomorphs. These symptoms are typical signs of infec- S. sapinea spore presence in Příšťpo compared to that tion by honey fungus (Armillaria spp.), which is a very seen in Valtice. Overall, S. sapinea spore presence in our serious pathogen of woody plants, such as P. sylvestris study significantly differed between regions (higher in (Příhoda 1959). The virulence of this fungus increases Bohemia than in Moravia), higher humidity and pre- with high temperatures and low precipitation during the cipitation affected it positively, while the effects of both growing season (Lindner et al. 2008). Hurel et al. (2021) temperature and altitude were not significant. recorded a lower susceptibility to S. sapinea infection in Spore presence of S. sapinea on cones in our study populations of marine pine (Pinus pinaster Aiton) from was highest from March 2020–June 2020. Results areas with high temperatures and frequent droughts, from previous studies are different. Palmer et al. (1988) although a higher susceptibility to Armillaria ostoyae recorded the largest dispersion of S. sapinea spores on (Romagn.) Herink was recorded as well. Jankovský & red pine (Pinus resinosa Aiton) cones from April–June Palovčíková (2003) recorded S. sapinea on a mass scale in both research years 1981 and 1982. Kalder (2015) on shoots of declining Pinus nigra trees in the south- recorded the peak of S. sapinea sporulation on trunks of ern Moravia (Czech Republic), whereas Armillaria sp. 20-year-old pines in Estonia in early November. Brook- occurred only sparsely and only proliferated as a response houser & Peterson (1971) found the largest amount to the tree dieback, not as causal agents of the decline. It of releasing S. sapinea spores on P. nigra in Nebraska follows that pycnidial colonization of S. sapinea on pine from June–August in research year 1969, but only if trunks is not in direct positive relationship with coloniza- precipitation occurred during the relevant sampling tion by wood-decaying fungi. period. Capretti et al. (2013) reported a positive effect Increase in the drought frequency as a stress factor of air humidity on germination of S. sapinea spores. In causes a reduction in the assimilation apparatus, which our study, the period with the highest presence of spores reduces the carbon content in woody plants and subse- was first characterized by low humidity (March, April), quently weakens their resistance to biotic pests (Oliva et which then increased due to high precipitation (May, al. 2014), including fungal pathogens (Desprez-Loustau June) (Fig. 3). Thus, the seasonal dynamics of S. sapinea et al. 2006) and subcortical insects (Økland & Berryman 2004; Netherer et al. 2015). Secondary colonization by sporulation may vary signic fi antly between years depend - ing on weather conditions, especially precipitation and cambiophagous insects of trees infected by S. sapinea air humidity. can increase infection of S. sapinea and consequently the On trunks, pycnidial colonization of S. sapinea in our onset of dieback through girdling of branches and the study was signic fi antly positively dependent on coloniza - bole (Zwolinski et al. 1995). According to meta-analysis tion by subcortical insects both in inner bark and wood. by Jactel et al. (2012), primary pests and pathogens liv- Davydenko & Baturkin (2020) observed an association ing in wood (including A. ostoyeae) caused significantly between Ips acuminatus Gyllenhal and S. sapinea on P. lower damage to the water-stressed trees compared with the control, whereas primary pests and pathogens living sylvestris. An association between S. sapinea coloniza- tion and subcortical insects was also observed in other on foliage caused more damage to water-stressed trees, hosts. Monterey pines (Pinus radiata D. Don) infested all irrespective of stress severity. Damage by secondary with Pissodes neotensis Germar and Orthotomicus erosus pests and pathogens (including S. sapinea) increased Wollaston were more frequently infected with S. sapinea with water stress severity (Jactel et al. 2012). In our study, (Zwolinski et al. 1995). Bezos et al. (2018) found that, on colonization (presence) of S. sapinea without its relation Monterey pines, S. sapinea spores were found abundantly to damage was evaluated. S. sapinea can be present on in the galleries of bark beetles Tomicus piniperda L. (on tree mass like a saprophyte, without harming the host (Bußkamp et al. 2020; Blumenstein et al. 2021b). So, branches), Ips sexdentatus Börner, Hylastes attenuatus relationship between colonization and infection of S. Erichson, Hylastes ater Paykull, H. angustatus Herbst, Hylurgops palliatus Gyllenhal (in these 5 species in inner sapinea may not be always positively correlated. How- 220 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 ever, S. sapinea has ability to accumulate unnoticed as references an endophyte in healthy trees before the disease breaks Adamson, K., Kavina, D., Drenkhan, R., Gaitnieks, T., out, representing a sudden threat to P. sylvestris in the Hanso, M., 2015: Diplodia sapinea is colonizing future, especially with increasing drought conditions the native Scots pine (Pinus sylvestris) in the north- experienced by pines (Blumenstein et al. 2021b). ern Baltics. European Journal of Plant Pathology, 143:343–350. Adamson, K., Laas, M., Blumenstein, K., Busskamp, 5. Conclusion J., Langer, G. J., Klavina, D., Kaur, A., 2021: Highly clonal structure and abundance of one haplotype On cones, S. sapinea pycnidial colonization and its spore characterise the Diplodia sapinea populations in presence was positively affected mainly by air humidity. Europe and Western Asia. Journal of Fungi, 7:634. Although long periods of drought lead to the weaken- Bezos, D., Martínez-Álvarez, P., Sanz-Ros A.V., Martín- ing of trees that resulted in reduced resistance infection García, J., Fernandez, M.M., Diez, J.J., 2018: Fungal by pathogens (Oliva et al. 2014), including S. sapinea Communities Associated with Bark Beetles in Pinus (Vornam et al. 2019), the direct effect of drought on S. radiata Plantations in Northern Spain Affected by sapinea is negative (Desprez-Loustau et al. 2006; Hurel Pine Pitch Canker, with Special Focus on Fusarium et al. 2021). Relationship between colonization and Species. Forests, 9:698. infection of S. sapinea may not be positively correlated. Bußkamp, J., Langer, G. J., Langer, E. J., 2020: Sphaer- However, due to ability of S. sapinea to accumulate as opsis sapinea and fungal endophyte diversity in twigs an endophyte in healthy trees before the disease breaks of Scots pine (Pinus sylvestris) in Germany. Mycologi- out (Blumenstein et al. 2021b), pycnidial colonisation cal Progress, 19:985–999. and spore presence of the fungus can be useful indica- Bußkamp, J., Blumenstein, K., Terhonen, E., Langer, G. tors of possible threat of pine stands decline and dying in J., 2021: Differences in the virulence of Sphaeropsis the coming years. Climate change, manifested by rising sapinea strains originating from Scots pine and non- temperatures and more frequent extremes that include pine hosts. Forest Pathology, 51: e12712. longer and stronger droughts (Lindner et al. 2008), cur- Blumenstein, K., Bußkamp, J., Langer, G. J., Schlößer, rently leads to the increased infections of S. sapinea. R., Rojas, N. M. P., Terhonen, E., 2021a: Sphaer- However, reversing this trend cannot be ruled out due opsis sapinea and Associated Endophytes in Scots to the ambivalent relationship between S. sapinea and Pine: Interactions and Effect on the Host Under Vari- drought. able Water Content. Frontiers in Forests and Global The results of our study further confirm the relation- Change, 4:1–18. ship between colonization by subcortical insects both in Blumenstein, K., Bußkamp, J., Langer, G. J., Langer, inner bark and wood with the colonization of S. sapinea E. J., Terhonen, E., 2021b: The Diplodia Tip Blight on P. sylvestris. Subcortical insects can be vectors od S. Pathogen Sphaeropsis sapinea Is the Most Common sapinea spores (Zwolinski et al. 1995; Whitehill et al. Fungus in Scots Pines’ Mycobiome, Irrespective of 2007; Davydenko & Baturkin 2020). Moreover, coloni- Health Status–A Case Study from Germany. Journal zation by cambiophagous insects may extracerbate the of Fungi, 7:607. infection of S. sapinea and consequently onset to dieback Bosso, L., Luchi, N., Maresi, G., Cristinzio, G., Smer- of pines (Zwolinski et al. 1995). Thus, forest protection aldo, S., Russo, D., 2017: Predicting current and measures preventing colonization by subcortical insects future disease outbreaks of Diplodia sapinea shoot (including bark beetles) can also be useful for reduction blight in Italy: species distribution models as a tool of S. sapinea colonization and infection of pine trees. for forest management planning. Forest Ecology and Management, 400:655–664. Brodde, L., Adamson, K., Camarero, J. J., Castaño, C., Acknowledgement Drenkhan, R., Lehtijärvi, A. et al., 2019: Diplodia Tip This study was supported by the National Agency for Agricultural Blight on Its Way to the North: Drivers of Disease Research (NAZV) of the Ministry of Agriculture of the Czech Emergence in Northern Europe. Frontiers in plant Republic, Project No. QK1920406. The authors would also like Science, 9:1818. to thank the forest managers in the Město Poděbrady, Město Brookhouser, L. W., Peterson, G. W., 1971: Infection Týnec nad Sázavou, Lesní závod Židlochovce and Lesní správa of Austrian, Scots, and Ponderosa Pines by Diplodia Třebíč of the Forest of the Czech Republic for allowing us to use the stands for research and for providing the necessary docu- pinea. Phytopathology, 61:409–414. ments, and to anonymous editor from Scribendi for fast and Capretti, P., Santini, A., Solheim, H., 2013. Branch and quality English proofreading. tip blight. In: Gonthier, P., Nicolotti, G. (eds.): Infec- tious Forest Diseases. CABI, Croydon, United King- dom, p. 420–435. 221 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Davydenko, K. V., Baturkin, D. O., 2020: Pine engraver Jactel, H., Petit, J., Desprez-Loustau, M. 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Sphaeropsis sapinea (Fr.) Dyko & B. Sutton in Pinus sylvestris L. stands affected by long-term drought

Lorenc, František; Véle, Adam
Forestry Journal , Volume 68 (4): 10 – Dec 1, 2022
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Abstract

In this study, the fruit bodies (pycnidial) colonization and spore presence of Sphaeropsis sapinea (Fr.) Dyko & B. Sutton on Scots pine (Pinus sylvestris L.) trees in stands affected by long-term drought in the Czech Republic were evaluated. A total of 520 cones at four sites were evaluated every 1.5 months from June 2019 to December 2020. The pycnidia of S. sapinea in relation to colonization by subcortical insects in inner bark and wood, and wood-decaying fungi a total of 340 trunks at 17 sites during the autumn of 2020 were also evaluated. Pycnidial colonization of S. sapinea on cones was significantly higher at the site with the highest air humidity and significantly lower in the sampling periods of June 2019, August 2019, and November 2019, which were characterized by low precipitation levels. S. sapinea spore presence on cones was significantly higher at sites in Bohemia compared to those in Moravia, in sites with higher air humidity, and in three consecutive sampling periods in March 2020–June 2020. Pycnidial colonization of S. sapinea on trunks was significantly positively dependent on the colonization of subcortical insects in both inner bark and wood, but not with the colonization of wood-decaying fungi. The results of this study show a positive relationship between high humidity and colonization by subcortical insects in inner bark and wood with S. sapinea on Scots pine. Key words: Diplodia tip blight; fungal pathogens; Scots pine; subcortical insects; wood-decaying fungi Editor: Andrej Kunca µm (Swart et al. 1993). Colonization of pine cones by S. 1. Introduction sapinea increases with higher winter temperatures and Sphaeropsis sapinea (Fr.) Dyko & B. Sutton, syn. Diplo- higher summer precipitation (Fabre et al. 2011). Germi- dia sapinea (Fr.) Fuckel, is an endophytic, ascomycet- nation of S. sapinea spores increases with high humid- ous fungus, plant saprophyte, and parasite that causes ity (Capretti et al. 2013). The optimal temperature for Diplodia tip blight (Bußkamp et al. 2020). Infection mycelial growth of the pathogen is about 30 °C (Keen & with S. sapinea can result in serious damage to conifers Smith 1989). Significant factors that influence the out - (Doğmuş-Lehtijärvi et al. 2014). The most common host break of S. sapinea are temperature, altitude and land trees of S. sapinea are pines (Pinus spp.), but Abies spp., cover (Bosso et al. 2017). Subcortical insects (Whitehill Cedrus spp., Larix spp., Picea spp. Pseudotsuga spp., et al. 2007; Davydenko & Baturkin 2020) and large pine Tsuga spp., Chamaecyparis spp., Cupressus spp., Juni- weevil (Hylobius abietis L.) (Drenkhan et al. 2017) can perus spp., Platycladus spp., Fagus spp., Quercus spp., be vectors of S. sapinea spores, making it easier for this Alnus spp. and Arceuthobium spp. can also serve as host pathogen to colonize the host’s cambial tissues. (Zwo- trees (Zlatković et al. 2017; Smahi et al. 2017; Bußkamp linski et al. 1995). S. sapinea is able to survive on dead et al. 2021; CABI 2021). host tissues for at least several months up to one year S. sapinea forms fruit bodies (pycnidis) that contain (Santini et al. 2008). spores (conidia) on the trunks, branches, needles, and S. sapinea attacks cones, which reduces the amount cones of the hosts (Zhou et al. 1997). Pycnidia are dark, of seed production and germination (Doğmuş-Lehtijärvi immersed to erumpent, ovoid, and ostiolate. Conidia are et al. 2014). S. sapinea also attacks trees from the seedling ovoid to obovoid, rounded at the apex, initially hyaline stage in nurseries to mature trees in ornamental plant- to yellowish becoming dark brown, usually 0–1 septate, ing, forest plantations and natural stands (Georgieva & thick-walled, and approximately 30–45 µm × 10–16 Hlebarska 2016). S. sapinea has an endophytic life stage *Corresponding author. František Lorenc, e-mail: lorenc@vulhm.cz, phone: +420 724 352 558 © 2022 Authors. This is an open access article under the CC BY 4.0 license. F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 when it does not harm the host (Smith et al. 1996; Flow- therefore be a useful method for determining stands that ers et al. 2001; Terhonen et al. 2020; Blumenstein et al. are in danger of being afflicted with Diplodia tip blight. 2021b). However, the fungus can accumulate unnoticed The aims of this study, which was performed in forest in healthy trees before the disease breaks out, represent- pine stands affected by long-term drought in the Czech ing a sudden threat to hosts (Stanosz et al. 2001; Blumen- Republic, were to: 1) monitor the dynamics of S. sap- stein et al. 2021a). The pathogenicity of S. sapinea has inea pycnidial colonization and its spore presence on pine increased due to climate change, climate warming, and cones and assess how they are affected by air temperature longer or more frequent droughts (Desprez-Loustau et al. and air humidity; 2) assess the link between the occur- 2007; Vornam et al. 2019). S. sapinea has changed from rence of S. sapinea pycnidial colonization on pine trunks a relatively harmless species to a virulent one in many and the colonization by subcortical insects intinner bark, countries (Spathelf et al. 2014). Pathogen-induced defo- subcortical insects in wood, and wood-decaying fungi. liation can act as predisposing and inciting factors for tree death, reducing the capacity of trees to survive short- or long-term stressing events, such as bark beetle attacks 2. Material and methods (Oliva et al. 2016). After years with prolonged drought episodes culmitating The occurrence of S. sapinea has been confirmed in in 2018 (Skalák et al. 2019; ČHMÚ 2021), 4 permanent a total of 128 countries in Europe, Asia, Africa, North research sites were established in the Czech Republic America, South America, Australia and Oceania (CABI in pine forest with visible symptoms of decline due to 2021). In Europe, S. sapinea is rapidly spreading to drought in June 201t: Valtice, Příšťpo, Brodce, Vrbová the north. Now, it is commonly seen in the Baltic Sea Lhota (Table 1). Each research site was approximately region (Adamson et al. 2015), Finland (Terhonen et al. rectangular in shape and consisted of 50 live P. sylvestris 2020) and Scandinavia (CABI 2021) and is threatening trees. A temperature-humidity logger (type S3631 from to become a serious pathogen in these areas (Brodde et Comet System, s.r.o, Czech Republic) was installed on al. 2019; Adamson et al. 2021). In recent years, water the trees in the centre of each site at a height of approxi- balance disturbances in Poland have contributed to the mately 1.3 m above the ground and was protected against spread of fungal pathogens, including S. sapinea, on P. direct sunlight and rain by a plastic cup coated with dark sylvestris (Skrzecz & Perlińska 2018). In Slovakia, S. sap- adhesive tape. The loggers recorded the air temperature inea has been a serious pathogen on Austrian pine (Pinus and relative air humidity at 1-hour intervals. Data was nigra J.F. Arnold) since 2000 (Kunca & Leontovyč 2013; gathered from the sites between July 2019 and Novem- Leontovyč et al. 2020), including urban trees (Juhásová ber with the exception of the Vrbová Lhota site. Only the et al. 2006). In the Czech Republic, S. sapinea previously period between January 2020 and November 2020 was occurred mainly on non-native P. nigra (Jankovský & considered for this site, as no data was gathered outside Palovčíková 2003; Novotný et al. 2012), but since 2015, of this period (due to logger failure). The mean daily it has also begun attacking native P. sylvestris, especially air temperature was calculated from the temperatures in stands weakened by drought and high temperatures measured by the logger at 7:00, 14:00, and 21:00 Central (Pešková & Soukup 2016). European Time, according to the formula: (T + T + 2 The most important measures to control the spread 7 14 × T ) / 4. The mean daily air humidity was calculated of S. sapinea are to provide and conserve water during as the arithmetic mean from the values measured by the drought seasons (Sinclair & Lyon 2005). Pruning and logger. The mean monthly air temperature and humidity removal of excised shoots of both seedlings (Munck were calculated as the arithmetic mean from the mean & Stanosz 2008) and mature trees may improve their appearance, but a new colonization may occur because daily values. conidia are also released from diseased cones on green Every 1.5 months, 10 light-coloured pine cones branches (Sinclair & Lyon 2005). The persistence of without traces of decomposition were collected at each pine-pathogenic species, such as S. sapinea, for up to research site from the sampling sites (evenly distrib- one year in dead plant material questions the feasibil- uted throughout the sites), from July 2019 to December ity of leaving coarse woody debris (Santini et al. 2008). 2020 (40 cones in each sampling period, 13 sampling Planting of more resistant tree species and varieties can periods, for a total of 520 cones). Pycnidial colonization also be recommended (Gerhold et al. 1994; Iturritxa et of S. sapinea on each cone was evaluated using a ster- al. 2013), but non-native species can be more susceptible eomicroscope in 4 classes: 0 (no pycnidia), 1 (individual to pathogens (Lombardero et al. 2008). In forest nurser- pycnidia), 2 (many pycnidia on some parts of cones only), ies, it is recommended to apply chemical preparations and 3 (many pycnidia on the whole cone) (Fig. 1). S. during the period of spore dissemination (Georgieva & sapinea spore presence in its pycnidia on each cone was Hlebarska 2016). There is a link between the S. sapinea subsequently evaluated using a laboratory microscope in spore presence on cones and the occurrence of Diplodia two levels: 0 (no spores) and 1 (spores present). Other tip blight (Peterson et Wysong 1968). Monitoring of fruit fungi on the cones were excluded from the evaluation. bodies and sporulation of S. sapinea on pine cones could 215 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 1. The examples of pycnydial colonization of Sphaeropis sapinea classes on cones: 0 – no pycnidia, 1 – individual pycnidia, 2 – many pycnidia on some parts of cones only, 3 – many pycnidia on the whole cone. Table 1. Summary information about research sites for evalu- (crown) parts of trunk only, because the pycnidia were ations on pine cones. Altitude – values in meters above sea totally absent on the thick bark in the other parts of the level; Soil type according to CENIA (2010–2020). trunks. Colonization of wood-decaying fungi was evalu- Site GPS Altitude Soil type ated as a presence of visible symptoms of the colonization Valtice 48.7596542N, 16.8160897E 185 Arenic Cambisols of these fungi: wood rot, fruit bodies on the trunk, myc- Příšťpo 49.0505056N, 15.9360144E 450 Dystric Cambisols Brodce 49.8422722N, 14.5976958E 305 Eutric Cambisols elium, syrrocium or rhizomorphs under bark. In unclear Vrbová Lhota 50.1180942N, 15.0869150E 190 Calcic Chernozems cases, samples were taken from the trunks and examined in a laboratory using a microscope. In 2020, a one-time evaluation was carried out at 17 The obtained data was statistically tested in SPSS sites in the Czech Republic (Table 2) that had a signic fi ant software. Generalized linear models (GLM) were used proportion of pine stands (ÚHÚL 2021), on this year’s (Denis 2019). fallen P. sylvestris trunks due to windfall, windbreak or cutting (based on informations from forest owners). Trunks which fall down before 2020 were not evaluated 3. results due to high colonization of saprotrophic fungi. Twenty trunks were evaluated per site (total 340 trunks). Pyc- The dynamics of air temperature and air humidity during nidial colonization of S. sapinea on trunks, colonization the measurement period (July 2019–November 2020) by subcortical insects in inner bark, subcortical insects were similar in all 4 permanent research sites. The high- in wood, and wood-decaying fungi were evaluated, all est mean monthly temperatures were recorded at the Val- in 3 levels: 0 (absent), 1 (low occurrence in a limited tice site and then at the Vrbová Lhota site. Above-average part of the trunk), 2 (strong or widespread occurrence). temperatures (compared to the normal from 1981–2010) Pycnidial colonization of S. sapinea was related to upper were recorded in all months at all sites, except for May Table 2. All sites for evaluation of Sphaeropsis sapinea on pine trunks, their positions and mean ± standard deviation (range 0–2) of assessed variables. Number of sampled trunks for each site: 20. Site GPS S. sapinea Insect inner bark Insect wood Fungi wood Býšť 50.1519389N, 15.8684200E 0.60 ± 0.94 1.30 ± 0.98 0.00 ± 0.00 0.20 ± 0.62 Horšovský Týn 49.5410833N, 12.9355556E 1.10 ± 0.91 1.90 ± 0.45 1.00 ± 0.97 0.85 ± 0.99 Chramosty 49.6632256N, 14.3142286E 1.85 ± 0.49 2.00 ± 0.00 0.85 ± 0.93 1.35 ± 0.93 Jemčina 49.1109722N 14.8534881E 0.30 ± 0.73 1.55 ± 0.83 0.00 ± 0.00 2.00 ± 0.00 Kladruby 49.7170089N, 13.0268167E 0.55 ± 0.89 0.80 ± 0.85 0.00 ± 0.00 0.10 ± 0.45 Kryry 50.2112686N, 13.4334769E 0.45 ± 0.69 1.40 ± 0.82 0.40 ± 0.75 0.05 ± 0.22 Nový Ples 50.3105811N 15.9525286E 1.65 ± 0.49 1.55 ± 0.83 1.50 ± 0.76 1.55 ± 0.83 Přelovice 50.0657689N, 15.6119669E 1.10 ± 0.91 1.70 ± 0.73 0.90 ± 0.91 1.30 ± 0.98 Rakov 49.3475000N, 14.3336111E 0.55 ± 0.89 1.45 ± 0.83 0.15 ± 0.49 0.50 ± 0.89 Rozkoš 49.0263511N 15.9537692E 0.40 ± 0.82 2.00 ± 0.00 1.30 ± 0.86 0.00 ± 0.00 Srní u České Lípy 50.6411639N, 14.6103083E 0.50 ± 0.83 1.80 ± 0.52 0.30 ± 0.66 1.60 ± 0.82 Strážnice 48.9428686N, 17.2704803E 1.40 ± 0.82 1.50 ± 0.76 0.00 ± 0.00 0.00 ± 0.00 Třeboň 49.0021900N, 14.8220656E 0.70 ± 0.98 1.70 ± 0.66 0.40 ± 0.75 0.20 ± 0.41 Tvořihráz 48.9092297N, 16.0999289E 0.50 ± 0.89 2.00 ± 0.00 0.00 ± 0.00 0.10 ± 0.45 Valtice 48.7663567N, 16.7900678E 0.05 ± 0.22 0.65 ± 0.93 0.00 ± 0.00 0.00 ± 0.00 Vrbová Lhota 50.1139339N, 15.0938819E 0.60 ± 0.88 0.60 ± 0.94 0.50 ± 0.89 0.10 ± 0.45 Ždírec 49.4648753N, 15.6571569E 1.10 ± 1.02 1.00 ± 1.03 0.00 ± 0.00 0.00 ± 0.00 216 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 2020 (Fig. 2). The highest air humidity was recorded at successive sampling periods March 2020, April 2020, the Brodce site, which was higher compared to other and June 2020 (Table 3, Fig. 4). sites, especially during June 2020–December 2020. The On pine trunks, S. sapinea pycnidia were recorded in lowest air humidity was recorded at the Vrbová Lhota site low occurrence (level 1) on 32 trunks (9%) and in strong (in all measurement months), and in terms of the period, occurrence (level 2) on 118 trunks (35%). Pycnidial from March 2020 to May 2020 with a minimum in April colonization of S. sapinea on trunks was significantly 2020 at all sites (Fig. 3). positively dependent on the colonization by subcortical On cones, pycnidial colonization of S. sapinea was insects in inner bark (Table 3, Fig. 5) and by subcortical significantly higher at the Brodce site (Table 3, Fig. 4), insects in wood (Table 3, Fig. 5), but independent from and in the sampling periods June 2019, August 2019, and the colonization by wood-decaying fungi (Table 3, Fig. 5). November 2019 (Table 3, Fig. 4). S. sapinea spore pres- White rot on wood occurred on most trunks colonized by ence differed among all sites, ranked in decreasing order: wood-decaying fungi, along with white syrrocium and/or Brodce, Vrbové Lhota, Příšťpo, Valtice (Table 3, Fig. 4). black cord-like rhizomorphs of Armillaria sp. Pycnidial colonization was also significantly higher in -5 2019 2019 2019 2019 2019 2019 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Valtice Příšťpo Brodce Vrbová Lhota Mean 1981–2010 Fig. 2. Mean monthly air temperature at research localitiessites for the evaluation of pine cones during the research period (own data), and mean monthly temperature for the Czech Republic in 1981–2010 (ČHMÚ 2021). 100 160 0 0 2019 2019 2019 2019 2019 2019 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 2020 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Valtice Příšťpo Brodce Vrbová Lhota Precipitation levels Fig. 3. Mean monthly moisture at research sites for the evaluation of pine cones during the research period (own data) and pre- cipitation levels for the Czech Republic (ČHMÚ 2021). Mooisture [%] Temperature [C] Precipitation levels [mm] F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 4. Box plots of pycnidial colonization of Sphaeropsis sapinea and its spore presence on pine cones. Centre line – mean, box – standard deviation, whiskers – 1.96 * standard deviation. 130 samples per site box, 40 samples per sampling period box. Table 3. Generalized linear models (GLMs) of pycnidial colonization of Sphaeropsis sapinea and its spore presence on pine cones, and pycnidial colonization on pine trunks. Effect – tested variables, df – degrees of freedom, Wald – value of the Wald Chi-square test; p – significance level (number non-significant * p < 0.05 ** p < 0.01 *** p < 0.001). Model N Effect Wald df P Significantly different groups Pycnidial colonization Site 9.26 3 * higher: Brodce Sampling period 70.27 12 *** lower: 2019 June, 2019 August, 2019 November on cones Spore presence Site 58.54 3 * Brodce > Vrbová Lhota > Příšťpo > Valtice Sampling period 47.02 12 *** higher: 2020 March, 2020 April, 2020 June on cones Insect inner bark 12.95 2 ** positive dependence Pycnidial colonization 340 Insect wood 12.12 2 ** positive dependence on trunks Fungi wood 4.04 2 0.13 Pycnidial colonization of S. sapinea on cones was 4. Discussion significantly higher at the Brodce site, which was char - Higher temperatures at the Valtice and Vrbová Lhota acterized by the highest air humidity (Fig. 3). Zwolin- sites were related to their lower altitude (Table 1). Dur- ski et al. (1990) recorded a higher intensity of dieback ing our study, temperatures at all sites were higher than by S. sapinea on Pinus radiata in South Africa in areas mean temperatures in all months except May 2020. with lower altitudes, enclosed valley sites, and sheltered Low humidity at the Vrbová Lhota was probably due stands that are all characterised by higher air humidity to it being located on the edge of the forest next to a and smaller temperature variation. Pycnidial coloniza- meadow, whereas the other sites were within the forest tion of S. sapinea in our study was significantly lower stand. The high humidity at the Brodce site during June in the sampling periods June 2019, August 2019, and 2020–November 2020 compared to the other sites in our November 2019, which were characterized by high study was probably due to extremely high precipitation in temperatures compared to the mean from 1981–2020 June 2020 (171% compared to the mean from 1981–2020 (Fig. 2) and by low precipitation (ČHMÚ 2021; Fig. 3). for Prague and the Central Bohemian Region) (ČHMÚ High summer precipitation has a positive effect on the 2021). A subsequent period with sufficient precipita- colonization of pine cones by S. sapinea (Fabre et al. tion (ČHMÚ 2021) and the microclimatic conditions at the site were also causes of the high humidity. 2011). In the Czech Republic, lower precipitation lev- 218 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 Fig. 5. Scatterplots of pycnidial colonization of Sphaeropsis sapinea fruit body growth rate on pine trunks. Numbers next to circles – number of its samples. Total 340 samples in each scatterplot. els were recorded in 2019 compared to 2020 during our Brodce, Vrbové Lhota, Příšťpo, Valtice. The Brodce and study (ČHMÚ 2021, Fig. 3). Blumenstein et al. (2021b) Vrbová Lhota sites were in Bohemia, while the remain- recorded a significantly higher abundance of S. sapinea ing 2 sites were in Moravia. These results are consist- on P. sylvestris branches in Germany in June compared ent with surveys of the Forest Protection Service in the to September. Contrary, pycnidial colonization of S. sap- Czech Republic, where the colonization of S. sapinea in inea on cones showed seasonal dynamics in our study, dying pine stands was higher in Bohemia than in Moravia probably due to negative effect of low humidity, respec- (Liška et al. 2018), although these differences were less tively low precipitations, and high summer temperatures. pronounced in the period of our study (2019–2020) than S. sapinea spore presence on cones in our study differed in previous years (Lorenc 2021). Of the pairs of sites both signic fi antly between all sites, ranked in decreasing order: in Bohemia and Moravia, S. sapinea spore presence was 219 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 higher at those with higher altitudes, which were char- bark and wood), and Orthotomicus erosus Wollaston (in acterized by lower air temperature (Fig. 2). In contrast, wood). The colonizationof S. sapinea was also associated the intensity of S. sapinea colonization (presence) (Fabre with infestation from the genus Dioryctia in P. resinosa et al. 2011) as so as infection (as a pathogen) (Zwolinski (Feci et al. 2003) and from pine cone bugs (Gastrodes et al. 1990) on pines decreased with increasing altitude grossipes De Geer) in P. nigra (Feci et al. 2002), which in previous studies (Zwolinski et al. 1990; Fabre et al. indicates the role of various groups of insects in spreading 2011). In Bohemia, the lower S. sapinea spore presence this fungus. Therefore, subcortical insects in both inner at the Vrbová Lhota site could be due to lower air humid- bark and wood could contribute to S. sapinea coloniza- ity (Fig. 3). In Moravia, the differences in air humidity tion of pine trunks in our study. S. sapinea pycnidial measurements between sites were small. According to colonization on trunks in our study was not depend- ČHMÚ (2021), precipitation levels in the same period ent on the colonization of wood-decaying fungi. White were 967 mm in the South Moravian Region (Valtice) wood rot was observed on most of the colonized trunks, and 1120 mm in the Vysočina region (Příšťpo). Thus, along with white syrrocium and/or black cord-like rhi- increased precipitation could be the reason for the higher zomorphs. These symptoms are typical signs of infec- S. sapinea spore presence in Příšťpo compared to that tion by honey fungus (Armillaria spp.), which is a very seen in Valtice. Overall, S. sapinea spore presence in our serious pathogen of woody plants, such as P. sylvestris study significantly differed between regions (higher in (Příhoda 1959). The virulence of this fungus increases Bohemia than in Moravia), higher humidity and pre- with high temperatures and low precipitation during the cipitation affected it positively, while the effects of both growing season (Lindner et al. 2008). Hurel et al. (2021) temperature and altitude were not significant. recorded a lower susceptibility to S. sapinea infection in Spore presence of S. sapinea on cones in our study populations of marine pine (Pinus pinaster Aiton) from was highest from March 2020–June 2020. Results areas with high temperatures and frequent droughts, from previous studies are different. Palmer et al. (1988) although a higher susceptibility to Armillaria ostoyae recorded the largest dispersion of S. sapinea spores on (Romagn.) Herink was recorded as well. Jankovský & red pine (Pinus resinosa Aiton) cones from April–June Palovčíková (2003) recorded S. sapinea on a mass scale in both research years 1981 and 1982. Kalder (2015) on shoots of declining Pinus nigra trees in the south- recorded the peak of S. sapinea sporulation on trunks of ern Moravia (Czech Republic), whereas Armillaria sp. 20-year-old pines in Estonia in early November. Brook- occurred only sparsely and only proliferated as a response houser & Peterson (1971) found the largest amount to the tree dieback, not as causal agents of the decline. It of releasing S. sapinea spores on P. nigra in Nebraska follows that pycnidial colonization of S. sapinea on pine from June–August in research year 1969, but only if trunks is not in direct positive relationship with coloniza- precipitation occurred during the relevant sampling tion by wood-decaying fungi. period. Capretti et al. (2013) reported a positive effect Increase in the drought frequency as a stress factor of air humidity on germination of S. sapinea spores. In causes a reduction in the assimilation apparatus, which our study, the period with the highest presence of spores reduces the carbon content in woody plants and subse- was first characterized by low humidity (March, April), quently weakens their resistance to biotic pests (Oliva et which then increased due to high precipitation (May, al. 2014), including fungal pathogens (Desprez-Loustau June) (Fig. 3). Thus, the seasonal dynamics of S. sapinea et al. 2006) and subcortical insects (Økland & Berryman 2004; Netherer et al. 2015). Secondary colonization by sporulation may vary signic fi antly between years depend - ing on weather conditions, especially precipitation and cambiophagous insects of trees infected by S. sapinea air humidity. can increase infection of S. sapinea and consequently the On trunks, pycnidial colonization of S. sapinea in our onset of dieback through girdling of branches and the study was signic fi antly positively dependent on coloniza - bole (Zwolinski et al. 1995). According to meta-analysis tion by subcortical insects both in inner bark and wood. by Jactel et al. (2012), primary pests and pathogens liv- Davydenko & Baturkin (2020) observed an association ing in wood (including A. ostoyeae) caused significantly between Ips acuminatus Gyllenhal and S. sapinea on P. lower damage to the water-stressed trees compared with the control, whereas primary pests and pathogens living sylvestris. An association between S. sapinea coloniza- tion and subcortical insects was also observed in other on foliage caused more damage to water-stressed trees, hosts. Monterey pines (Pinus radiata D. Don) infested all irrespective of stress severity. Damage by secondary with Pissodes neotensis Germar and Orthotomicus erosus pests and pathogens (including S. sapinea) increased Wollaston were more frequently infected with S. sapinea with water stress severity (Jactel et al. 2012). In our study, (Zwolinski et al. 1995). Bezos et al. (2018) found that, on colonization (presence) of S. sapinea without its relation Monterey pines, S. sapinea spores were found abundantly to damage was evaluated. S. sapinea can be present on in the galleries of bark beetles Tomicus piniperda L. (on tree mass like a saprophyte, without harming the host (Bußkamp et al. 2020; Blumenstein et al. 2021b). So, branches), Ips sexdentatus Börner, Hylastes attenuatus relationship between colonization and infection of S. Erichson, Hylastes ater Paykull, H. angustatus Herbst, Hylurgops palliatus Gyllenhal (in these 5 species in inner sapinea may not be always positively correlated. How- 220 F. Lorenc, A. Véle / Cent. Eur. For. J. 68 (2022) 214–223 ever, S. sapinea has ability to accumulate unnoticed as references an endophyte in healthy trees before the disease breaks Adamson, K., Kavina, D., Drenkhan, R., Gaitnieks, T., out, representing a sudden threat to P. sylvestris in the Hanso, M., 2015: Diplodia sapinea is colonizing future, especially with increasing drought conditions the native Scots pine (Pinus sylvestris) in the north- experienced by pines (Blumenstein et al. 2021b). ern Baltics. European Journal of Plant Pathology, 143:343–350. Adamson, K., Laas, M., Blumenstein, K., Busskamp, 5. Conclusion J., Langer, G. J., Klavina, D., Kaur, A., 2021: Highly clonal structure and abundance of one haplotype On cones, S. sapinea pycnidial colonization and its spore characterise the Diplodia sapinea populations in presence was positively affected mainly by air humidity. Europe and Western Asia. Journal of Fungi, 7:634. Although long periods of drought lead to the weaken- Bezos, D., Martínez-Álvarez, P., Sanz-Ros A.V., Martín- ing of trees that resulted in reduced resistance infection García, J., Fernandez, M.M., Diez, J.J., 2018: Fungal by pathogens (Oliva et al. 2014), including S. sapinea Communities Associated with Bark Beetles in Pinus (Vornam et al. 2019), the direct effect of drought on S. radiata Plantations in Northern Spain Affected by sapinea is negative (Desprez-Loustau et al. 2006; Hurel Pine Pitch Canker, with Special Focus on Fusarium et al. 2021). Relationship between colonization and Species. Forests, 9:698. infection of S. sapinea may not be positively correlated. Bußkamp, J., Langer, G. J., Langer, E. J., 2020: Sphaer- However, due to ability of S. sapinea to accumulate as opsis sapinea and fungal endophyte diversity in twigs an endophyte in healthy trees before the disease breaks of Scots pine (Pinus sylvestris) in Germany. Mycologi- out (Blumenstein et al. 2021b), pycnidial colonisation cal Progress, 19:985–999. and spore presence of the fungus can be useful indica- Bußkamp, J., Blumenstein, K., Terhonen, E., Langer, G. tors of possible threat of pine stands decline and dying in J., 2021: Differences in the virulence of Sphaeropsis the coming years. Climate change, manifested by rising sapinea strains originating from Scots pine and non- temperatures and more frequent extremes that include pine hosts. Forest Pathology, 51: e12712. longer and stronger droughts (Lindner et al. 2008), cur- Blumenstein, K., Bußkamp, J., Langer, G. J., Schlößer, rently leads to the increased infections of S. sapinea. R., Rojas, N. M. P., Terhonen, E., 2021a: Sphaer- However, reversing this trend cannot be ruled out due opsis sapinea and Associated Endophytes in Scots to the ambivalent relationship between S. sapinea and Pine: Interactions and Effect on the Host Under Vari- drought. able Water Content. Frontiers in Forests and Global The results of our study further confirm the relation- Change, 4:1–18. ship between colonization by subcortical insects both in Blumenstein, K., Bußkamp, J., Langer, G. J., Langer, inner bark and wood with the colonization of S. sapinea E. J., Terhonen, E., 2021b: The Diplodia Tip Blight on P. sylvestris. Subcortical insects can be vectors od S. Pathogen Sphaeropsis sapinea Is the Most Common sapinea spores (Zwolinski et al. 1995; Whitehill et al. Fungus in Scots Pines’ Mycobiome, Irrespective of 2007; Davydenko & Baturkin 2020). Moreover, coloni- Health Status–A Case Study from Germany. Journal zation by cambiophagous insects may extracerbate the of Fungi, 7:607. infection of S. sapinea and consequently onset to dieback Bosso, L., Luchi, N., Maresi, G., Cristinzio, G., Smer- of pines (Zwolinski et al. 1995). Thus, forest protection aldo, S., Russo, D., 2017: Predicting current and measures preventing colonization by subcortical insects future disease outbreaks of Diplodia sapinea shoot (including bark beetles) can also be useful for reduction blight in Italy: species distribution models as a tool of S. sapinea colonization and infection of pine trees. for forest management planning. Forest Ecology and Management, 400:655–664. Brodde, L., Adamson, K., Camarero, J. J., Castaño, C., Acknowledgement Drenkhan, R., Lehtijärvi, A. et al., 2019: Diplodia Tip This study was supported by the National Agency for Agricultural Blight on Its Way to the North: Drivers of Disease Research (NAZV) of the Ministry of Agriculture of the Czech Emergence in Northern Europe. 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Journal

Forestry Journal – de Gruyter

Published: Dec 1, 2022

Keywords: Diplodia tip blight; fungal pathogens; Scots pine; subcortical insects; wood-decaying fungi

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