Santini A, Faccoli M (2015). Dutch Elm Disease and Elm Bark Beetles

Home , Dutch elm disease, Ophiostoma, Ophiostoma ulmi, Scolytus, Scolytus multistriatus, Scolytus schevyrewi

Review Article - doi: 10.3832/ifor1231-008 ©iForest – Biogeosciences and Forestry

Collection: 3rd International Elm Conference, Florence (Italy - 2013) the fungus growth, enhancing the pathogen “The elms after 100 years of Dutch Elm disease” aggressiveness. Guest Editors: A. Santini, L. Ghelardini, E. Collin, A. Solla, J. Brunet, M. Faccoli, A. Scala, After a century since the beginning of the S. De Vries, J. Buiteveld first pandemic of DED in Europe (Spieren- burg 1921), and the introduction in the USA of one of its most effective vector, the small Dutch elm disease and elm bark beetles: a elm bark beetle Scolytus multistriatus (Chap- man 1910), the amount of available scienti- century of association fic data is indeed vast and covers many aspects. The aim of the present paper is to provide a thorough review of the knowledge (1) (2) Alberto Santini , Massimo Faccoli concerning the association between DED pathogens and vectors. Possible challenges for future research topics are also explored. Bark beetles of the genus Scolytus Geoffroy are the main vectors of the fungus Ophiostoma ulmi s.l., which causes the Dutch elm disease. The large and small Ophiostoma ulmi s.l. and Dutch elm bark beetles - S. scolytus (F.) and S. multistriatus (Marsham), respectively elm disease - are the most common and important species spreading the pathogen world- As a result of DED, during the last century wide. The success of the pathogen-insect interactions is mainly due to the cha- elms suffered major losses worldwide, with racteristic reproductive behavior of the elm bark beetles, which, however, lar- the near-total disappearance of adult trees in gely depends on the occurrence of infected trees. During feeding activity on many European, Asian and North American elm twigs, callow adults carrying pathogen conidia on their bodies contaminate areas. Two pandemics occurred. The first, healthy trees and facilitate pathogen development and movement within the caused by O. ulmi (Buisman) Nannfield, be- wood vessels. Infected trees become then suitable for insect breeding in the gan in Europe in the 1910s (Spierenburg stem bark. This well-known mutualistic association has devastating consequen- 1921) and rapidly devastated elm popula- ces for elm survival. Although much is known about insect-pathogen interactions in Europe and, 20 years later, in North tions and transmission mechanisms, many topics still deserve additional atten- America (Brasier 2000, Guries 2001). tion, as, for example, beetle systematic based on new molecular tools and Around 1940, the disease declined in Europe morphological characters; selection of European elm clones based on disease (Brasier 1979, Mittempergher 1989). A few avoidance; consequences of global warming on life-history of the three orga- years later, in the mid-1900s, a second and nisms (fungus-insect-tree) involved in the pathosystem; new problems resulting more destructive pandemic caused the wide- from the rapid increase of international trade among continents, leading to the spread destruction of mature elms in Europe, accidental introduction of new vector species or new pathogen species or Western Asia and North America (Gibbs & races, or to the introduction of new highly susceptible elm species in gardens Brasier 1973, Brasier & Kirk 2001). This and public parks. A holistic approach to tackle the problem is highly recom- second still active pandemic is due to a dif- mended, taking into account how these organisms interact with each other and ferent fungus species, the highly virulent O. the environment, and how their interactions could be modified in order to face novo-ulmi Brasier (Brasier 1991), which has one of the most destructive diseases ever known in plant pathology. almost totally replaced O. ulmi. Moreover, two subspecies of O. novo-ulmi are known: Keywords: Dutch Elm Disease, Elm Bark Beetles, Scolytus-Ophiostoma Interac- O. novo-ulmi ssp. novo-ulmi, previously tions, DED Cycle, Avoidance Mechanisms, Disease Escape, Resistance known as the Euro-Asian race (EAN), and O. novo-ulmi ssp. americana, previously known as the North American race (NAN - Introduction vities, providing a number of different fo- Brasier 1979, Brasier & Kirk 2001). Since Dutch elm disease (DED), caused by some rest, agricultural and cultural services. DED the 1980s, the presence of hybrids has been Ascomycete fungi of the genus Ophiostoma spreading and infection of suitable hosts is detected between these two subspecies. The (Ophiostoma ulmi s.l.), is one of the most mainly due to a synchrony between life cy- hybrids, whose pathogenicity does not differ destructive diseases of woody trees ever cles of host-tree, pathogen and elm bark bee- from that of their parent subspecies (Santini known in plant pathology. The severity and tles (Coleoptera: Curculionidae, Scolytinae), et al. 2005b), are now expanding across the devastation of its pandemics stirred up the the main fungus vectors. Such a synchrony continents (Brasier & Kirk 2010). A third interest of public opinion and researchers allows the insect vectors to spread the pa- species, O. himal-ulmi Brasier & Mehrotra, (Rohring 1996). Since prehistory, elms (Ul- thogen when host plants are more prone to which also causes DED, was identified in the mus spp.) are strictly linked to human acti- be infected and temperatures are favorable to Himalayas (Brasier & Mehrotra 1995), but its presence has still not been reported in Eu- (1) Institute of Sustainable Plant Protection, CNR, v. Madonna del Piano 10, I-50019 Sesto rope or North America. Fiorentino (FI - Italy); (2) Department of Agronomy, Food, Natural Resources, Animals and The destructiveness and severity of this di- Environment (DAFNAE), Agripolis, v.le dell’Università 16, I-35020 Legnaro (PD - Italy) sease is mainly due to the rapidity and efficiency of its spread, which is particularly @ Alberto Santini ([email protected]) quick and effective because O. ulmi s.l. has exploited an ancient association between the Received: Jan 02, 2014 - Accepted: May 18, 2014 native saprotrophic species O. quercus and Citation: Santini A, Faccoli M, 2015. Dutch elm disease and elm bark beetles: a century of the elm bark beetles active in Europe prior to association. iForest 8: 126-134 [online 2014-08-07] URL: http://www.sisef.it/ the arrival of O. ulmi (Brasier 1990). Va- iforest/contents/?id=ifor1231-008 rious species of elm bark beetles are involved in the disease transmission. Callow bee- Communicated by: Marco Borghetti

© SISEF http://www.sisef.it/iforest/ 126 iForest (2015) 8: 126-134 Santini A & Faccoli M - iForest 8: 126-134 tles (i.e., sexually immature) emerge in duces the hydraulic conductivity in the func- fic insects (Pearce et al. 1975, Wood 1982, spring from the bark of dying infected elms tional xylem, resulting in a severe wilt syn- Faccoli 2004), assuring the whole bark colo- and fly to the crown of healthy elms to feed drome which kills the tree rapidly (MacHar- nization (Peacock et al. 1971). at the crotches of young twigs. Infected bee- dy & Beckman 1973). Elm bark beetles usually lay eggs in the tles contaminate healthy elms by carrying the phloem of weakened trees (Fig. 1). After pathogen spores into feeding wounds, in di- Life history of the elm bark finding and acceptance of the host, elm bark rect contact with the host’s vascular tissues. beetles beetle females bore an entrance hole through Spores germinate into a growing mycelium Bark beetles belonging to the genus Scoly- the tree bark, communicating with a small and reach the xylem, where the pathogen tus Geoffroy are the main vectors of Ophio- mating (or nuptial) chamber excavated in the moves into the vessels through a yeast multi- stoma ulmi s.l. (Webber & Brasier 1984). phloem, where mating occurs (Fransen 1939, plication phase (Webber & Brasier 1984). Although about 10 species of Scolytus live Svihra & Clark 1980). Each mated female Later on, the beetles move to dying elms, on elms (Wood & Bright 1992, Pfeffer excavates a maternal tunnel (or egg gallery) i.e., infected by DED, to lay eggs in the inner 1995), the large and small elm bark beetles - in the phloem where eggs are laid along both bark of the stem and main branches, which S. scolytus (F.) and S. multistriatus (Mar- sides. The maternal galleries run parallel to provide an ideal environment for both larval sham), respectively - are the most common the wood fibers, without ramifications (Sin- development (Rudinsky 1962) and pathogen and important species spreading the patho- clair & Campana 1978, Burdekin 1979, fructification (Webber & Brasier 1984). The gen worldwide (Webber & Kirby 1983, Agrios 1988). Construction of the maternal new contaminated beetles emerge from the Webber & Brasier 1984, Webber & Gibbs tunnels and egg-laying take about three bark and move toward the crown of new 1989, Webber 1990, Webber 2000, Faccoli weeks (Betrem 1929). Larvae hatch about healthy elms, completing the cycle. The in- 2001, 2004). one week after oviposition, and immediately fection may also occur through root anasto- Many species of elms have been recorded begin to bore characteristic larval galleries moses between infected and healthy trees as potential elm bark beetle hosts, both in developing in an orthogonal direction from (Webber & Brasier 1984). the insects’ native distribution range and in the maternal ones (Balachowsky 1949, Bur- Initial external symptoms of DED include countries of new introduction (Balachowsky dekin 1979, Agrios 1988). Larval galleries of crown discoloration and leaf wilting. Symp- 1949, Stark 1952, Michalski 1973, Wood & Scolytus spp. are 60-150 mm long on ave- toms spread along branches centrally, affec- Bright 1992, Pfeffer 1995). Elm bark beetles rage and they cross each other only rarely ting the entire crown, and the tree dies attack trees dying, stressed or weakened by (Betrem 1929, Buisman 1932, Manojlovic & rapidly. A typical internal symptom of the different factors (e.g., drought, diseases, pru- Sivcev 1995, Kletecka 1996). Larval tunnels disease is the formation of a brown ring in ning, defoliations). Mature beetles identify become wider as the larvae develop and the infected sapwood due to the formation of potentially suitable hosts by a blend of vola- move away from the maternal gallery (Be- tyloses and gels in the xylem vessels (Stipes tiles released by damaged or diseased elms trem 1929). Larvae feed in the phloem for & Campana 1981, Rioux et al. 1998, Ouel- (Meyer & Norris 1967, Pearce et al. 1975). about 30 days, passing through 5 developing lette et al. 2004a, 2004b, Et-Touil et al. Following initial attacks by the pioneer bee- instars before becoming fully grown (Fran- 2005), resulting in their obstruction (Zim- tles, most of the insect populations find the sen 1939). Shortly before pupation, mature mermann & McDonough 1978, Newbanks et suitable hosts in response to a blend of ag- larvae bore a pupal chamber in the external al. 1983). A systemic infection drastically re- gregation pheromones released by conspeci- part of the sap-wood, where they metamor- phose first into pupae (Webber & Brasier 1984, Webber 1990) and after about two weeks into adults (Zanta & Battisti 1990). The new callow adults then emerge from the bark of the host tree through a hole excavated directly from the pupal chamber (Kle- tecka 1996). After emergence, adults fly and disperse looking for healthy trees on which they carry out the sexual maturation feeding. Elm bark beetles may be mono- or bivoltine. In favorable climatic conditions there are usually two generations per year (Della Beffa 1949), the first starting in late spring (May-June) and emerging in late summer (August-September), the second beginning in autumn (September) overwintering as larvae, and emerging in the following spring (Betrem 1929, Buisman 1932, Fransen 1939, Lanier & Peacock 1981, Zanta & Battisti 1990). In all monogamous bark beetle species, before reproducing in the bark of dying trees, the newly emerged callow adults need a period of sexual maturation reached by feeding in crotches of 2-3 years old twigs of healthy and vigorous elms. The maturation feeding lasts a few days, during which the insects ex- cavate short tunnels (2-4 cm long) in the twig phloem and sapwood (Fransen 1939, Webber & Brasier 1984). Twig feeding, Fig. 1 - Dutch elm disease cycle (modified from Ghelardini & Santini 2009). iForest 8: 126-134 127 © SISEF http://www.sisef.it/iforest/ Ophiostoma ulmi and Scolytus spp. association which is a prerequisite for sexual maturation 1990). Later, the arrival in Europe of the feeding results, however, in pathogen trans- of callow adults, is associated also with congeneric O. ulmi s.l., a fungus having ni- mission (Fransen 1939). Parker et al. (1941) restoration of the beetle reserves (food and che requirements similar to O. quercus but reported that 13% of all cases resulted in tree water - Fransen 1939, Svihra & Clark 1980, far more aggressive, caused the complete re- infection, whereas Webber & Brasier (1984) Lanier & Peacock 1981, Heybroek et al. placement of the endemic fungus. The new found that about 30% of feeding wounds 1982, Lunderstadt & Rohde 1993). Although association became an effective DED trans- were infected by O. ulmi s.l. Xylem infection Scolytus beetles prefer twigs occurring on mission pathway, with devastating conse- may be a result either of a primary and direct the upper part of the crown (Svihra & Clark quences for elm survival. spore transfer from the beetle into the xylem 1980, Webber & Kirby 1983), feeding tun- The success of the pathogen-insect interac- vessels or, more likely, of a secondary infec- nels can be made in almost any young and tions is mainly due to the characteristic re- tion due to earlier pathogen colonization of sappy bark (Fransen 1939, Lanier & Peacock productive behavior of the elm bark beetles, the feeding wound followed by subsequent 1981, Webber & Kirby 1983). Scolytus bee- and largely depends on the occurrence of O. growth into the xylem tissues (Buisman tles can stay in the feeding tunnels for up to ulmi infected trees. The feeding activity of 1932). 13 days (Fransen 1939). When sexual matu- callow adults emerged from infected trees, rity is reached, adults fly away looking for and carrying pathogen conidia on their bo- Host resistance weakened trees in which they lay eggs and dies, contaminates healthy trees and facilita- There is considerable variation among elm start a new generation. tes consequent development and movement species in host resistance to DED. Asian of the pathogen within their wood vessels elms are usually the most resistant (Smalley Interactions among elms, DED (Fransen & Buisman 1935, Goidanich 1936, & Kais 1966, Ware 1995, Smalley & Guries fungi and elm bark beetles Goidanich & Goidanich 1937, Gibbs 1974, 2000), while most North American elms are The mechanisms of pathogen transmission Burdekin 1979, Webber & Kirby 1983, highly susceptible and European species are were deeply investigated in the past (Webber Webber & Brasier 1984). Basset et al. moderately to very susceptible (Gibbs 1978, & Brasier 1984). Some authors considered (1992) showed that a contact for at least 72 Dunn 2000). the wind to be important in spreading fungal hours between infected beetles and xylem Compared with susceptible elms, both at spores from infected plants to tissues of can be sufficient for the pathogen transmis- species and individual level, naturally resis- healthy trees exposed by wounds or pruning sion. This is known as the pathogenic phase tant elms show some peculiar anatomical (Westerdijk & Buisman 1929, Smucker of the disease (Lea 1977, Gibbs & Smith features such as smaller (McNabb et al. 1935). This hypothesis, however, was soon 1978). The canopy of every tree may host 1970, Sinclair et al. 1975, Solla & Gil disproved, as anemochoral dispersion of the several dozen callow adults, and the process 2002a, 2002b, Solla et al. 2005b) and shor- spores would be too casual and generic, and can be repeated for several years; thus, ter vessels (Elgersma 1970, Ewers et al. could not ensure ideal growing conditions to healthy trees growing close to elms infected 1990, Tyree & Zimmermann 2002), smaller the pathogen for a rapid development (Goi- by O. ulmi s.l. and infested by elm bark bee- pit membrane diameter and pit aperture area, danich & Goidanich 1937). tles are exposed to a very high risk of infec- lower pit membrane abundance per vessel- Other authors suggested the rain as the tion. This transient phase is very important wall, smaller ray width and ray tangential main responsible of the conidial spread, allo- for pathogen spread, as it is the only way for area (Martín et al. 2009). Anatomical fea- wing them to reach the leaf stomata (Sch- the fungus to reach and infect isolated trees. tures, however, show much variability also warz 1922). However, in 1927 Marchal pro- Maturation feeding and pathogen infection between and within species. For instance, posed that bark beetles could be vectors of weaken trees that will become attractive for the mean maximum vessel length and diame- O. ulmi s.l., as they migrate between infected mature reproductive adults of the following ter are significantly higher in U. minor than and healthy elms (Marchal 1927). Although insect generations, which will be looking for in U. minor x pumila, and these differences the pathogen may be transmitted effectively dying (i.e., diseased) elms where to lay eggs increase with age (Martin et al. 2013). in several ways (Schwarz 1922, Westerdijk in the bark of trunk and main branches. Du- Induced resistance to DED is associated & Buisman 1929, Smucker 1935), elm bark ring bark infestation and excavation of the strictly with the host’s capacity to quickly lo- beetles belonging to the genus Scolytus were mating galleries, the mature adults again in- calize the infection, preventing the pathogen found to be the most effective pathogen vec- fect the hosts with the conidia carried on from spreading in the vascular system (Sin- tors (Marchal 1927, Fransen 1931, Jacot their tegument, fulfilling their role as vectors clair et al. 1975) and reaching the cambium 1934, 1936, Collins et al. 1936, Webber & for a second time. Bark colonization by in- (Shigo & Tippet 1981, Bonsen et al. 1985). Brasier 1984, Webber 1990, Basset et al. sects and pathogen on already infected elms Reactions taking place as a consequence of 1992, Favaro & Battisti 1993, Battisti et al. (from the twigs) is known as the saprophytic the infection may include vessel closing by 1994, Faccoli & Battisti 1997, Faccoli et al. phase of the disease (Lea 1977, Gibbs & tyloses, embolisms, accumulation of pectin 1998, Faccoli 2004). The definitive demon- Smith 1978). In this respect, maternal gal- and hemicelluloses (Elgersma 1982, Shigo stration of Marchal’s theory was provided by leries and pupal chambers are an ideal mi- 1982, Ouellette & Rioux 1992, Rioux et al. Fransen (1931) and Fransen & Buisman cro-environment for both fungal growth and 1998), synthesis of chemicals such as phyto- (1935), who showed pathogen presence and sporulation (Webber & Brasier 1984). Inte- alexin-like sesquiterpenes (Jeng et al. 1983, proliferation in the short galleries bored by restingly, in this phase two fungus isolates Duchesne et al. 1985, Sticklen et al. 1991), elm bark beetles in healthy plants during having different origins, one from previous and formation of histological barriers typi- maturation feeding. Many other vectors were maturation feeding and the other from the cally containing phenols and suberin (Rioux later identified, mainly mites and insects li- more recent bark colonization, may meet in & Ouellette 1991a, 1991b, Ouellette et al. ving on elms, but none as effective as bark the same tree. This gives to the pathogen 2004a, 2004b, Et-Touil et al. 2005). beetles (Jacot 1934, 1936, Collins et al. more chances of sexual reproduction, being Elm susceptibility to DED shows strong 1936). O. ulmi s.l. an obliged outcrossing fungus. seasonal variation in both resistant and sus- Elm bark beetles originally had a mutuali- The emerging beetle offspring developed in ceptible species. The period of highest sus- stic ectosymbiosis with the indigenous sa- the phloem of infected trees will become ceptibility and its duration, i.e., the period protrophic fungus O. quercus, previously new vector of fungal conidia and the disper- during which trees can easily become infec- known as the hardwood biological species sal cycle will start again (Webber & Brasier ted varies greatly among elm species and group, or OPH group, of O. piceae (Brasier 1984). Not every wound due to maturation even among elm populations and experimen-

© SISEF http://www.sisef.it/iforest/ 128 iForest (2015) 8: 126-134 Santini A & Faccoli M - iForest 8: 126-134 tal conditions (Banfield 1941, 1968, Pomer- gesting that early flushing is a mechanism of elm bark beetle species must be better de- leau 1965, 1968, Neely 1968, 1970, Smalley DED avoidance based on asynchrony be- fined by sequencing specific regions of the 1963, Tchernoff 1965, Smalley & Kais tween maximum susceptibility period and in- DNA in phylogenetic studies, to provide a 1966, Santini et al. 2005a, Solla et al. oculation time (Santini et al. 2005a). correct identification of the Scolytus species, 2005a). According to studies correlating sus- Variations in tree susceptibility related to as already done with other scolytid genera ceptibility to O. ulmi s.l. with seasonal host different growth rhythms, caused by either (Chang et al. 2014). Genetic improvement phenology (Pomerleau 1965, Neely 1968, seasons or differences in elm populations or programs are also required on the host trees 1970, Takai & Kondo 1979, Solla et al. clones (Sutherland & Brasier 1997), fit well aiming to select new European elm clones 2005a, Santini & Ghelardini, unpublished with the growth-differentiation balance hy- with higher levels of DED resistance, based, data), the period of highest susceptibility co- pothesis (Herms & Mattson 1992). This hy- for instance, on the bud-burst precocity incides with the seasonal maximum growth pothesis provides a framework for predicting (Santini et al. 2005a). This resistance could rate, recorded at the beginning of leaf expan- how plants balance resource allocation be- be exploited by specific studies exploring sion and formation of large spring xylem tween differentiation-related processes and how different climatic conditions affect bud- vessels, all genotype-dependent characters. growth-related processes over a range of en- burst date and growth rhythm, and the natu- The decrease in susceptibility observed from vironmental conditions, as it is known that ral history (i.e., phenology and voltinism) of spring to late summer is also correlated to resources cannot be allocated to both func- Scolytus spp. (Ghelardini & Santini 2009). the seasonal changes in wood anatomy, i.e., tions simultaneously (Lorio 1986). Resource Early flushing European elm clones could be the transition from early wood, characterized availability is high in spring, when favorable selected to obtain elms avoiding natural in- by large vessel elements, to late wood, made temperatures are combined with plentiful fection through an asynchrony between host up of smaller cells with thicker cell walls water supply, a condition lasting for a short and insect phenology, both of which are re- (Pope 1943, Solla et al. 2005a). Pathogen time in the Mediterranean climate until the gulated by temperature (Sinclair & Campana development is, hence, highly dependent on early, hot and dry summer occurs. At this 1978, Sengonca & Leisse 1984, Ghelardini the host’s seasonal morphogenesis and cam- time of the year, elm energy reserves are al- et al. 2010). Although many studies were bial activity, as well as on the pattern of lon- ready exhausted by the flowering process conducted to select elm species and clones gitudinal and radial growth of the host plant. that occurs in late winter, and by the con- resistant to O. ulmi s.l. (Smalley & Guries Because efficient wood compartmentaliza- struction of the new porous ring, which has 2000, Mittempergher & Santini 2004), no ef- tion forces the plant to keep building new to provide nutrients for the expanding photo- fort was made to identify mechanisms of barriers, which limit the accessibility of its synthetic surfaces. Growing meristems beha- combined resistance to both DED and elm own reserves in the stem (Bonsen et al. ve as strong photosynthetic sinks, provisio- bark beetles. Concerning pathogens, consi- 1985), the highest susceptibility occurs with ned by carbon sources that include neighbo- derable progress has been made in genetic low energy reserves, high growth rate, not ring mature leaves (Marcelis 1996) and also and systematic knowledge of the Ophio- fully efficient photosynthesis and large ves- newly formed leaves. No resources are dedi- stoma species associated with elm bark bee- sels (Ghelardini & Santini 2009). Since plant cated to defense, which make elms especially tles (Kirisits 2013). The significance of the physiological processes are seasonally regu- susceptible to DED during spring, exactly in association, however, is still matter of dis- lated, and elms are exposed to fungus inocu- the period of the vector’s inoculative phase. cussion, especially regarding the role of lation only in a transitory and short phase of As time passes, resource availability and fungi - and spore load carried by the beetles the vector life history (twig-crotch feeding growth rate decrease so that photosynthates - in exhausting tree defenses, the relations phase), the infection will occur only if insect can be allocated to differentiation. This between fungus pathogenicity and beetle ag- feeding phase and time of host susceptibility process could explain why inoculations by gressiveness, and their role in the tree killing overlap. Thus, an asynchrony between these the second beetle generation in summer - process. phenological phases may allow trees to which furthermore accounts for a lower per- There have been very few morphological avoid infection, representing a particular centage of vectors (Faccoli & Battisti 1997) studies on the Ulmus-Ophiostoma-Scolytus form of disease-escape resistance. For in- - is less effective or totally ineffective in system. Concerning insects, the structure and stance, although inoculated in the same day pathogen transmission compared to the first ultra-structure of the mycangia or mycetan- in central Italy, southern European clones of generation in spring. Because in early-flush- gia on the bark beetle tegument was deeply U. minor showed fewer disease symptoms ing elms these phenological and physiologi- investigated in the past (Francke-Grosmann than northern ones, with a significant direct cal events occur earlier in spring, the emerg- 1956a, 1956b, 1963a, 1963b, 1967, Batra relationship between disease severity and ing beetles will feed on trees having already 1963, Beaver 1989, Berryman 1989, Lévieux bud burst date (Santini et al. 2005a). As mature leaves able to allocate carbohydrates et al. 1991), but not specifically in the Scoly- southern clones cultivated in central Italy to secondary metabolism, and therefore bet- tus species except for a few preliminary ob- flushed significantly earlier than northern ter defend against pathogen infections. In servations (Faccoli 1995). The host-patho- ones (Ghelardini et al. 2006), this suggests this period early-flushing elms are also al- gen interactions leading to DED symptoms that, at the inoculation date, the southern ready producing latewood that, being consti- were recently analyzed in vitro by histo- and clones had already passed the period of ma- tuted of small and scattered vessels with a cyto-chemical tests. Callus cultures of sus- ximum susceptibility, which for European greater proportion of fibers, is less suitable ceptible U. americana were inoculated with elms begins 40-50 days after bud burst and for spore diffusion. the highly aggressive pathogen O. novo- lasts for a number of days related to environ- ulmi. Inoculated callus tissues were then mental conditions and genotype (Tchernoff Challenges for the nearby future compared with water-treated callus tissues 1965, Smalley & Kais 1966, Santini & Ghe- Although we are learning much about in- using TEM and SEM light microscopy. New lardini, unpublished data). Southern clones sect-pathogen interactions and transmission aspects of these interactions were described, completed the formation of the large spring mechanisms, many topics still deserve addi- including histological observations - for the vessels and the production of latewood early, tional attention. first time in plant callus cultures - on sube- reducing their risk of infection (Pope 1943, The systematic of species belonging to the rin, with its typical lamellar structure, and Solla et al. 2005a, Santini & Ghelardini, un- genus Scolytus is one of the most complica- the intracellular presence of O. novo-ulmi published data). These studies provided new ted amongst bark beetles (Michalski 1973, (Aoun et al. 2009). Other SEM applications information on susceptibility to DED, sug- Pfeffer 1995). The systematic position of were the description of the typical tyloses in-

iForest 8: 126-134 129 © SISEF http://www.sisef.it/iforest/ Ophiostoma ulmi and Scolytus spp. association duced by the pathogen within the spring ves- modern researches. Characterizing the phy- to the accidental introduction of new vector sels of infected elms, or the tissue invasion siological status of trees in relation to their species, or new highly pathogenic strains, or process operated by blastoconidia (Elgersma susceptibility is also needed prior to building new highly susceptible elm species in gar- 1973, Elgersma & Heybroek 1979). How- risk prediction models in non-epidemic dens and public parks. Introductions of new ever, the studies were limited to a simple de- areas, such as Northern Europe and America. pathogens or vectors, for instance, may lead scription of the host reactions to pathogen What will the responses be of elms, DED to new and unexpected associations, able to attacks, and did not investigate the structure and elm bark beetles to increasing tempera- increase the fitness of both organisms with of the reaction tissues. tures? In U. minor a large intra-specific va- tremendous consequences for the host popu- Chemical communication is of crucial im- riation in timing of bud burst was found to lations, as recorded in other insect-fungus portance to manage insect populations, DED be mainly dependent on geographic origin. associations (Battisti et al. 1999, Luchi et al. epidemics and their damage to elms. Gaps in The bud burst date was directly related to 2012). our knowledge concern, for instance, the se- latitude and altitude, i.e., temperature, with a lection mechanisms driving callow adult greater chilling requirement for dormancy in Conclusion beetles in the plant choice for maturation northern areas or highlands than in southern The processes that regulate the current bee- feeding. In this phase, tree attractiveness to or lowlands (Ghelardini et al. 2006). It can tle-fungus symbiosis remain poorly under- elm bark beetles is of primary importance for be hypothesized, for instance, that under cli- stood. The relationships between elm bark a susceptible plant to be infected by O. ulmi mate warming European elms would start to beetles and O. ulmi s.l. depend on several s.l. Therefore, once the chemical attractant flush earlier in most parts of their natural factors, such as the climatic and environment has been identified a specific marker assisted range, maybe escaping the pathogen infec- characteristics, and the interactions between tree-breeding program may be developed for tion (Santini et al. 2004, Ghelardini et al. the components of the biotic community, in- both native European and American elm 2010), but how the insect phenology will cluding, for example, the d-factor, a citoplas- species. Such a tree-breeding strategy would change in front to a warmer climate? The mically transmitted virus disease of Ophio- avoid the use of Asian species as source of few models describing the population dyna- stoma ulmi s.l. (Brasier 1983). Commonly to resistance, as they could become invasive, mics of pathogen and insects consider clima- other bark beetle-fungus symbiosis, all these posing a threat to the native biodiversity (Za- tic conditions only marginally. They are ge- factors play important roles in determining lapa et al. 2009, Brunet et al. 2013). nerally never focused on changing environ- composition, fidelity and longevity of the as- Because the number of papers published on ments, nor on the prediction of future im- sociation between beetles and DED fungi different Scolytus species is directly related pacts in new areas or on new elm species, as (Six 2012). to the economic importance of the organi- recently observed in Colorado following the Insects play a role of primary concern in sms, only biology and ecology of the most introduction of the banded elm bark beetle, transmitting diseases to elms, like for in- harmful species were investigated, while ve- S. schevyrewi Semenov from Siberia (Jacobi stance several species of leaf-hoppers identi- ry little is known about the less common et al. 2007). Studied carried out at larger ge- fied as vectors of the elm yellow phyto- species - such as S. laevis, S. sulcifrons and ographic scale should hence lead to more dy- plasma (Carraro et al. 2004). S. triarmatus - which, however, are recently namic models. There are thus several aspects that still de- showing an increasing importance as DED Some factors suspected to be of seconda- serve to be studied for a better understanding vectors. There is hence a dramatic lack of ry importance in the epidemic dynamics of of the pathogen-insect interactions. In ad- detailed information on less damaging spe- DED were in the past largely underestima- dressing these issues, a holistic approach is cies, although it would be very useful for ted. The case of natural enemies of the elm highly recommended, taking into account all comparison and generalization, and would bark beetles should be, for instance, valuable the many factors affecting pathogen trans- certainly also lead to a better understanding for further research. Similarly, apart a few mission and disease spread. of the reasons for the aggressiveness of the studies concerning the unattractiveness of U. dangerous species. There is, therefore, a wi- laevis toward the Scolytus beetles (Sacchetti References de and regrettable gap in our knowledge et al. 1990), neither the effects of intra- and Agrios GN (1988). Plant diseases caused by fungi. concerning secondary, or less common, Sco- inter-specific variations in the nutritional In: “Plant Pathology”. Academic Press, S. Diego, lytus species. quality of elms nor the tree constitutive de- CA, USA, pp. 265-509. Research is also needed about the environ- fenses against elm bark beetles were consi- Aoun M, Rioux D, Simard M, Bernier L (2009). mental factors affecting elm bark beetles and dered. Research on genetic variations in bee- Fungal colonization and host defense reactions pathogen performance and their adaptation tle/pathogen populations, especially by com- in Ulmus americana callus cultures inoculated to new and changing environments, especial- paring endemic and epidemic areas, should with Ophiostoma novo-ulmi. Phytopathology 99: ly in relation to global change. New prob- also provide very useful information on their 642-650. - doi: 10.1094/PHYTO-99-6-0642 lems can emerge from climate change that role in epidemic dynamics. Moreover, the Balachowsky A (1949). Faune de France n° 50: modify the geographic distributions of pests, possible occurrence and importance of trans- Coléoptères Scolytides. Libraire de la Faculté des pathogen and hosts. Although the northward mission mechanisms different than those due Sciences, Lechevalier, Paris, France, pp. 320. [in and upward spread of both DED epidemics to elm bark beetle maturation feeding or the French] and some Scolytus species (e.g., S. multistri- occurrence of other possible vectors were in- Banfield WM (1941). Distribution by the sap atus in southern Sweden (Faccoli 2003, pers. completely explored (Covassi & Masutti stream of spores of three fungi that induce vas- obs., - or at higher altitudes on Apennines, 1980). For instance, the high efficiency of S. cular wilt diseases of elm. Journal of Agricultural Pecori et al. 2013) was recently associated to scolytus in spreading DED was recently sug- Research 62: 637-681. global warming, considerable knowledge gested to be partly due to its association with Banfield WM (1968). Dutch elm disease recur- gaps exist regarding the effects of these fac- two mites, Proctolaelaps scolyti Evans and rence and recovery in American elm. Phytopa- tors on insect aggressiveness and fungus Tarsonemus crassus (Schaarschmidt), and thologische Zeitschrift 62: 21-60. - doi: 10.1111/ pathogenicity in both Europe and North the hyperphoretic spores of O. novo-ulmi j.1439-0434.1968.tb02345.x America. Very little information is also avai- they carry (Moser et al. 2010). Another chal- Basset Y, Favaro A, Springate ND, Battisti A lable regarding the relations between global lenge concerns the emergence of new pro- (1992). Observations on the relative effective- change and tree resistance, although this to- blems resulting from the rapid increase of in- ness of Scolytus multistriatus (Marsham) and pic represents a considerable component of ternational trade among continents, leading Scolytus pygmaeus (Fabricius) (Coleoptera, Sco-

lytidae) as vectors of the Dutch Elm Disease. as subspecies: their perithecial size differences Ceratocystis ulmi. Netherlands Journal of Plant Bulletin de la Société Entomologique Suisse 65: and geographical distributions. Mycological Re- Pathology 76: 179-182 - doi: 10.1007/BF01974 61-67. search 105: 547-554. - doi: 10.1017/S0953756 328 Batra LR (1963). Ecology of ambrosia fungi and 201004087 Elgersma DM (1973). Tylose formation in elms their dissemination by beetles. Transactions of Brasier CM, Kirk SA (2010). Rapid emergence of after inoculation with Ceratocystis ulmi, a possi- the Kansas Academy of Science 66: 213-236. - hybrids between the two subspecies of Ophiosto- ble resistance mechanism. Netherlands Journal doi: 10.2307/3626562 ma novo-ulmi with a high level of pathogenic fit- of Plant Pathology 79: 218-220. - doi: 10.1007/ Battisti A, Favaro A, Faccoli M, Masutti L (1994). ness. Plant Pathology 59: 186-199. - doi: 10.11 BF01974237 Suscettibilità dei ceppi di Ulmus sp. all’attacco 11/j.1365-3059.2009.02157.x Elgersma DM (1982). Susceptibility and possible primario di Scolytus sp.pl. (Coleoptera, Scolyti- Brasier CM, Mehrotra MD (1995). Ophiostoma mechanisms of resistance to Dutch elm disease. dae) [Susceptibility of Ulmus species to primary himal-ulmi sp. nov., a new species of Dutch elm In: Proceedings of the “Dutch elm disease sym- infestation of Scolytus species (Coleoptera, Sco- disease fungus endemic to the Himalayas. Myco- posium and workshop” (Kondo ES, Hiratsuka Y, lytidae)]. In: “Innovazioni e Prospettive nella Di- logical Research 99: 205-215. - doi: 10.1016/S Denyer WBG eds). Winnipeg (Canada) 5-9 Oc- fesa Fitosanitaria” (Istituto Sperimentale di Pato- 0953-7562(09)80887-3 tober 1981, pp. 169-177. logia Vegetale, Roma). Convegno MiRAAF, Fer- Brunet J, Zalapa JE, Pecori F, Santini A (2013). Elgersma DM, Heybroek HM (1979). Spread and rara, Italy, pp. 351-354. [in Italian] Hybridization and introgression between the exo- survival of an aggressive and a non-aggressive Battisti A, Roques A, Colombari F, Frigimelica G, tic Siberian elm, Ulmus pumila, and the native strain of Ophiostoma ulmi in elms. Netherlands Guido M (1999). Efficient transmission of an in- Field elm, U. minor, in Italy. Biological Inva- Journal of Plant Pathology 85: 235-240. - doi: troduced pathogen via an ancient insect-fungus sions 15: 2717-2730 - doi: 10.1007/s10530-013- 10.1007/BF01977595 association. Naturwissenschaften 86: 479-483. - 0486-z Et-Touil A, Rioux D, Mathieu FM, Bernier L doi: 10.1007/s001140050658 Buisman C (1932). De olmen- of iepenziekte [The (2005). External symptoms and histopathological Beaver RA (1989). Insect-Fungus Relationships in elms and elm disease]. Dirix-Van Riet K, Ant- changes following inoculation of elms putatively the Bark and Ambrosia Beetles. In: Proceedings werpen, Belgium, pp. 15. [in Dutch] resistant to Dutch elm disease with genetically of the 14th Symposium of the Royal Entomologi- Burdekin D (1979). Beetle and fungus: the unholy close strains of Ophiostoma. Canadian Journal of cal Society of London / British Mycological So- alliance. Heinemann, London, UK, pp. 65-79. Botany 83: 656-667. - doi: 10.1139/b05-037 ciety “Insect-Fungus Interactions” (Wilding N, Carraro L, Ferrini F, Ermacora P, Loi N, Martini Ewers FW, Fisher JB, Chiu ST (1990). A survey Collins NM, Hammond PM, Webber JF eds). M, Osler R (2004). Macropsis mendax as a vec- of vessel dimensions in stems of tropical lianas Academic Press, London, UK, pp. 121-143. tor of elm yellows phytoplasma of Ulmus spe- and other growth forms. Oecologia 84: 544-552. Berryman AA (1989). Adaptive pathways in sco- cies. Plant Pathology 53: 90-95. - doi: 10.1111/ - doi: 10.1007/BF00328172 lytid-fungus associations. In: Proceedings of the j.1365-3059.2004.00940.x Faccoli M (1995). Coleotteri scolitidi e grafiosi 14th Symposium of the Royal Entomological So- Chang H, Liu Q, Hao D, Liu Y, An Y, Qian L, dell’olmo. Prove di controllo combinato [Elm ciety of London / British Mycological Society Yang X (2014). DNA barcodes and molecular bark beetles and the Dutch elm disease: trials of “Insect-Fungus Interactions” (Wilding N, Collins diagnostics for distinguishing introduced Xyle- combined control]. Master thesis in Forest Sci- NM, Hammond PM, Webber JF eds) . Academic borus (Coleoptera: Scolytinae) species in China. ences, University of Padua, Italy, pp. 79. [in Ita- Press, London, UK, pp. 145-160 Mitochondrial DNA 25: 63-69. - doi: 10.3109/ lian] Betrem JG (1929). De iepenziekte en de iepen- 19401736.2013.779260 Faccoli M (2001). Elm bark beetles and Dutch spintkevers [The elm disease and elm bark bee- Chapman JW (1910). The introduction of an Eu- elm disease: tests of combined control. Journal tles]. Tijdschr Plantenziekten 35: 272-289. [in ropean scolytid, the smaller bark beetle, Scolytus of Pest Science 74: 22-29. - doi: 10.1046/j.1439- Dutch] - doi: 10.1007/BF02810222 multistriatus (Marsham) into Massachusetts. 0280.2001.00033.x Bonsen KJM, Scheffer RJ, Elgersma DM (1985). Psyche 17: 63-68. - doi: 10.1155/1910/ 76129 Faccoli M (2004). Scolytus scolytus (F.). In: Barrier zone formation as a resistance mecha- Collins CW, Buchanan WD, Witten RR, Hoffman “Crop Protection Compendium 2004 Edition”. nism of elms to Dutch elm disease. IAWA Bul- CH (1936). Bark beetles and other possible in- CAB International, Wallingford, UK, CD-ROM. letin 6: 71-77. - doi: 10.1163/22941932-90000 sect vectors of Dutch elm disease Ceratostomel- Faccoli M, Battisti A (1997). Observations on the 916 la ulmi (Schwarz) Buisman. Journal of Econo- transmission of Ophiostoma ulmi by the Smaller Brasier CM (1979). Dual origin of recent Dutch mic Entomology 29: 169-176. Elm Bark Beetles (Scolytus spp.). In: Proceeding Elm disease outbreaks in Europe. Nature 281: Covassi M, Masutti L (1980). Generalità sull’en- of the IUFRO meeting “Integrating cultural tac- 78-79. - doi: 10.1038/281078a0 tomofauna degli olmi con particolare riguardo ai tics into the management of bark beetles and re- Brasier CM (1983). A citoplasmically transmitted coleotteri scolitidi vettori della grafiosi [Review forestation pest”. Vallombrosa (Italy) 1-4 Sep disease of Ceratocystis ulmi. Nature 305: 220- of the elm entomofauna with particular regard to 1996. General Technical Report NE-236, USDA 223. - doi: 10.1038/305220a0 bark beetles vectors of DED]. Informatore Fito- Forest Service, pp. 172-176. Brasier CM (1990). China and the origins of Dut- patologico 30: 19-26. [in Italian] Faccoli M, Zanocco D, Battisti A, Masutti L ch elm disease: an appraisal. Plant Pathology 39: Della Beffa G (1949). Gli insetti dannosi all’agri- (1998). Chiave semplificata per la determina- 5-16. - doi: 10.1111/j.1365-3059.1990.tb0247 coltura e i moderni mezzi e metodi di lotta [The zione degli Scolytus Geoffroy (Coleoptera Scoly- 0.x insects harmful to agriculture and the modern tidae) italiani viventi sugli olmi [Morphological Brasier CM (1991). Ophiostoma novo-ulmi sp. control means and methods]. Hoepli, Milano, key for determination of the Italian elm bark bee- nov., causative agent of current Dutch elm disea- Italy, pp. 978. [in Italian] tles of the genus Scolytus Geoffroy (Coleoptera se pandemics. Mycopathologia 115: 151-161. - Duchesne LC, Jeng RS, Hubbes M (1985). Accu- Scolytidae)]. Redia 81: 183-197. [in Italian] doi: 10.1007/BF00462219 mulation of phytoalexins in Ulmus americana in Favaro A, Battisti A (1993). Observations on the Brasier CM (2000). Intercontinental spread and response to infection by a nonaggressive strain of elm bark beetle Scolytus pygmaeus (Fabricius) continuing evolution of the Dutch elm disease Ophiostoma ulmi. Canadian Journal of Botany (Coleoptera, Scolytidae) as possible vector of the pathogens. In: “The elms: breeding, conservation 63: 678-680. - doi: 10.1139/b85-086 fungus Ophiostoma ulmi (Schwarz) Nannfeld. and disease management” (Dunn CP ed). Kluwer Dunn CP (2000). The elms: breeding, conserva- Redia 76: 459-466. Academic Publishers, Dordrecht, The Nether- tion and disease management. Kluwer Academic Francke-Grosmann H (1956a). Hautdrüsen als lands. pp. 61-72. Publishers, Boston, USA, pp. 228. Träger der Pilzsymbiose bei Ambrosiakäfern Brasier CM, Kirk SA (2001). Designation of the Elgersma DM (1970). Length and diameter of [Mycangia as carriers of the fungus symbiosis EAN and NAN races of Ophiostoma novo-ulmi xylem vessels as a factors in resistance of elms to with ambrosia beetles]. Zeitschrift für Morpholo-

iForest 8: 126-134 131 © SISEF http://www.sisef.it/iforest/ Ophiostoma ulmi and Scolytus spp. association

gie und Ökologie der Tiere 45: 275-308. [in Ger- tween cultural characters and pathogenicity in beetle, Ips sexdentatus Boerner: ultrastructure of man] - doi: 10.1007/BF00430256 Ceratocystis ulmi from Britain, Europe and a mycangium. Canadian Entomologist 123: 245- Francke-Grosmann H (1956b). Grundlagen der North America. Nature 241: 381-383. - doi: 254. - doi: 10.4039/Ent123245-2 Symbiose bei pilzzüchtenden Holzinsekten [Ba- 10.1038/241381a0 Lorio PL (1986). Growth-differentiation balance sics of symbiosis with fungus-growing wood in- Gibbs JN, Smith ME (1978). Antagonism during provides a basis for understanding southern pine sects]. Verhandlungen der Deutschen Zoologi- the saprophytic phase of the life cycles of two beetle-tree interactions. Forest Ecology and Ma- schen Gesellschaft Hamburg, Leipzig, Germany, pathogens of woody host - Heterobasidium an- nagement 14: 259-273. - doi: 10.1016/0378-112 pp. 112-118. [in German] nosum and Ceratocystis ulmi. Annals of Applied 7(86)90172-6 Francke-Grosmann H (1963a). Some new aspects Biology 89: 125-128. - doi: 10.1111/j.1744-73 Lunderstadt J, Rohde M (1993). Biologie, Ausbre- in forest entomology. Annual Review of Ento- 48.1978.tb02586.x itungsstrategie und Bekampfungsmoglichkeiten mology 8: 415-438. - doi: 10.1146/annurev.en. Goidanich G (1936). La moria dell’olmo (Gra- der Ulmensplintkafer [Biology, dispersal strategy 08.010163.002215 phium ulmi) [The elm disease (Graphium ulmi)]. and possible fungus acquisition of the elm bark Francke-Grosmann H (1963b). Zur Übertragung Reda, Roma, Italy, pp 124. [in Italian] beetles]. Hessische Forstliche Versuchsanstalt, der Pilzflora bei dem Borkenkäfer Ips acumina- Goidanich A, Goidanich G (1937). Moria degli Hann Munden 16: 26-29. [in German] tus [Transfer of the fungal flora in the bark bee- olmi e scolitidi [Elm decline and bark beetles]. Luchi N, Mancini V, Feducci M, Santini A, Ca- tle Ips acuminatus]. Zeitschrift für Angewandte Italia Agricola 71: 941-948. [in Italian] pretti P (2012). Leptoglossus occidentalis and Entomologie 52: 355-361. [in German] - doi: Guries RP (2001). Elms: past, present, and future. Diplodia pinea: a new insect-fungus association 10.1111/j.1439-0418.1963.tb02 046.x In: Proceeding of the “National conference on in Mediterranean forests. Forest Pathology 42: Francke-Grosmann H (1967). Ectosymbiosis in wilt diseases of shade trees” (Ash CL ed). St. 246-251. - doi: 10.1111/j.1439-0329.2011.007 wood inhabiting insects. In: “Symbiosis. Asso- Paul (MN, USA) August 1999. APS Press, USA, 50.x ciations of invertebrates, birds, ruminants and pp. 29-36. MacHardy WE, Beckman CH (1973). Water rela- other biota (vol. 2)” (Henry SH ed). Academic Herms DA, Mattson WJ (1992). The dilemma of tions in American elm infected with Ceratocys- Press, New York, USA, pp. 141-205. plants - To grow or defend. Quarterly Review of tis ulmi. Phytopathology 63: 98-103. - doi: 10.10 Fransen JJ (1931). Enkele gegevens omtrent de Biology 67: 283-335. - doi: 10.1086/417659 94/Phyto-63-98 verspreiding van de door Graphium ulmi Heybroek HM, Elgersma DM, Scheffer RJ (1982). Manojlovic B, Sivcev I (1995). The effect of elm Schwarz veroorzaakte iepenziekte door de iepen- Dutch elm disease: an ecological accident. Out- bark thickness on Scolytus scolytus (F.) (Cole- spintkevers, Eccoptogaster (Scolytus) scolytus F. look on Agriculture 11: 1-9. optera: Scolytidae) growth in laboratory condi- en Eccoptogaster (Scolytus) multistriatus Marsh. Jacobi WR, Koski RD, Harrington TC, Witcosky tions. Zastita Bilja 46: 35-42. [online] URL: in verband met de bestijding dezer ziekte [Com- JJ (2007). Association of Ophiostoma novo-ulmi http://www.cabdirect.org/abstracts/19961100386 paring some data about spreading of Graphium with Scolytus schevyrewi (Scolytidae) in Colora- .html ulmi Schwarz elm disease caused by the elm do. Plant Disease 91: 245-247. - doi: 10.1094/ Marcelis LFM (1996). Sink strength as a determi- bark beetles, Eccoptogaster (Scolytus) Scolytus PDIS-91-3-0245 nant of dry matter partitioning in the whole F. and Eccoptogaster (Scolytus) multistriatus Jacot AP (1934). Acarina as possible vector of the plant. Journal of Experimental Botany 47: 1281- Marsh. in connection with this disease]. Tijd- Dutch elm disease. Journal of Economic Ento- 1291. - doi: 10.1093/jxb/47.Special_Issue.1281 schrift over Plantenziekten 37: 49-62. [in Dutch] mology 27: 858-859. Marchal E (1927). Rapport sur les résultats des Fransen JJ (1939). Iepenziekte, iepenspintkevers Jacot AP (1936). Three possible mites vector of recherches effectuées à la station de Phytopatolo- en beider bestrijding [Elm disease, elm bark bee- the Dutch elm disease. Entomological Society of gie de l’Etat à Gembloux sur la maladie de tles and their control]. Veenman and Zonen, Wa- America 29: 627-635. l’orme [Report on the research results of the geningen, The Netherland, pp. 118. [in Dutch] Jeng RS, Alfenas AC, Hubbes M, Dumas MT Plant Pathology State Station of Gembloux's Fransen JJ, Buisman C (1935). Infectieproeven op (1983). Presence and accumulation of fungitoxic about elm disease]. Forestière de Belgique 35: verschillende iepensoorten met behulp van de substances against Ceratocystis ulmi in Ulmus 162-164. [in French] iepenspintkever [Experiments on different spe- americana: possible relation to induced resistan- Martín JA, Solla A, Esteban LG, de Palacios P, cies of elm with the bark beetles]. Tijdschrift ce. European Journal of Forest Pathology 13: Gil L (2009). Bordered pit and ray morphology over Plantenziekten 41: 221-239. [in Dutch] 239-244. - doi: 10.1111/j.1439-0329.1983.tb00 involvement in elm resistance to Ophiostoma Ghelardini L, Santini A (2009). Avoidance by ea- 124.x novo-ulmi. Canadian Journal of Forest Research rly flushing: a new perspective on Dutch elm di- Kirisits T (2013). Dutch elm disease and other 39: 420-429. - doi: 10.1139/X08-183 sease research. iForest 2: 143-153. - doi: 10.383 Ophiostoma diseases. In: “Infectious forest di- Martin JA, Solla A, Ruiz-Villar M, Gil L (2013). 2/ifor0508-002 seases” (Gonthier P, Nicolotti G eds). CABI, Vessel length and conductivity of Ulmus bran- Ghelardini L, Falusi M, Santini A (2006). Varia- Wallingford, UK, pp. 256-282. ches: ontogenetic changes and relation to resi- tion in timing of bud-burst of Ulmus minor Kletecka Z (1996). The xylophagus beetles (In- stance to Dutch elm disease. Trees 27: 1239- clones from different geographical origins. Cana- secta, Coleoptera) community and its succession 1248. - doi: 10.1007/s00468-013-0872-2 dian Journal of Forest Research 36: 1982-1991. - on Scotch elm (Ulmus glabra) branches. Biolo- McNabb HS, Heybroek HM, McDonald WL doi: 10.1139/x06-092 gia 51: 143-152. [online] URL: http://www.cab- (1970). Anatomical factors in resistance to Dut- Ghelardini L, Santini A, Black-Samuelsson S, direct.org/abstracts/19971100241.html ch elm disease. Netherland Journal of Plant Pa- Myking T, Falusi M (2010). Bud dormancy re- Lanier GN, Peacock JW (1981). Vectors of the thology 76: 196-204. - doi: 10.1007/BF01974 lease in elm (Ulmus spp.) clones - a case study of pathogen. In: “Compendium of elm diseases” 331 photoperiod and temperature responses. Tree (Stipes RJ, Campana RJ eds). The American Meyer HJ, Norris DM (1967). Vanillin and sy- Physiology 30: 264-274. - doi: 10.1093/treephys/ Phytopathological Society, St. Paul, MN, USA, ringaldehyde as attractants for Scolytus multis- tpp110 pp. 14-16. triatus (Coleoptera: Scolytidae). Annals of the Gibbs JN (1974). Biology of Dutch elm disease Lea T (1977). A comparison of the saprophitic Entomological Society of America 60: 858-859. Ceratocystsi ulmi. Forest Record 94: 1- 9. and parasitic stages of Ceratocystis ulmi. Ph.D. [online] URL: http://www.ingentaconnect.com/ Gibbs JN (1978). Intercontinental epidemiology of Thesis, University of London, London, UK, pp. content/esa/aesa/1967/00000060/00000004/art0 Dutch elm disease. Annual Review of Phytopa- 77. 0024 thology 16: 287-307. - doi: 10.1146/annurev.py. Lévieux J, Cassier P, Guillaumin D, Roques A Michalski J (1973). Revision of the paleartic spe- 16.090178.001443 (1991). Structures implicated in the transporta- cies of the Scolytus Geoffroy (Coleoptera, Gibbs JN, Brasier CM (1973). Correlation be- tion of pathogenic fungi by the European bark Scolytidae). Panstwowe Wydawnictwo

Naukowe, Warszava, Krakow, Poland, pp. 214. (2013). Monitoring Wych elm population in sou- pean elms. In: Proceedings of the 2nd Internatio- Mittempergher L (1989). Il declino dell’olmo: da thern Apennines. In: Proceedings of the “3rd In- nal Elm Conference “New approaches to elm latifoglia nobile a cespuglio [The elm decline: ternational Elm Conference. The elm after 10 conservation”. Valsaìn (Spain) 20-23 May 2003. from tree to shrub]. Annali Accademia Italiana years of Dutch elm disease” (Manzo R ed). Flo- Investigatión Agraria: Sistemas y Recursos Fore- Scienze Forestali 38: 585-609. rence (Italy) 9-11 October 2013. IPP-CNR, Flo- stales 13: 37-45. [online] URL: http://revistas. Mittempergher L, Santini A (2004). The history of rence, Italy, pp. 40. [online] URL: http:// inia.es/index.php/fs/article/view/811 elm breeding. Investigación agraria: Sistemas y elm2013.ipp.cnr.it/downloads/book_of_abstract- Santini A, Montaghi A, Vendramin GG, Capretti Recursos Forestales 13: 161-177. [online] URL: s.pdf P (2005b). Analysis of the Italian Dutch elm di- http://revistas.inia.es/index.php/fs/article/view/8 Pfeffer A (1995). Zentral- und westpaläarktische sease population. Journal of Phytopathology 153: 21 Borken- und Kernkäfer (Coleoptera: Scolytidae, 73-79. - doi: 10.1111/j.1439-0434.2004.00931.x Moser JC, Konrad H, Blomquist SR, Kirisits T Platypodidae) [Central and Western Palearctic Schwarz MB (1922). The twig vascular disease of (2010). Do mites phoretic on elm bark beetles Bark and Ambrosia beetles (Coleoptera: Scoly- the elm. Das Zweig-sterben der Ulmen, Trauer- contribute to the transmission of Dutch elm di- tidae, Platypodidae)]. Pro Entomologica, Natur- weiden und Pfirsichbaume [The twig vascular sease? Naturwissenschaften 97: 219-227 - doi: historisches Museum Basel, Switzerland, pp. disease of the elm, willows and peach trees]. 10.1007/s00114-009-0630-x 310. Medelingen uit het Phytopathologisch laborato- Neely D (1968). Twig inoculations on American Pomerleau R (1965). The period of susceptibility rium Willie Commelin Scholten 5: 1-73. [in Ger- elm with Ceratocystis ulmi. Phytopathology 58: of Ulmus americana to Ceratocystis ulmi under man] 1566-1570. conditions prevailing in Quebec. Canadian Jour- Sengonca C, Leisse N (1984). Bedeutung der Neely D (1970). Dutch elm disease symptom pro- nal of Botany 43: 787-792. - doi: 10.1139/b65- Borkenkafer (Col., Scolytidae) bei der Verbrei- gression. Plant Disease Report 54: 127-129. 089 tung des Erregers der Hollandischen Ulmenkran- Newbanks D, Bosh A, Zimmermann MH (1983). Pomerleau R (1968). Progression et localisation kheit im Raum Euskirchen [Importance of bark Evidence for xylem dysfunction by embolization de l’infection par le Ceratocystis ulmi dans l’or- beetles (Col., Scolytidae) in the dissemination in Dutch elm disease. Phytopatology 73: 1060- me d’Amérique [Progression and localization of the causal agent of the Dutch-Indian elm disease 1063. - doi: 10.1094/Phyto-73-1060 the infection by Ceratocystis ulmi in the Ameri- in the area of Euskirchen]. Journal of Applied Ouellette GB, Rioux D (1992). Anatomical and can elm]. Phytopathologische Zeitschrift 63: Entomology 98: 413-423. [in German] physiological aspects of resistance to Dutch elm 301-327. [in French] - doi: 10.1111/j.1439- Shigo AL (1982). Dutch elm disease: a CODIT disease. In: “Defense mechanisms in woody 0434.1968.tb02396.x perspective. In: Proceedings of the “Dutch elm plants against fungi” (Blanchette A, Biggs R Pope SA (1943). Some studies on the Dutch elm disease symposium and workshop” (Kondo ES, eds). Springer-Verlag, Berlin, Germany, pp. 257- disease and the causal organism. Doctoral The- Hiratsuka Y, Denyer WBG eds). Winnipeg 305. sis, Cornell University, Ithaca, NY, USA, pp. 66. (Canada) 5-9 October 1981, pp. 151-168. Ouellette GB, Rioux D, Simard M, Cherif M Rioux D, Ouellette GB (1991a). Barrier zone for- Shigo AL, Tippet JT (1981). Compartmentaliza- (2004a). Ultrastructural and cytochemical stu- mation in host and nonhost trees inoculated with tion of America elm tissues infected with Cera- dies of host and pathogens in some fungal wilt Ophiostoma ulmi. I. Anatomy and histochem- tocystis ulmi. Plant Disease 65: 715-718. - doi: diseases: retro- and introspection towards a bet- istry. Canadian Journal of Botany 69: 2055- 10.1094/PD-65-715 ter understanding. Investigación agraria: Sis- 2073. - doi: 10.1139/b91-258 Sinclair WA, Campana RJ (1978). Dutch elm dis- temas y Recursos Forestales 13: 119-145. [on- Rioux D, Ouellette GB (1991b). Barrier zone for- ease: perspectives after 60 years. Plant Pathology line] URL: http://revistas.inia.es/index.php/fs/ mation in host and nonhost trees inoculated with 1: 5-52. [online] URL: http://www.cabdirect.org/ article/view/819 Ophiostoma ulmi. II. Ultrastructure. Canadian abstracts/19800671247.html Ouellette GB, Rioux D, Simard M, Chamberland Journal of Botany 69: 2074-2083. - doi: 10.113 Sinclair WA, Zahand JP, Melching JB (1975). H, Cherif M, Baayen RP (2004b). Ultrastructure 9/b91-259 Anatomical markers for resistance of Ulmus of the alveolar network and its relation to coating Rioux D, Nicole M, Simard M, Ouellette GB americana to Ceratocystis ulmi. Phytopathology on vessel walls in elms infected by Ophiostoma (1998). Immunocytochemical evidence that se- 65: 349-352. - doi: 10.1094/Phyto-65-349 novo-ulmi and in other plants affected with simi- cretion of pectin occurs during gel (gum) and ty- Six DL (2012). Ecological and evolutionary deter- lar wilt diseases. Investigación agraria: Sistemas losis formation in trees. Phytopathology 88: 494- minants of bark beetle-fungus symbioses. Insects y Recursos Forestales 13: 147-160. [online] 505. - doi: 10.1094/PHYTO.1998.88.6.494 3: 339-366. - doi: 10.3390/insects3010339 URL: http://revistas.inia.es/index.php/fs/article/ Rohring E (1996). Elms in Europe: ecology and Smalley EB, Guries RP (2000). Asian elms: view/820 Dutch elm disease. Forstarchiv 67: 179-198. source of disease and pest resistance. In: “The Parker KG, Rankin WH, Collins DL (1941). Rudinsky JA (1962). Ecology of Scolytidae. An- Elms: Breeding, Conservation, and Disease Ma- Dutch Elm Disease fungus prevalent in bark bee- nual Review of Entomology 7: 327-348 - doi: nagement” (Dunn CP ed). Kluver Academic tle infested wood. Journal of Economic Entomo- 10.1146/annurev.en.07.010162.001551 Publishers, Boston, USA, pp. 215-230. logy 34: 548-551. Sacchetti P, Tiberi R, Mittempergher L (1990). Smalley EB, Kais AG (1966). Seasonal variation Peacock JW, Lincoln AC, Simeone JB, Silverstein Preferenza di Scolytus multistriatus (Marsham) in the resistance of various elm species to Dutch RM (1971). Attraction of Scolytus multistriatus durante la fase di maturazione delle gonadi nei elm disease. In: “Breeding Pest-Resistant Trees” (Coleoptera, Scolytidae) to a virgin female pro- confronti di due specie di olmo [Preference of (Gerhold HD, Schreiner EJ, Mc Dermott RE, duced pheromone in the field. Annals of the En- Scolytus multistriatus (Marsham) during the ma- Winieski JA eds). Pergamon Press, Elmsford, tomological Society of America 64: 1143-1149. turation feeding for two species of elm]. Redia, NY, USA, pp. 279-292. [online] URL: http://www.ingentaconnect.com/ pp. 347-354. [in Italian] Smalley EG (1963). Seasonal fluctuations in sus- content/esa/aesa/1971/00000064/00000005/art0 Santini A, Fagnani A, Ferrini F, Ghelardini L, ceptibility of young elm seedlings to Dutch elm 0031 Mittempergher L (2005a). Variation among Ita- disease. Phytopathology 53: 846-853. Pearce GT, Gore WE, Silverstein RM, Peacock lian and French elm clones in their response to Smucker SJ (1935). Air currents as possible car- JW, Cuthbert RA, Lanier GN, Simeone JB Ophiostoma novo-ulmi inoculation. Forest Pa- riers of Ceratostomella ulmi. Phytopathology 25: (1975). Chemical attractants for the smaller Eu- thology 35: 183-193. - doi: 10.1111/j.1439-032 442-443. ropean elm bark beetle Scolytus multistriatus 9.2005.00401.x Solla A, Gil L (2002a). Influence of water stress (Coleoptera: Scolytidae). Journal of Chemical Santini A, Ghelardini L, Falusi M, Bohnens J, on Dutch elm disease symptoms in Ulmus minor Ecology 1: 115-124. - doi: 10.1007/BF00987724 Buron M, Collin E, Solla A, Van den Broeck, A Miller. Canadian Journal of Botany 80: 810-817. Pecori F, Bottacci A, Migliorini D, Santini A (2004). Vegetative bud-burst variability of Euro- - doi: 10.1139/b02-067

Solla A, Gil L (2002b). Xylem vessel diameter as Takai S, Kondo ES (1979). Seasonal development “Insect-Fungus Interactions” (Wilding N, Collins a factor in resistance of Ulmus minor to Ophio- of Dutch elm disease on white elms in Central NM, Hammond PM, Webber JF eds). Academic stoma novo-ulmi. Forest Pathology 32: 123-134. Ontario, Canada. I. Following wound inocula- Press, London, UK, pp. 541-546. - doi: 10.1046/j.1439-0329.2002.0027 4.x tion. Canadian Journal of Botany 57: 341-352. - Webber JF, Kirby JN (1983). Host feeding prefe- Solla A, Martin JA, Corral P, Gil L (2005a). Sea- doi: 10.1139/b79-046 rence of Scolytus scolytus. Forest Commission sonal changes in wood formation of Ulmus pu- Tchernoff V (1965). Methods for screening and Bulletin 60: 47-49. mila and U. minor and its relation with Dutch for the rapid selection of elms for resistance to Westerdijk J, Buisman C (1929). De iepenziekte. elm disease. New Phytologist 166: 1025-1034. - Dutch elm disease. Acta Botanica Neerlandica Rapport over het ondeszoek verricht op verzoek doi: 10.1111/j.1469-8137.2005.01384.x 14: 409-452. - doi: 10.1111/j.1438-8677.1965. van de Nederlandsche Heidemaatschappij [The Solla A, Martin JA, Ouellette G, Gil L (2005b). tb00204.x elm disease. Report on the probe looking out at Influence of plant age on symptom development Tyree MT, Zimmermann MH (2002). Xylem the request by the Dutch Society Heath]. Arn- in Ulmus minor following inoculation by Ophio- structure and the ascent of sap. Springer Verlag, hem, The Netherlands, pp. 122. [in Dutch] stoma novo-ulmi. Plant Disease 89: 1035-1040. - NY, USA, pp. 285. Wood DL (1982). The role of pheromones, kairo- doi: 10.1094/PD-89-1035 Ware G (1995). Little-known elms from China: mones, and allomones in the host selectioin and Spierenburg T (1921). Een onbekende ziekte in de landscape tree possibilities. Journal of Arboricul- colonization behaviour of bark beetles. Annual iepen [An unknown disease in elm]. Tijdschrift ture 21: 284-288. Review of Entomology 27: 411-446. - doi: 10.11 over Plantenziekten 27: 53-61. Webber JF (1990). Relative effectiveness of 46/annurev.en.27.010182.002211 Stark VN (1952). Fauna SSSR, vol. 31 (Scoly- Scolytus scolytus, S. multistiatus and S. kirschi Wood SL, Bright DE (1992). A catalogue of Sco- tidae). Koroedy, Akad N SSSR, Moskva, as vectors of Dutch elm disease. European Jour- lytidae and Platypodidae (Coleoptera), part 2: Leningrad, Russia, pp 462. nal of Forest Pathology 20: 184-192. - doi: taxonomic index. Great Basin Naturalist Mem- Sticklen MB, Bolyard MG, Hajela RK, Duchesne 10.1111/j.1439-0329.1990.tb01129.x oirs 13: 1-1553. LC (1991). Molecular and cellular aspects of Webber JF (2000). Insect vector behaviour and the Zalapa JE, Brunet J, Guries RP (2009). Patterns of Dutch elm disease. Phytoprotection 72: 1-13. - evolution of Dutch elm disease. In: “The elms: hybridization and introgression between invasive doi: 10.7202/705997ar breeding, conservation and disease management” Ulmus pumila (Ulmaceae) and native U. rubra. Stipes RJ, Campana R (1981). Compendium of (Dunn CP ed). Kluwer Academic Publishers, American Journal of Botany 96: 1116-1128. - elm diseases. American Phytopathological So- Boston, USA, pp. 47-60. doi: 10.3732/ajb.0800334 ciety, St Paul, MN, USA, pp 66. [online] URL: Webber JF, Brasier CM (1984). The transmission Zanta F, Battisti A (1990). Notes on the distribu- http://www.cabdirect.org/abstracts/19811376781 of Dutch elm disease: a study of the process in- tion and biology of the elm bark beetles in north- .html volved. In: “Invertebrate-Microbial Interactions” eastern Italy (Coleoptera Scolytidae). Gortania - Sutherland ML, Brasier CM (1997). A compa- (Anderson JM, Rayner ADM, Walton D eds). Atti Museo Friulano di Storia Naturale, Udine rison of thirteen d-factors as potential biological Cambridge University Press, Cambridge, UK, 11: 189-205. control of agents of Ophiostoma novo-ulmi. pp. 271-306. Zimmermann MH, McDonough J (1978). Dysfun- Plant Pathology 46: 680-693. - doi: 10.1046/j.13 Webber JF, Gibbs JN (1989). Insect dissemination ction in the flow of food. In: “Plant disease - an 65-3059.1997.d01-62.x of fungal pathogens of trees. In: Proceedings of advanced treatise, vol 3: How plants suffer from Svihra P, Clark JK (1980). The courtship of the the 14th Symposium of the Royal Entomological disease” (Horsfall JG, Cowling ED eds). Acade- elm bark beetles. California Agriculture 4: 7-9. Society of London / British Mycological Society mic Press, New York, USA, pp. 117-140.