Interactions between insects and fungal pathogens of forest and ornamental trees
10.6092/issn.2531-7342/6362
Gli Autori hanno analizzato le interazioni tra insetti fitofagi e agenti fungini patogeni del castagno, cipresso, olmo, pini e querce in ambienti naturali ed in ambito urbano. È riportata una breve descrizione del ciclo vitale dell’insetto ponendo in relazione determinate sue fasi di sviluppo con il fungo che viene veicolato. Il fine di tale lavoro è di rapportare le varie tipologie associative insetto/patogeno fungino con l’ambiente che li ospita in modo da far emergere il ruolo di tali simbiosi nel determinare, assieme ovviamente ai fattori di natura abiotica, la destabilizzazione degli ecosistemi forestali ed urbani. Le interazioni accertate e possibili, come pure quelle che potrebbero verificarsi in futuro tra insetti e funghi patogeni immigranti e residenti in conseguenza di nuove introduzioni, vengono trattate separatamente, tracciando le linee di lotta prevedibili e perseguibili, con particolare riferimento all’ambiente urbano.
application/pdf
2531-7342
6362
en
Salvatore Moricca
Italian Journal of Mycology
interactions
Interactions between insects and fungal pathogens of forest and ornamental trees
Text.Serial.Journal
https://italianmycology.unibo.it/
45
Articles
2016-11-11
2016-11-10
2016-04-21
2018-08-20
54-65
Ital J Mycol
Salvatore Moricca
2016/11/11
10.6092/issn.2531-7342/6362
54
University of Firenze
2531-7342
interactions
en
65
Interactions between insects and fungal pathogens of forest and ornamental trees
https://italianmycology.unibo.it/article/download/6362/6129
45
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.          Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362




   Interactions between insects and fungal pathogens
   of forest and ornamental trees
   ________________________________________________________________________________

         Riziero Tiberi, Tiziana Panzavolta, Matteo Bracalini, Alessandro Ragazzi,
                                      Beatrice Ginetti, Salvatore Moricca

   Department of Agrifood Production and Environmental Sciences, Plant Pathology and Entomology
          Division, University of Florence, Piazzale delle Cascine, 18, 50144, Firenze, Italy

   Correspondig Author e-mail: tiziana.panzavolta@unifi.it

   Abstract

        The Authors have analyzed the interactions between insects and fungal pathogens of chestnut, cypress, elm,
        oak and pine trees in the natural environment and in urban areas. A brief description of the insect's life cycle is
        provided by relating some of its phases with the vectored fungus. The purpose of this work is to relate the
        different insect/pathogen associations with their environment in order to bring out the role of such symbioses in
        determining, together with abiotic factors, the destabilization of forest and urban ecosystems. The ascertained
        and possible interactions, as well as the ones that might occur in the future between immigrant and resident
        insects and fungal pathogens as a consequence of new introductions, are treated separately, taking into account
        the available control strategies, in particular those that are feasible in human-frequented areas.

        Keywords: forest and ornamental trees; insects; fungal pathogens; interactions


   Riassunto

        Gli Autori hanno analizzato le interazioni tra insetti fitofagi e agenti fungini patogeni del castagno, cipresso,
        olmo, pini e querce in ambienti naturali ed in ambito urbano. È riportata una breve descrizione del ciclo vitale
        dell’insetto ponendo in relazione determinate sue fasi di sviluppo con il fungo che viene veicolato. Il fine di tale
        lavoro è di rapportare le varie tipologie associative insetto/patogeno fungino con l’ambiente che li ospita in
        modo da far emergere il ruolo di tali simbiosi nel determinare, assieme ovviamente ai fattori di natura abiotica,
        la destabilizzazione degli ecosistemi forestali ed urbani. Le interazioni accertate e possibili, come pure quelle
        che potrebbero verificarsi in futuro tra insetti e funghi patogeni immigranti e residenti in conseguenza di nuove
        introduzioni, vengono trattate separatamente, tracciando le linee di lotta prevedibili e perseguibili, con
        particolare riferimento all’ambiente urbano.

        Parole chiave: piante forestali ed ornamentali; insetti; patogeni fungini; interazioni

   Introduction

   Plant pathogenic microorganisms like fungi, and animal organisms (such as arthropods, and especially
   insects), very far in terms of structural and functional organization, can contract associative relationships
   54
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.      Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    with reciprocal advantages. The most important difference in life-history traits between these two types of
    organisms is that insects are mobile, thus able to colonize space autonomously, while most fungal pathogens
    need to be passively transported, and perhaps this limitation is one of the main factors at the basis of insect-
    fungus interactions. The topic might appear at first glance scarcely connected with the recovery of stressed
    forests, where phenomena of ecological instability can be triggered. However, it is known that these
    imbalances are more and more frequently caused by phytophagous insects, often in combination with plant
    pathogenic microorganisms, such as fungi and, more rarely, bacteria.
    These situations are becoming increasingly common, and their complexity explains why, starting from the
    last decades of the 20th century, a specific field of research on phytosanitary control has been established.
    The scientific and practical importance of these studies is remarkable and, in the restoration of declining
    forests as a result of the action of insects and fungal pathogens, measures directed to the control of new
    attacks should be developed, since the eradication of already established parasites is no longer feasible.
    During interactions between insects and pathogenic fungi of woody plants, many circumstances occur that
    may allow them to become linked, more or less closely and permanently, so that benefits are granted to both.
    A clear example is given by bark beetles, which require plants stressed by various causes, including fungal
    infections, to breed. It is in fact common for fungi and insects to get in touch inside the woody plant tissues
    establishing special relationships (BEAVER 1989; TIBERI et al., 2002a, 2002b; JANKOWIAK, 2006; ÁLVAREZ
    et al., 2015). Although less frequently, relationships between pathogenic microorganisms and defoliating
    insects associated with green parts of the plant may also be established.
    The onset of these phenomena has a different importance in natural or semi-natural ecosystems, compared
    with urban and peri-urban systems and with areas maintained for recreational and landscaping purposes. In
    the first case, insects and pathogenic microorganisms are an integral part of the biotic component, and
    therefore, until their activity does not exceed the carrying capacity of the system, they turn out useful as they
    contribute to the modification of the structure and composition of the forest, shaping the stand in relation
    also to environmental conditions. In human-modified environments, and thereby not only in towns, insects
    and pathogenic microorganisms, individually or in combination, are usually a problem because their attacks
    may threaten heritage trees. In these environments, even individual plants are of fundamental importance,
    mostly when inserted in particularly valuable landscaped contexts. It becomes therefore crucial a prompt
    identification of the best strategies for plant protection.
    In such circumstances, the main problem consists in having to cope with different agents of different nature,
    for which differentiated control measures exist. Not an easy task considering the costs and, above all, the
    safety concerns typical of urban areas. The relationships that develop between insects and fungal pathogens
    are not always true obligate symbioses, but the non-mutualistic ties that may be established are nonetheless
    able to influence both the insect's development and the physiological state of the host plants. These
    relationships are very dangerous since they can trigger extended, and often irreversible, weakening
    phenomena (WEBBER and BRASIER, 1984; BATTISTI and COVASSI, 1991; TIBERI et al., 2002a).
    In some cases, insects strictly depend on the relationship with fungal pathogens, so as to have developed
    special body structures to transport fungi in order to increase their chances of survival. These structures,
    called mycangia, can appear as pits or pouches of various sizes, in which a substance, secreted by their
    associated glands, creates the best conditions for the survival of the fungus, inhibiting, at the same time, the
    antagonistic microorganisms (FRANCKE-GROSMANN, 1963; BEAVER, 1989).
    In the case of facultative symbioses, the transport of the pathogen seems to be a random phenomenon. This
    may occur simply through the adhesion of spores to insect setae or other tegumental structures, or even
    through its excrements. However, we cannot exclude the occurrence of specific invaginations, which
    represent optimum locations for the pathogenic fungus, being insects sometimes equipped with glands
                                                                                                                  55
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.          Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



   secreting substances having the function of preventing spore desiccation. This has been demonstrated for the
   fungus Ophiostoma ulmi (Buisman) Nannf., the causative agent of Dutch Elm Disease (DED), and for the
   bark beetle Scolytus multistriatus (Marsham) (FRANCKE-GROSMANN, 1963; WEBBER, 1990; FAVARO and
   BATTISTI, 1993).

   Ascertained interactions between insects and plant fungal pathogens

   The role of insects in spreading fungal pathogens of chestnuts, cypresses, oaks and pines has been proven
   over the course of multi-year surveys carried out also in Italy. In particular, the xylophagous insects infesting
   these plants are the most important vectors of some plant pathogens.
   However, in the case of cypress and pine trees, the ability of some insects, which colonize cones and seeds,
   to transport fungal pathogens was also demonstrated (Fig. 1). These types of interactions are facultative, the
   transport mechanism being in all cases the simple adhesion to insect’s body or through excrements. The
   interaction between insects and pathogens of cypress, due to their diffusion and importance in Italy, will be
   treated first.




   Fig. 1. Trophic diversity of dangerous forest insects.
   Fig. 1. Diversità trofica degli insetti forestali dannosi.
   Cupressus spp.
   In the facultative symbiosis between Seiridium cardinale (W.W. Wagener) B. Sutton et I.A.S. Gibson, the
   agent of cypress canker (Fig. 2), and phytophagous insects (COVASSI et al., 1975), the two parasites may get
   in contact on cypress bark, both of trunk and branches, as well as on cones and seeds. In the first case, bark
   beetles are mainly involved, but even wood boring insects and some vertebrates, such as birds and rodents,
   can play a role in the spread of the fungus. Conidia occurring outside or inside cones and seeds can adhere to
   the body of various insects. However, some vertebrates can also transport the fungus if they feed on infected
   cones. It might also be possible, though it has not been proven, that both xylophagous insects and cone/seed
   insects may ingest fungal mycelium during feeding, spreading it through their excrements.
   Surveys carried out in Italy on the role of insects in the spread of S. cardinale showed that, among
   xylophagous insects, the bark beetle Phloeosinus aubei Perris deserves particular attention (COVASSI, 1975).
   This species, found in Central and Southern Europe, North Africa and Asia Minor, is associated with the
   56
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.      Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    Cupressaceae, with a preference for the genus Cupressus. Like similar bark beetles, it attacks its host in two
    distinct phases.




    Fig. 2. Cupressus sempervirens trees with large crown dieback by Seiridium cardinale, agent of cypress canker
    Fig. 2. Piante di Cupressus sempervirens con vistosi disseccamenti della chioma da Seiridium cardinale, agente di
    cancro corticale.

    The reproductive activity takes place in trunk and branch phloem of cypress trees stressed by biotic or abiotic
    causes (1st phase): e.g. infestations with the aphid Cinara cupressi (Buckton) or vegetative impairment due to
    site conditions. For the maturation of gonads, however, the newly formed adults must move on twigs of
    vigorous trees (2nd phase), where they dig feeding tunnels (indeed called maturation galleries), which are also
    used for overwintering. In the case of strong activity on twigs, trees can become stressed as a result, and then
    they are attacked by mature adults for reproduction.
    In Italy, P. aubei completes two generations per year, overwintering being carried out by adults of the second
    generation (ZOCCHI, 1956; TIBERI and NICCOLI, 1991). In the northern regions and in colder environments
    the bark beetle develops a single reproductive cycle, or it can start a second one, which will be completed
    during the following spring; in this case the species overwinters as larvae in the reproduction galleries. In
    Mediterranean regions with milder climates, such as in Israel, the species may develop 3 to 4 generations,
    partially overlapping; this implies the presence of adults virtually all year round (MENDEL, 1984).
    The newly formed adults can come in contact with S. cardinale. They can load conidia present on the bark
    during emergence from the subcortical layers, where the insect’s preimaginal development took place.
    Conidia adhere to the insect’s setae or other body structures. The bark beetle then flies on the shoots of
    vigorous cypress trees to dig maturation galleries, thus carrying the conidia to healthy trees. Considering the
    coincidence in time between the appearance of adults (spring and late summer-early fall) and conidia
    discharge from the acervula, the chances that adults of the bark beetle may get contaminated by propagules
    of the fungus are substantial (MORIONDO, 1972).
    The seed insect Orsillus maculatus (Fieber) is also able to transport the conidia of S. cardinale. In fact,
    conidia of the fungus can be produced also on the cones, on which O. maculatus nymphs and adults feed.
    The insect has a thick pubescence to which conidia can adhere, thus fungal propagules can be transported to
    healthy cones during insect feeding or oviposition. Its phenology makes this hemipteran particularly

                                                                                                                  57
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.      Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



   dangerous, since it completes several reproductive cycles, widely overlapping, during one year. Therefore,
   the presence of nymphs and adults on the cones is almost continuous from spring to autumn (BATTISTI et al.,
   1997).
   Quercus spp.
   It is known that xylophagous insects and many fungal pathogens play a key role in oak decline, both in Italy
   and in other European countries. In fact, they can initiate and sustain the decline of the host plant by acting
   individually or simultaneously (TIBERI and RAGAZZI, 1996 RAGAZZI et al., 2000).
   In the spread of oak fungal pathogens, the insects involved are mainly beetles belonging to the family
   Buprestidae as well as bark beetles (Curculionidae: Scolytinae). All these xylophagous insects can play a
   remarkable role in the spread of many fungal pathogens that grow in woody tissues. For example, the
   buprestid Agrilus graminis Kiesenwetter is an active vector for some species of the genus Verticillium; the
   bark beetle Scolytus intricatus (Ratzeburg) for Fusarium solani (Mart.) Sacc. and Verticillium dahliae Kleb.;
   and the wood boring beetle Xyleborus dispar (F.) for Fusarium eumartii C.V. Carp., F. solani and V.
   dahliae. As regards Fusarium spp., the contact between the insect and the pathogen can take place on the
   outer bark as well as in the subcortical and woody layers.
   It remains unclear where the contact with species of Verticillium takes place, in particular in the case of V.
   dahliae and the buprestid A. graminis. In fact, microsclerotia of the fungus occur in the soil, a site less visited
   by the beetle, and therefore it is assumed that the contact can only take place at the base of the trunk of
   infected oaks (TIBERI et al., 2002b).
   Pinus spp.
   During the last decades of the 20th century, pines also entered a phase of gradual decline. This
   phenomenon may be connected with the chronological succession of attacks by insects and fungal pathogens
   and to vegetative difficulties of trees. Many researches have provided evidence that insects and fungal
   pathogens are important factors in the progressive decline of pine stands (JANKOWIAK, 2006; ÁLVAREZ et
   al., 2015) and, in this connection, many of these formations may be at risk of survival in Europe.
   We list some bark beetles and pathogenic fungi which, due to the high damage they cause, are among the
   major concerns in the protection of pine forests. As regards insects, the main species are Ips sexdentatus
   (Börner) (Fig. 3), and those of the genus Tomicus. The latter occurs in Italy with three species: T. minor
   (Htg.), T. piniperda (L.) and T. destruens (Woll.). As concerns fungi, some members of the Ophiostomatales,
   responsible for vascular infections and discoloration of the timber, are active and damaging agents
   contributing to pine decline (CAPRETTI and RAGAZZI, 2009).
   Insects, in particular bark beetles such as the aforementioned species, transport many of these fungi
   (DELORME and LIEUTIER, 1990; BOIS et al., 1999). Research carried out in pine forests of coast and inland
   Tuscany demonstrated, for example, the ability of T. destruens to transport conidia of Leptographium
   serpens (Goid) Siemaszko and Diplodia sapinea (Fr.) Fuckel (SABBATINI PEVERIERI et al., 2006) (Fig. 4).
   This insect/pathogen association is believed to be facultative, as the isolation of the fungus was achieved
   only from substrates on which the insect had been placed, or using the washing technique. Insect and fungal
   propagules can get together either in the phloem, where the preimaginal development of the insect occurs, or
   on the bark. Here the insects remain for a while, before flying in search of vigorous pine shoots for gonad
   maturation. This succession of phases resembles the one already described for P. aubei.
   These same studies have also demonstrated the association between D. sapinea and the coreid Leptoglossus
   occidentalis Heidemann, a seed insect associated with conifers. Again, as with O. maculatus and S.
   cardinale on cypress, nymphs and adults of L. occidentalis can get in touch with fungal propagules on the

   58
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.          Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    surface of infected cones; these conidia, adhering to body setae of L. occidentalis, may be vehiculated on
    other plants (MANCINI et al., 2010).




    Fig. 3. Ips sexdentatus galleries under pine bark. The dark color is given by the infection of Leptographium sp., which
    can be transported by the bark beetle.
    Fig. 3. Gallerie sottocorticali di Ips sexdentatus. Il colore scuro è dato dall’infezione di Leptographium sp., di cui lo
    scolitide può essere un vettore.


    .




    Fig. 4. Tomicus destruens association with fungal pathogens may result, for example, in the spread of Diplodia pinea
    and Leptographium spp., whose fruiting bodies are shown in the picture.
    Fig. 4. Le associazioni di Tomicus destruens con patogeni fungini possono portare, ad esempio, alla diffusione di
    Diplodia pinea e Leptographium spp., di cui nella foto si possono osservare le fruttificazioni.
    Castanea sativa
    The chestnut blight fungus Cryphonectria parasitica (Murrill) M. E. Barr, can be spread by bark mites. The
    mycelium of the fungus is in fact part of the diet of these small arthropods and, consequently, its conidia can
    occur in their excreta while hyphae can adhere to their body (NANNELLI et al., 1998).




                                                                                                                          59
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.     Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



   Possible interactions

   With “possible interactions” we mean those interactions which could be established between insects and
   pathogenic microorganisms occurring on the same examined samples, but at different times, though the
   pathogens have never been isolated from the body of investigated insects (TIBERI et al., 2002a). Among the
   possible interactions between phytophagous insects and fungal pathogens, it is worth mentioning those that
   might occur on cypress, oak and pine.
   Cupressus spp.
   While continuing to keep separate insects that exploit trunks and branches from those feeding on
   reproductive organs, there are more species, in addition to those already mentioned, which feed on cypress
   and that could be effective in spreading S. cardinale. Among xylophagous beetles, two other bark beetles of
   the genus Phloeosinus, namely P. armatus Reitter and P. thujae (Perris), are worth mentioning. The first
   species, native to the Eastern Mediterranean, was reported in Italy (Liguria) by COVASSI in 1991 and more
   recently in Tuscany (PENNACCHIO et al., 2013). This bark beetle develops two generations per year (up to
   four in Israel), overwintering as adults. It can be considered oligophagous on Cupressaceae but, similarly to
   the congeneric P. aubei, it shows a preference for Cupressus sempervirens L. P. thujae is present in many
   countries of Central and Eastern Europe as well as in Mediterranean countries, and even in England. It is
   associated with Cupressaceae as well, with a marked preference for species in the genera Juniperus and
   Thuja. Generally, it has a behavior similar to P. aubei and P. armatus, but it develops only one generation
   per year and it overwinters as mature larvae in the subcortical layers of attacked trees. Adults, which emerge
   in spring, may be already sexually mature, since they do not always need to feed on young shoots of
   vigorous plants to mature gonads. This assumes a lesser importance in P. thujae than other Phloeosinus
   species as concerns the transport of S. cardinale. Other xylophagous insects associated with cypress could
   play a significant role in the dispersal of the agent of cypress canker, as they can encounter conidia on the
   bark of infected trees.
   Many species of phytophagous insects are associated with cypress cones and seeds. One of the most feared
   species, given its wide distribution in Italy, is the tortricid moth Pseudococcyx tessulatana Staudinger, whose
   larvae feed on cone and seed tissues. This species completes three generations per year in central Italy.
   Adults, emerging from infected cones, may accidentally collect a load of S. cardinale conidia and transport
   them away, flying in search for new cones for oviposition. The seed chalcid Megastigmus wachtli Seitner is
   more dangerous where it is more common, and therefore it turns particularly harmful to cypress seeds. Less
   worrying, due to its lower frequency, is the twirler moth Brachyacma oxycedrella Millière (Gelechiidae).
   The possibility for scavenging insects, like barkflies, to contract casual relationships with S. cardinale on old
   infected cones, should not be underestimated. Recently, in fact, conidia of S. cardinale have been detected in
   the laboratory on the body of these insects (BATTISTI, unpublished data). On the other hand, the presence of
   various fungi, such as D. sapinea and Seiridium spp., has already been ascertained in the gut of barkflies
   collected on cypress in the field (PORCELLI et al., 1996).
   Also the role of some vertebrates should not be underestimated. More specifically the role of birds, which
   use lignified parts of the crown for nesting or simply as roost. Other possible vectors of the pathogen are
   rodents, which climb on plants to feed on cones. They can also get in contact with S. cardinale by eating
   seeds contained in infected cones or by moving over infected bark.




   60
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.         Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    Quercus spp.
    More numerous are the insects which may establish mutual relationships with pathogenic fungi on oaks.
    These are mainly xylophagous beetles. Worth mentioning, as potential vectors of some pathogenic fungi like
    Diplodia mutila (Fr.) Mont. and Phomopsis quercina (Sacc.) Höhn. Ex Died, are Sinoxylon sexdentatum
    (Olivier) and S. perforans (Schrank) (Bostrichidae). Other four beetles belonging to the family Buprestidae,
    such as Coroebus florentinus (Herbst), Chrysobotris affinis (F.), Agrilus biguttatus (F.) and Anthaxia
    millefolii (F.), may establish interactions with D. mutila, Verticillium spp., F. eumartii, and Sporothrix spp.
    Finally, the beetle Platypus cylindrus (F.) (Curculionidae) may be associated with V. dahliae.
     D. mutila and P. quercina are endophytic fungi, but many other well-known potential pathogens live as
    endophytes in healthy, asymptomatic plants, deploying their virulence only when infected hosts undergo
    stress conditions, ultimately contributing to their death (MORICCA and RAGAZZI, 2008).
    The following species display such a behavior on oaks: Biscogniauxia mediterranea (De Not.) Kuntze (Fig.
    5), Botryosphaeria dothidea (Moug.) Ces. & De Not. (Fig. 6), Diplodia seriata De Not., Phoma cava
    Schulzer, Neofusicoccum parvum (Pennycook & Samuels) Crous, Slippers & A.J.L. Phillips. These
    endophytic pathogens, similarly to D. mutila and P. quercina, may be transported by the above insect
    vectors, or by other bark beetles occurring on the same oak trees (RAGAZZI, 2004; TIBERI and ROVERSI,
    2004).




    Fig. 5. Large stromata of Biscogniauxia mediterranea, agent of charcoal canker on oaks. The perithecia are immersed
    in the inner layer of stromata, in contact with the woody tissue; at maturity they release the ascospores which can
    contaminate potential insect vectors.
    Fig. 5. Stroma di Biscogniauxia mediterranea, agente del cancro carbonioso delle querce. I periteci sono immersi nello
    strato interno dello stroma, a contatto con il tessuto legnoso; a maturità, essi liberano le ascospore che possono
    contaminare potenziali insetti vettori.




                                                                                                                       61
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.      Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362




   Fig. 6. Longitudinal lesions caused by Botryosphaeria dothidea on the stem of many Acer pseudoplatanus trees. Deep
   bark cracks induce tree death.
   Fig. 6. Lesioni longitudinali provocate da Botryosphaeria dothidea sul fusto di numerose piante di Acer
   pseudoplatanus. Profonde lacerazioni del tessuto corticale portano a morte le piante.
   Pinus spp.
   What reported for oaks can be in part true also for pine trees. However, reliable data on the possibility that
   other insects, and among these xylophagous beetles, can contract relationships with various pathogenic fungi
   of lignified parts and in particular with blue-stain fungi, such as the species in the genus Leptographium
   (CAPRETTI and RAGAZZI, 2009), are not yet available.

   Possible new associations because of extra-range spread into new areas

   Alien plant parasites pose a serious threat to natural and artificial ecosystems on our planet (PANCONESI et
   al., 2014). In the past, the colonization of new areas by living organisms occurred through long lasting
   patterns of natural dispersal, which have in part contributed to nourish that ecological mechanism which
   represents the basis for natural selection. Evolutionary processes triggered by newly introduced species often
   represented real co-evolution between organisms, in the fight for survival.
   In recent decades, due to the intensification of world trade and the greater ease of travelling from one
   continent to another, these natural processes have changed considerably, owing to the accidental dispersal of
   plants, animals and microbes or their deliberate release for varied purposes (PICCO et al., 2011). This has
   given rise to severe alterations of native ecosystems, which often led to the extinction of one or more native
   species. In this framework, it is highly possible that exotic fungal pathogens introduced to Italy can meet
   local insects, establishing new associations, or viceversa.
   Quercus spp.
   Among the associations that could arise in our country between introduced and native parasites, one in
   particular causes today major concern. It is the possible association between the fungus Ceratocystis
   fagacearum (Bretz) J. Hunt, widespread in North America, where it causes a disease known as "oak wilt" on
   Quercus rubra L. and Q. velutina Lam., and suitable vectors such as bark beetles of the genus Scolytus, as
   well as in some buprestids belonging mainly to the genus Agrilus (BATTISTI and COVASSI, 1991).
   62
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.       Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    Pinus spp and other conifers
    Another phytosanitary emergency, which involves insects as vectors, regards the dreaded introduction of the
    nematode Bursaphelenchus xylophilus Nikle, parasitic on conifers, especially pines. This species, native to
    North America, has long been introduced into East Asia. Recently, it was reported from pine forests in
    Portugal, France and in Scandinavian countries, suspected to have been introduced with timber imported
    from North America. In natural conditions various insects, especially longhorn beetles of the genus
    Monochamus, which are users of lignified organs of conifers (including pines), favor the spread of this
    parasite (SOUSA et al., 2011).

    Discussion and conclusions

    The environmental impact deriving from the combined action of insects and fungal pathogens undoubtedly
    affects forest ecosystems and, as a consequence, the unique beauty of the landscape. Ecosystem alteration
    and devastation by xylophagous insects and their associated pathogenic fungi are the cause of huge
    ecological and economic losses.
    Many trees attacked by insects and their associated pathogenic fungi are an important component of natural
    forests. Trees are also an important asset for public health in artificial forests and parks. Indeed, outdoor
    sport activity has been especially in recent years revalued together with a greater need of contact with nature,
    due to an increased human awareness. Not by chance the "welfare of population" was sponsored by the
    United Nations Environmental Programme with the Millennium Ecosystem Assessment Project (UNEP,
    2012), undertaken to identify environmentally-friendly development strategies, and to consolidate the culture
    of exploitation of "multiple benefits provided by ecosystems to mankind". These benefits, which can be
    synthesised in the sentence “ecosystem services”, refer to the relationships between environmental resources,
    economic systems and man (TOMAO et al., 2013).
    The spread of a fungal pathogen by insect vectors, and their joint action, may induce, in some cases, the
    extinction of attacked species. Such events would result undoubtedly in severe losses of that priceless
    heritage that takes the name of “biodiversity”. Such a heritage is unquestionably worthy of being preserved
    and protected because it provides an important source of economic, ecological, biochemical and medical
    resources which represent a priceless value for mankind.
    Insect and pathogen control in forest stands has some limitations in the intervention costs, but also in the risk
    of environmental impact. The now established principle of environmentally-friendly control tends to
    "rediscover" the good silvicultural practices, especially those aiming at avoiding the associations between
    phytophagous insects and fungal pathogens. More specifically, it can be summarized as follows: 1) working
    on the host plant, to reduce its susceptibility; 2) acting against both the insect and the fungus, to prevent their
    establishment and hinder possible relationship between them, thus limiting their spread; 3) modifying the
    environmental conditions, making them unfavorable for both the insects and the infectious microorganisms.
    In urban environments, however, the particular ecological conditions may often favor harmful insects and
    fungal pathogens, thus hindering the above mentioned practices, which cannot be always adequately applied.
    In fact, in urban systems some insect/fungus associations show a higher incidence; here, the two organisms
    represent always a problem as their attacks, singly or in combination, have major implications in the
    conservation of historical or valuable tree heritage. Insect/fungus relationships, as already mentioned, can
    substantiate in "obligate symbioses" or “non mutualistic symbioses": both are very harmful since they can
    trigger extensive and irreversible in situ and ex situ epidemics.
    In urban environments, control strategies must take into account the nature and the context of the damage,
    thus requiring a deeper assessment and more intense work than in natural systems. In the urban setting, in
                                                                                                                    63
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.   Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



   fact, the hygienic-sanitary function, the safety of citizens, and the aesthetic/recreational aspects become
   much more important than the mere production of timber. The preferred approach should be an integrated
   control strategy, with preventive and curative measures applied in an ideal balance.

   References

   ÁLVAREZ G., FERNÁNDEZ M., DIEZ J.J., 2015. Ophiostomatoid fungi associated with declined Pinus pinaster
     stands in Spain. Forest Systems, 24 (1), 1-9.
   BATTISTI A., COVASSI M., 1991. I principali insetti xilofagi viventi su querce in Italia e loro ruolo nei
     fenomeni di deperimento. Atti del Convegno Aspetti fitopatologici delle Querce, Firenze, 19-20
     Novembre 1990, 251-272.
   BATTISTI A., COLOMBARI F., FRIGIMELICA G., GUIDO M., 1997. Life history of Orsillus maculatus, a true
     bug damaging seeds of Cupressus sempervirens. In A. Battisti, J.J. Turgeon (eds), Proceedings of the 5th
     Cone and Seed Insects Working Party Conference (IUFRO S7.03.01), September 1996, Monte Bandone,
     Italy, 215-220.
   BEAVER R.A., 1989. Insect-fungus relationships in the bark ambrosia beetles. In N. Wilding, N. M. Collins,
     P.M. Hammond, J.F. Webber (eds.), Insect-fungus interactions. 14th Symposium of the Royal
     Entomological Society of London in collaboration with the British Mycological Society, London:
     Academic Press.
   BOIS E., LIEUTIER F., YART A., 1999. Bioassays on Leptographium wingfieldii, a bark beetle associated
     fungus, with phenolic compounds of Scots pine phloem. European Journal of Plant Pathology, 105, 51-
     60.
   CAPRETTI P., A. RAGAZZI, 2009. Elementi di Patologia forestale. Pàtron Editore, Bologna, 432 pp.
   COVASSI M., INTINI M., PANCONESI A., 1975. Osservazioni preliminari sui rapporti fra Coryneum cardinale
     Wag. e Phloeosinus aubei Perr. in Toscana. Redia, 56, 159-166.
   DELORME L., LIEUTIER F., 1990. Monoterpene composition of the preformed and induced resins of Scots
     pine and their effect on bark beetles and associated fungi. European Journal of Forest Pathology, 20, 304-
     316.
   FRANCKE-GROSMANN H., 1963. Some new aspects in forest entomology. Annual Review of Entomology, 8,
     415-438.
   FAVARO A., BATTISTI A., 1993. Observation on the elm bark beetle Scolytus pygmaeus (Fabricius)
     (Coleoptera Scolytidae) as a possible vector of the fungus Ophiostoma ulmi (Schwarz) Nannfeldt. Redia,
     76, 459-466.
   JANKOWIAK R., 2006. Fungi associated with Tomicus piniperda in Poland and assessment of their virulence
      using Scots pine seedlings. Annals of Forest Science, 63, 801-808.
   MANCINI V., LUCHI N., FEDUCCI M., CAPRETTI P., 2010. Diplodia pinea detection on Leptoglossus
     occidentalis (insect vector) by Real time-PCR. Journal of Plant Pathology, 92, (4, Supplement), S4.89.
   MENDEL Z., 1984. Life history of Phloeosinus armatus Reitter and P. aubei Perris (Coleoptera: Scolytidae)
     in Israel. Phytoparasitica, 12, 89-97.
   MORICCA S., RAGAZZI A., 2008. Fungal endophytes in Mediterranean oak forests: a lesson from Discula
     quercina. Phytopathology, 98, 380-386.
   MORIONDO F., 1972. Il cancro del cipresso da Coryneum cardinale Wag. I° contributo. La progressione del
     processo infettivo nei tessuti caulinari. Annali Accademia Italiana di Scienze Forestali, 21, 399-426.
   NANNELLI R., TURCHETTI T., MARESI G., 1998. Corticolous mites (acari) as potential vectors of
     Cryphonectria parasitica (Murr.) Barr hypovirulent strains. International Journal of Acarology, 24, 237-
     244.


   64
R. Tiberi, T. Panzavolta, M. Bracalini, A. Ragazzi, B.       Italian journal of Mycology vol. 45 (2016) ISSN 2531-7342
Ginetti, S. Moricca
DOI: 10.6092/issn.2531-7342/6362



    PANCONESI A., MORICCA S., RAGAZZI A., DELLAVALLE I., TIBERI R., 2014. Parassiti delle piante arboree
      forestali ed ornamentali. Specie introdotte e di temuta introduzione. Pàtron Editore, Bologna, 447 pp.
    PENNACCHIO F., DANTI R., BENASSAI D., SQUARCINI M., MARZIALI L., DI LONARDO V., ROVERSI P.F.,
      2013. A new additional record of Phloeosinus armatus Reitter from Italy (Coleoptera Curculionidae
      Scolytinae). Redia, 96, 45-50.
    PICCO A.M., ANGELICI P., CICCARONE C., FRANCESCHINI A., RAGAZZI A., RODOLFI M., VARESE G.C.,
       ZOTTI M., 2011. Biodiversity of emerging pathogenic and invasive fungi in plants, animals and humans in
       Italy. Plant Biosystems, 145 (4), 988-996.
    PORCELLI F., DE MARZO L., FRISULLO S., SPARAPANO L., 1996. Possible dissemination of Sphaeropsis
      sapinea (Fr.) Dyko and Sutton f. sp. cupressus Solel et Al. (Deuteromycotina) by Psocoptera
      psocomorpha in Italy. Proceedings of the XX International Congress of Entomology, Florence, August 25
    RAGAZZI A., 2004. Endophytism: knowns and unknowns of an age-old phenomenon. In Endophytism in
      forest trees, by Alessandro Ragazzi, Salvatore Moricca, Irene Dellavalle. Accademia Italiana di Scienze
      Forestali (eds), Firenze, Italy, 15-32.
    RAGAZZI A., MORICCA S., DELLAVALLE I., TURCO E., 2000. Italian expansion of oak decline. In: Ragazzi A.,
      Dellavalle I. (eds.) Decline of oak species in Italy: problems and perspectives, Accademia Italiana di
      Scienze Forestali, Firenze, Italy, 41-75.
    SABBATINI PEVERIERI G., CAPRETTI P., TIBERI R., 2006. Associations between Tomicus destruens and
      Leptographium spp. in the forests of Pinus pinea and P. pinaster in Tuscany, central Italy. Forest
      Pathology, 36, 14-20.
    SOUSA E., BRAVO M.A., PIRES J., NAVES P., PENAS A.C., BONIFACIO L., MOTA M., 2011. Bursaphelenchus
      xylophilus (Nematoda; Aphelenchoididae) associated with Monochamus galloprovincialis (Coleoptera;
      Cerambycidae) in Portugal. Nematology, 3(1), 89-91.
    TIBERI R., NICCOLI A., 1991. I principali insetti dannosi al cipresso in Italia. In A. Panconesi ed.: Il cipresso.
       C.N.R. – C.E.E., Firenze, 178-186.
    TIBERI R., RAGAZZI A., 1996. Oak decline studies. CEE Project Studies on Forest Damage 92.60.IT.009.0,
       Concepts, Structure and 1995 Results, 85-87.
    TIBERI R., ROVERSI P.F., 2004. Forest insects that live in plant tissue as miners or borers. In Endophytism in
       forest trees, by Alessandro Ragazzi, Salvatore Moricca, Irene Dellavalle. Accademia Italiana di Scienze
       Forestali (eds), Firenze, Italy, 221-236.
    TIBERI R., RAGAZZI A., CAPRETTI P., ROVERSI P. F., TARASCO E., 2002a. Associazioni insetti fitofagi-
       Microrganismi fitopatogeni e protezione del verde urbano. Redia, 84, 29-39.
    TIBERI R., RAGAZZI A., MARIANELLI L., SABBATINI PEVERIERI G., ROVERSI P. F., 2002b. Insects and fungi
       involved in oak decline in Italy. Proceedings of IOBC-OILB, “Integrated Protection in Quercus sp.
       Forests” 1-4 October 2001, Oeiras – Lisboa, Portugal, 8pp.
    TOMAO A., CARBONE F., MARCHETTI M., SANTOPUOLI G., ANGELACCCIO C., AGRIMI M., 2013. Boschi,
      alberi forestali, esternalità e servizi eco sistemici. L’Italia Forestale e Montana, 68 (2), 57-73.
    UNEP, 2012.United Nations Environmental Programme. www.UNEP.org.
    WEBBER J.F., BRASIER C.M., 1984. The transmission of Dutch elm disease: a study of the processes
      involved. In: Invertebrate-microbial interactions, Anderson J.M., Rayner A.D.M., Walton D.W.H. Eds.,
      Joint Symposium of The British Mycological Society and The British Ecological Society, University of
      Exeter, September 1982, Cambridge University Press, Vol. 6, 271-306.
    WEBBER J.F., 1990. Relative effectiveness of Scolytus scolytus, S. multistriatus and S. kirshii as vectors of
      Dutch elm desease. European Journal of Forest Pathology, 20, 184-192.
    ZOCCHI R., 1956. Insetti del cipresso. I. Il genere Phloeosinus Chap. (Coleoptera: Scolytidae). Redia, 41,
      129-225.


                                                                                                                   65
