Pine Pitch Canker and Insects: Relationships and Implications for Disease Spread in Europe

Review Pine Pitch Canker and Insects: Relationships and Implications for Disease Spread in Europe

Mercedes Fernández-Fernández 1,2,* , Pedro Naves 3 , Johanna Witzell 4 , Dmitry L. Musolin 5 , Andrey V. Selikhovkin 5,6, Marius Paraschiv 7, Danut Chira 7, Pablo Martínez-Álvarez 2,8 , Jorge Martín-García 8,9, E. Jordán Muñoz-Adalia 10 , Aliye Altunisik 11, Giuseppe E. Massimino Cocuzza 12, Silvia Di Silvestro 13 , Cristina Zamora 2,8 and Julio J. Diez 2,8

1 Department of Agroforestry, ETSIIA Palencia, University of Valladolid, Avenida de Madrid 44, 34071 Palencia, Spain 2 Sustainable Forest Management Research Institute, University of Valladolid-INIA, Avenida de Madrid 44, 34071 Palencia, Spain 3 Instituto Nacional de Investigação Agrária e Veterinária, INIAV, Av. da República, Quinta do Marquês, 2780-505 Oeiras, Portugal 4 Swedish University of Agricultural Sciences. Southern Swedish Forest Research Centre, P.O. Box 49 SE-230 53 Alnarp, Sweden 5 Department of Forest Protection, Wood Science and Game Management, Saint Petersburg State Forest Technical University, Institutskiy per., 5 St. Petersburg 194021, Russia 6 Department of Biogeography and Environmental Protection, Saint Petersburg State University. 13B Universitetskaya Emb., St. Petersburg 199034, Russia 7 National Institute for Research and Development in Forestry “Marin Dracea”, Bras, ov Research Station,

13 Clos, ca Str., 500040 Bras, ov, Romania 8 Department of Plant Production and Forest Resources, University of Valladolid, Avenida de Madrid 44, 34071 Palencia, Spain 9 Department of Biology, CESAM (Centre for Environmental and Marine Studies), University of Aveiro, Campus Universitario de Santiago, 3810-193 Aveiro, Portugal 10 Forest Sciences Center of Catalonia (CTFC), Carretera St. Llorenç de Morunys, 25280 Solsona, Lleida, Spain 11 Department of Plant Protection-Phytopathology, Akdeniz University, 07070 Campus Antalya, Turkey 12 Department of Agriculture, Food and Environment, University of Catania, Via Santa Soﬁa, 100, 95123 Catania, Italy 13 Council for Agricultural Research and Economics (CREA), Research Centre for Olive, Citrus and Tree Fruit, Corso Savoia 190, 95024 Acireale, Italy * Correspondence: mﬀ[email protected]

Received: 6 June 2019; Accepted: 20 July 2019; Published: 26 July 2019

Abstract: The fungal pathogen Fusarium circinatum (Nirenberg and O’ Donnell) is the causal agent of pine pitch canker (PPC) disease, which seriously affects conifer species in forests and nurseries worldwide. In Europe, PPC is only established in the Iberian Peninsula; however, it is presumed that its range could expand through the continent in the near future. Infection caused by this fungus requires open wounds on the tree, including physical damage caused by insects. Therefore, a relationship probably occurs between PPC and a wide variety of insects. The aim of this review is to outline the taxonomic and ecological diversity of insect species with high potential association with F. circinatum in Europe and elsewhere. The insects were classified as vectors, carriers and wounding agents according to the association level with the PPC disease. In addition, we discuss the insect-mediated spreading of PPC disease in relation to the different phases of forest stand development, from seeds and seedlings in nurseries to mature stands. Lastly, to improve our predictive capacities and to design appropriate intervention measures and strategies for controlling disease dissemination by insects, variables such as geographic location, time of the year and host species should be considered.

Forests 2019, 10, 627; doi:10.3390/f10080627 www.mdpi.com/journal/forests Forests 2019, 10, 627 2 of 23

Our review provides a framework of the multiple factors that regulate the insect–host interactions and determine the success of the infection.

Keywords: pine pitch canker; vectors; carriers; wounding agents; forests; nurseries; insect control

1. Introduction The ascomycete fungus Fusarium circinatum (Nirenberg and O’ Donnell) is the causal agent of pine pitch canker (PPC), a serious disease that has been recorded in more than 50 species of pines (Pinus spp.) and Pseudotsuga menziesii (Mirb.) Franco [1]. Native to North America, this pathogen has been found in South Africa, Japan, Korea, Mexico, Chile, Uruguay, Colombia, Brazil as well as in Europe (France, Spain, Italy, and Portugal [1]). The fungus is currently included in the A2 list of quarantine organisms (recommended for regulation) of the European and Mediterranean Plant Protection Organization (EPPO) and has so far limited distribution in the European and Mediterranean regions [1,2]. Fusarium circinatum is a pathogen that causes high seed mortality [2]. It can also cause necrosis, chlorosis, wilting of needles, dieback, desiccation, and eventual death of seedlings [3]. In mature trees, it causes pitch resin-soaked cankers in trunks and large branches, which can girdle and predispose the trees to being broken during windstorms. The extent of damage varies among regions, host species, and habitats ranging from plantations, nurseries, parks and gardens or forests [4]. The pathogen can be found in all parts of the host trees (root, trunk, branches, shoots, cones, and seeds), as well as in the forest litter. The asexual spores (microconidia and macroconidia) are produced in a viscous liquid, but can also become airborne. As a wound pathogen, F. circinatum needs mechanical wounds or feeding/entrance holes of insects to enter the plant, and its spores may be attached to motile organisms. It is thus not surprising that studies conducted in different countries have demonstrated that forest insects associated with pines play an important role in the natural spreading of PPC (e.g., [1,4]). Some insect species act as vectors (carrying and transmitting the pathogen to the trees) [4–6], carriers (only carrying the pathogen) and others, as wounding agents (providing infection court for the pathogen). The assessment of the insects associated with F. circinatum is a dynamic exercise, as the nature of the association can vary between geographic locations, time of the year and pine hosts. Multiple factors regulate the association between the insect and the pathogen: for instance, the ecology and life cycle of the insects and their association with the host tree are crucial, as insects feeding on fresh tissues and requiring frequent visits to living pines are more prone to successfully inoculate the fungal spores into healthy hosts. The insect´s mobility is also important, and adults of the majority of the species associated with F. circinatum can actively move and disperse it by flight, resulting in a higher risk of disseminating the pathogen within and between forests. Finally, another fundamental aspect is the ability of the insects to transport the spores of the fungi on their body, which conditions the phoretic rate, i.e., the proportion of insects carrying the pathogen, and which is dependent of a complex interaction between environmental factors and anatomical characters of the insect. Given that F. circinatum was only recently recorded for the first time in Europe [1], it is foreseeable that its range can noticeably expand through the continent in the near future. To control or locally eradicate the pathogen, it is critically important to have detailed knowledge on which European insects can promote spreading of the fungus and how they can do it. In this review, we analyze the taxonomic and ecological diversity of insect species with known or high potential association with F. circinatum in Europe and elsewhere, and critically asses their potential risk as vectors sensu lato. Forests 2019, 10, 627 3 of 23

2. Interactions of Fusarium circinatum with Insects Worldwide, F. circinatum has been reported to be phoretically associated with a broad array of insect species [1,4]. Some of these are thought to be potential vectors of F. circinatum (meaning that in addition to carrying the pathogen, and visiting susceptible plant hosts, such species are capable of successfully transmitting the pathogen to trees that were not yet infected). Others are assumed to be carriers (which means that they carry the pathogen and visit susceptible hosts, but their capacity to transmit the pathogen has not yet been demonstrated). A third group of insects, which can contribute to PPC epidemiology, are the wounding agents, which create infection courts for the pathogen, by damaging the bark and wood with their tunnels and entrance holes, and/or feeding on shoots, twigs and cones [4]. Moreover, the wound has to be deep enough to provide adequate moisture; the spores need to germinate before wound desiccation, provided that not too much resin has been produced to stop the process [7,8]. Altogether, these groups of insects are taxonomically and ecologically heterogeneous and include, among others, shoot and foliar feeders (Coleoptera: Curculionidae; Lepidoptera: Tortricidae), bark beetles and wood borers (Coleoptera: Curculionidae), root borers (Coleoptera: Curculionidae), cone insects (Lepidoptera: Tortricidae, Pyralidae; Hemiptera: Coreidae, Scutelleridae; Coleoptera: Curculionidae, Anobiidae), sucking insects (Hemiptera: Aphrophoridae, Cercopidae) and predators (Coleoptera: Zopheridae, Cleridae; Diptera: Dolichopodidae). The assessment of the insects associated with F. circinatum as vectors, carriers or wounding agents is a challenging exercise, as the nature of the association can vary between geographic location, time of the year and host species. Multiple factors regulate the association between the insect and the pathogen: for instance, the spatiotemporal synchrony of ecological traits and life cycle of the insects and host trees are crucial [9]. The feeding habit is also important, and insects feeding on fresh tissues and requiring frequent visits to living pines are more prone to successfully inoculate the fungal spores into healthy hosts. Another important trait is the insect´s mobility, and the more active the species associated with F. circinatum, the higher the risk of disseminating the pathogen within and between forest stands [4]. Finally, a fundamental aspect is the ability of the insect to transport the spores of the fungi on their body, which conditions the phoretic rate, i.e., the proportion of insects carrying the pathogen, and being dependent on a complex interaction between environmental factors and anatomical characters of the insect [1,2,4].

2.1. Interactions of F. circinatum with Insects in European Countries Fusarium circinatum has been reported to be phoretically associated to various species of bark beetles (Coleoptera: Curculionidae) in Pinus radiata (D. Don) plantations in northern Spain, namely Pityophthorus pubescens (Marsham, 1802), Hylurgops palliatus (Gyllenhal, 1813), Ips sexdentatus (Börner, 1776), Hypothenemus eruditus Westwood, 1836, Hylastes attenuatus Erichson, 1836, Orthotomicus erosus (Wollaston, 1857), Pissodes validirostris (C.R. Sahlberg, 1834), Brachyderes incanus (Linnaeus, 1758) [10], and Tomicus piniperda (Linnaeus, 1758) [11]. In general, the biology of most of these species is well studied, as some are important forest or nursery pests (e.g., [12–17]). The nature of their association with F. circinatum as well their preferred hosts and distribution range are summarized in Table 1. Forests 2019, 10, 627 4 of 23

Table 1. Ecological characteristics and distribution of insects associated with Fusarium circinatum in Europe considered as vectors, carriers or wounding agents.

Association with F. circinatum and Preferred Pine Selected Species Distribution Range Possible Transmission Pathways Habitat References Shoot and foliage feeders Europe, North-Western Africa and Northern Vector; shoots (feeding); bark and Pine stands of Tomicus piniperda Asia; introduced in North-eastern North [11,18] phloem (oviposition) different ages America (USA and Canada) Widespread in Europe Asia, Northern Africa, Rhyacionia spp. Wounding agent; shoots (oviposition) Young pine stands [12,19] North America; introduced in South America Bark beetles and wood borers Carrier; bark and phloem of mainly Pine stands of Pityophthoruspubescens small branches (twigs) (oviposition Europe, Asia minor, Northern Africa (Morocco) [10,20–23] different ages and feeding) Carrier; bark and phloem of trunk, Pine stands of Europe, Northern Asia, Northern Africa; Hylurgops palliatus branches and occasionally roots [10,24,25] different ages introduced in North America (oviposition and feeding) Carrier; bark and phloem of trunks Ips sexdentatus Mature pine stands Europe, Northern Asia and East to China [10,26,27] (oviposition and feeding) Carrier; bark and phloem of small Widespread in tropical, subtropical and Hypothenemus twigs, even in leaf petioles Pine stands of temperate regions of the world; introduced in [10,28,29] eruditus (oviposition and feeding), different ages some European countries occasionally in seeds and fruits Carrier; bark and phloem of branches, Pine stands of Europe, Northern Africa, Asia and East to Hylastes attenuatus [4,10,25,30,31] trunk, stumps and roots different ages China, Korea and Japan Europe, Asia, Northern Africa; introduced in Carrier; bark and phloem of trunk and Pine stands of Orthotomicus erosus North and South America, Southern Africa, [1,10,24,30] branches (oviposition and feeding) different ages and Oceania Root borers Carrier; bark and phloem of Europe, introduced in North America (USA Brachyderes incanus Young pine stands [10,32] branches, roots and Canada) Cone insects Wounding agent, carrier; cones and Pissodes validirostris shoots (feeding of beetles); Mature pine stands Europe, Northern Asia and East to China [33–35] cones (oviposition)

2.1.1. Shoot and Foliage Feeders The genus Tomicus (Coleoptera: Curculionidae) has eight species worldwide, with three occurring in Europe: Tomicus minor (Hartig, 1834), T. piniperda and T. destruens (Wollaston, 1865) and are amongst the most important pests of pine forests. In Spain, T. piniperda is the most plausible vector of PPC [11] and, together with T. destruens, these species are widely distributed in Iberia Peninsula and Portugal [18,36]. The main hosts of European Tomicus are pines (Pinus spp.), including non-native species such as P. radiata and Pinus strobus Linnaeus [18,37]. Although these insects can attack apparently healthy trees, they prefer stressed pines, especially scorched and burnt trees [38,39]. Tomicus species occupy diﬀerent niches in their hosts during their life cycle; while the preadult stages develop subcortically in the phloem, the adults perform maturation and regeneration feedings within the shoots of healthy pines (hence the common name of “pine shoot beetles”). The hibernation period continues within the shoots of the pine crown in the Southern latitudes, in the base of the pine trunks or in the soil litter in northern latitudes [21,40]. For the maturation and regeneration feeding, the adults ﬂy to the crown of healthy pines and excavate galleries into the pith of the current-year shoots, which eventually break after windy or rainy conditions and fall to the ground. Shoot feeding can cause big damages when attacks occur in young plantations or when a large proportion of shoots is destroyed, resulting in loss of growth and pine decline, making the trees suitable for trunk attack by the following beetle generation or by secondary beetles [18]. Several fungal species have been described as associated with Tomicus beetles, including species of Ophiostoma and Leptographium [18,41,42]. Despite these consistent associations, Tomicus beetles apparently do not have specialized structures, such as mycangia, to transport the fungi [43], although structures present in the base of setae could act as fungi transport frames [1]. Adults can also carry nematodes, including species of the Bursaphelenchus genus [18]. In Europe, it was concluded, according to Leach´s postulates, that T. piniperda is a plausible vector of PPC, although with a low phoresy rate [11]. The low phoresy rate could be explained because in Forests 2019, 10, 627 5 of 23

P. radiata terpene expression triggered by T. piniperda inhibits F. circinatum growth [44]. In other studies, propagules of F. circinatum were not obtained from insects collected from infected stands [10,45,46]. Nevertheless, Tomicus beetles should be considered important vectors of PPC in Europe due to their widespread distribution and their status as pests in pine forests. In addition, their particular behavior consisting in feeding on several shoots/insect creates feeding wounds in healthy tree that determines their potential importance in the disease spreading. Moreover, they are effective vectors/carriers of fungi and other organisms. Pine tip moths belonging to the genus Rhyacionia (Lepidoptera: Tortricidae) are also shoot feeders, and Rhyacionia buoliana (Denis and Schiffmüller, 1775) has been reported on more than 30 species of pines, including P. radiata [12]. Damage is caused by the larvae feeding in pine shoots and buds, with mining galleries usually accompanied by webbing and flow of resin [47]. Infested shoots and buds wilt and die, leading to deformation of the tree axis and affecting the tree shape and growth, which is particularly harmful in young plantations [48]. While this moth has not yet been found associated with PPC, they could be possible wounding agents, as it was mentioned for other species of the genus in USA. There are other moths for which association with PPC has not yet been demonstrated. However, due to their widespread distribution, their pest status and their ability to create feeding wounds in healthy trees, they could be possible carriers and, most likely, wounding agents. Another insect to consider is the pine sawyer beetle Monochamus galloprovincialis (Oliver) (Coleoptera: Cerambycidae) that is a shoot-feeder as an adult, being generally considered a secondary wood-boring insect associated with weakened, scorched or recently dead pines for breeding [20,49]. However, it can also occasionally damage conifer forests following population outbreaks [50–52]. Furthermore, M. galloprovincialis is the vector of the introduced pinewood nematode, which has been causing significant pine mortality in both Portugal and Spain [20]. Several fungal species have been found associated with M. galloprovincialis [53], including pathogenic and blue-stain fungi such as Ophiostoma minus (Hedgc.) (Syd. and P. Syd.), Ophiostoma piceae (Münch) (Syd. and P. Syd.), Leptographium procerum (W.B. Kendr.) (M.J. Wingf.) and Fusarium oxysporum Schltdl. found on insects and galleries with a relative abundance below 1% [53,54]. While these beetles have not yet been found associated with PPC, they are possible vectors and, most likely, wounding agents, that would contribute to its dissemination.

2.1.2. Bark Beetles and Wood Borers Bark beetles (Coleoptera: Curculionidae) associated with pines can generally be considered carriers of F. circinatum. Twig beetles (Pityophthorus spp.) (Coleoptera: Curculionidae) have been associated with PPC in Europe and North America. Pityophthorus pubescens is a non-aggressive forest insect, colonizing weakened trees or broken branches in healthy pines [22], where it constructs galleries in the phloem or in the pith of small branches [55]. In Spain, Romón et al. [10] found F. circinatum in 25% of the sampled P. pubescens adults, while Bezos et al. [22] reported a weaker association with lower phoresy rates (maximum of 2%) and low incidence of the pathogen in the insects’ galleries. These variations may result from differences in the ambient humidity, which can condition the efficiency of Pityophthorus species in carrying the PPC pathogen [55], or from different population levels in the pine stands. In addition to P. pubescens, other European Pityophthorus species share similar morphological and ecological traits and live on conifers (mainly on pines, but also on Picea and Abies species), and therefore also may become associated with the PPC pathogen. The genus Ips includes some of the most important forest pests of pines and spruces, with seven species occurring in Europe [26]. In Southern Europe, the most important species is I. sexdentatus, causing significant mortality in pine stands (Pinus sylvestris Linnaeus, P. pinaster and P. radiata) affected by fires, storms or droughts [30,56,57]. In Northern Spain, it is considered one of the most important pests affecting P.radiata in mature stands, where weakened trees are at particular risk [20,58]. The species is also shown to be a carrier of F. circinatum [10,59]. Ips beetles do not make wounds or galleries on Forests 2019, 10, 627 6 of 23 twigs or shoots of healthy pines, so the risk of being effective vectors of PPC is lower than for other similar bark beetles such as Tomicus species. However, Ips beetles can attack healthy pines (including P. radiata), inoculate fungi, fly for long distances and produce several generations per year in Southern Europe [60], suggesting high risk of becoming associated with F. circinatum in European pine forests. There is some possibility that the pine engraver bark beetle I. acuminatus might become a vector or carrier of F. circinatum in Europe. The species is considered a serious pest of pines and it is attracting growing attention in Ukraine, Belorussia, Russia, Finland and in some other countries [16,61,62]. It has been demonstrated that I. acuminatus can vector dozens of fungi including pathogens such as Diplodia pinea and Ophiostoma minus [63]. However, the role of this species in spreading PPC will likely be limited as this species has maturation feeding under the bark of exactly the same (and already weakened) trees on which they had just developed as larvae. Ips acuminatus can attack branches and tops of healthy trees, but it prefers to inhabit irreversibly weakened pines. Orthotomicus erosus has also been found carrying spores of F. сircinatum in Northern Spain [10]. This widespread bark beetle develops mainly on pines, including P. radiata [1,10,30], although it can also be found on other conifers [24,64–66]. Similarly to other bark beetles, Orthotomicus spp. are frequently found carrying fungi, particularly ophiostomatoid fungi [67–69], including species of Fusarium genus [10,25]. Hylurgops palliatus is another bark beetle also found carrying F. сircinatum in Northern Spain [10]. It is a widespread forest species found throughout the Palearctic region [24,70], being generally considered a secondary bark beetle on stumps or freshly cut logs [71]. It is associated with several fungi species, particularly blue-stain fungi of the genera Leptographium, Graphium [25,72–74], and Ophiostoma [75]. Hypothenemus eruditus has been found in Northern Spain carrying propagules of F. circinatum [10]. It is present in all tropical and subtropical regions of the world, and in many temperate regions [29], including Spain, France, Italy, and Malta [76]. The adults are extremely small (only up to 1.3 mm), and are exceptionally polyphagous, having been recorded from hundreds of plant hosts [28,77]. The widespread distribution, morphological variations, extended habits, and host range suggest that H. eruditus may, in fact, represent a species-complex still to be discriminated [29]. Pine weevils of the genus Pissodes (Coleoptera: Curculionidae) are important forest pests, and Pissodes castaneus can cause significant damage to pines (and occasionally to larches and spruces) as larvae and adults [58,78–80]. Larvae develop on the inner bark of branches, trunks and even roots, making a characteristic pupal cell under the bark before emergence [78]. These species show frequent mutualistic relationships with blue-stain fungi [25], including pathogenic species of the genera Leptographium [81], Armillaria [82], and Sporothrix [83,84]. Pissodes castaneus have been found to be carriers of F. сircinatum in Spain [10,30]. As with other similar bark beetles, species of the genus Hylastes are associated with several fungi species [25], particularly blue-stain fungi of the genus Ophiostoma (anamorph Graphium)[72] and Leptographium [85], which they transmit to pine seedlings by feeding [86]. Hylastes spp. are associated with PPC and have been found to be carriers of F. сircinatum in North America [4] and in Spain, e.g., H. attenuatus [10]. In Europe, eleven species occur, mainly associated with pines [37,87], including P. radiata [30,86]. Hylurgus ligniperda (Fabricius, 1787), native to Central and Southern Europe, Asia Minor and Algeria [87]. Its hosts are species of the family Pinaceae. It breeds on the bark of dead and dying trees, usually in the thick sections near the base of the trunk, stumps and in large exposed roots [88]. It is considered a secondary pest, not causing significant damage to pine forests [37]. Nevertheless, it is known to transmit blue-stain fungi to wood via its galleries, along with root pathogens [89–92]. Hylurgus beetles have not been found to be associated with PPC in Europe or North America [4,10], but should be considered possible carriers keeping in mind their ecology, life habits and frequent association with decaying pine hosts and fungi. Forests 2019, 10, 627 7 of 23

Hylobius abietis (Linnaeus, 1758) (Coleoptera: Curculionidae) is an important pest in Scandinavia, Northern European part of Russia and Eastern Siberia, aﬀecting particularly one- to three-year-old coniferous plantations and regeneration areas [93,94]. It can be found on P.radiata [25], and is considered a pest of signiﬁcant concern for plantations in Northern Spain [58]. Moreover, it is an important vector of numerous fungi (e.g., [84]), and although it has not been found associated with F. circinatum, a plausible association as carrier cannot be discarded.

2.1.3. Root Borers Brachyderes incanus (Coleoptera: Curculionidae), is considered a minor conifer pest, which is important only in newly established plantations [32], although it has been found carrying F. circinatum in Northern Spain [10]. Larvae bore into and strip bark from roots of the hosts, occasionally killing roots up to 3 mm in diameter, while the adults feed on conifer needles and occasionally damage the bark [32].

2.1.4. Cone Insects European insects associated with cones can be considered carriers or wounding agents that facilitate F. circinatum infections. Pissodes validirostris (Coleoptera: Curculionidae), is the only member of its genus feeding on the seed cones of pines [95], and in the Iberian Peninsula it is an important pest of Pinus pinea Linnaeus cones, causing economic losses [33]. It was considered a biological control agent against invasive pines in South Africa, and the relationship between P. validirostris and F. circinatum was investigated under controlled conditions [35]. The authors found that, under controlled conditions, the weevils were not able to transmit the fungus, but the feeding wounds favored the infection of the host by F. circinatum. Another cone insect is Leptoglossus occidentalis (Heidemann, 1910) (Hemiptera: Coreidae), native to North America but accidentally introduced into Europe [96]. Adults feed on the young seeds or ﬂowers of over 40 species of conifers, mainly pines, causing infertility or total destruction of the seeds [97–99]. In the Mediterranean Basin, this seed bug has been related to the strong reduction of pine seed production, with a negative impact on the production of edible pine-seeds in P. pinea [100–103]. Despite the economic impact of this species, little is known about its associated fungal community, but Luchi et al. [104] reported a phoretic relationship with the pine pathogen Diplodia pinea (Desm.) in Mediterranean pine forests. Its widespread distribution, abundance and polyphagy makes L. occidentalis a plausible wounding agent of PPC in Europe, similarly to Leptoglossus corculus (Say, 1832) in North America [4]. Another important cone insect due to the high losses of pine-seeds of Pinus pinea in Spain is Dyorictria mendacella (Staudinger, 1859) (Lepidoptera, Pyralidae) [105]. Although no evidence of any relationship between PPC disease and this moth currently exist, it could be also considered as an important wounding agent and an entry point for the disease.

2.1.5. Sucking Insects Even though there are no direct evidence of relationship between F. circinatum and sucking insects in Europe, some of the latter can potentially be at least wounding agents or carriers as they do make holes while feeding and can ﬂy or can be carried by wind from one tree to another. The following species of sucking insects could deserve some attention: scale insects such as Leucaspis spp. (Hemiptera: Diaspididae) (in particular, Leucaspis pusilla (Loew, 1883), Leucaspis lowi (Colvée, 1882) and Leucaspis pini (Hartig, 1839)) [106], aphids of the genus Cinara (Hemiptera: Aphididae), in particular, Cinara acutirostris (Hille Ris Lambers, 1956), Cinara brauni (Börner, 1940), Cinara pinea (Mordvilko, 1894), Cinara pinihabitans (Mordvilko, 1896) and Cinara schimitscheki (Börner, 1940). Moreover, bark bugs, such as Aradus cinnamomeus Panzer, 1806 (Hemiptera: Aradidae) or spittlebugs like Haematoloma dorsatum (Ahrens, 1812) (Hemiptera: Cercopidae) could also have some participation in the PPC spreading in Europe [107–112] although these associations should be further clariﬁed. Forests 2019, 10, 627 8 of 23

2.1.6. Predators The possible association of F. circinatum with predatory insects has not been assessed in Europe. Yet, these insects could be possible carriers of the PPC pathogen, given their habits of predating on bark beetles and other insects under the bark and in galleries, where they may get in contact with F. circinatum propagules, although their overall importance as dispersal agents is expected to be low.

2.2. Interaction of Fusarium circinatum with Insects in Non-European Countries As noted above, F. circinatum has been found in USA, South Africa, Japan, South Korea, Mexico, Chile, Uruguay, Colombia, and Brazil. However, to our knowledge, the available information regarding insects interacting with the pathogen outside of Europe is limited to studies carried out in USA, and, to a lesser extent, in Chile and South Africa. On the other hand, although F. circinatum has not been reported in Oceania [4,113], some potential vectors of PPC were reported in New Zealand. Taking into account that these authors already collated this information and no new relevant data are available, this review will focus only on the F. circinatum–insect interactions in those countries where PPC is already presented.

2.2.1. Shoot and Foliage Feeders In North America, the shoot-feeders are mainly considered wounding agents, including the pine tip moths of the genus Rhyacionia (Lepidoptera: Tortricidae). Blakeslee et al. [114] and Dwinell et al. [115] pointed out that airborne spores of F. circinatum can readily infect wounds created by the subtropical pine tip moth (Rhyacionia subtropica Miller, 1961) and other similar species. Other authors isolated the PPC pathogen from shoots damaged by pine tip moths, and from larvae and pupae [116,117]. Runion et al. [118] reported that in eastern North Carolina, the percentage of Pinus taeda Linnaeus seedling terminals damaged by pine tip moths was positively correlated with infection by the PPC pathogen. Other shoot feeders include Contarinia spp. ﬂies (Diptera: Cecidomyiidae), which cause wounds on pines (particularly on P. taeda and Pinus elliottii (Engelm.)) in seed orchards and plantations in the SE of the USA [115]. According to Dwinell et al. [115], the wounds are often colonized by the PPC pathogen.

2.2.2. Bark Beetles and Wood Borers Species of the genus Pityophthorus (Coleoptera: Curculionidae) are the most studied insects as agents of dispersion of the PPC disease outside Europe. Most of the studies have been performed in California (USA), where at least four species (Pityophthorus setosus (Blackman, 1928); Pityophthorus carmeli (Swaine, 1918); Pityophthorus nitidulus (Mannerheim, 1843); and Pityophthorus pulchellus (Eichhoff, 1869)) have been shown to act as carriers of the pathogen F. circinatum [119,120]. Storer et al. [6] demonstrated that P. setosus acts as a vector of F. circinatum in an experiment in which the insects were artificially contaminated with spores of the pathogen and caged with branches of P. radiata. It was found that trees baited with insect pheromones were more likely to develop the PPC disease than unbaited trees, while Erbilgin et al. [121] concluded that the transmission percentage and lesion length were positively correlated with the propagule load. Erbilgin et al. [121] also studied P. carmeli and found that adults artificially inoculated and confined to P. radiata branches transmitted the disease, therefore confirming their role as vectors under artificial conditions. Species of the genus Ips (Coleoptera: Curculionidae) can cause large-scale damage to conifer forests with destructive outbreaks usually triggered by weakened trees due to fires, windstorms, drought or other pests or diseases [122]. Trees weakened by PPC infections can be vulnerable to attacks by Ips beetles [123], which subsequently act as vectors of F. circinatum [124,125]. In California, Ips paraconfusus Lanier, 1970, has been confirmed as a vector of PPC [4,5], and Erbilgin et al. [126] found F. circinatum on 10%–17% of the adults of I. paraconfusus and Ips plastographus (LeConte, 1868). Spores of the pathogen were found also inside the galleries and on the body of larval stages of Ips mexicanus Forests 2019, 10, 627 9 of 23

(Hopkins, 1905) and I. paraconfusus [5]. The contamination rates and propagule loads suggest a higher risk of PPC transmission taking place in spring and early summer [127]. Other bark beetles such as Hylurgops spp. and Dendroctonus valens LeConte, 1860 (Coleoptera: Curculionidae) are considered carriers of the PPC pathogen in California [128]. In Chile, F. circinatum has occasionally been isolated from nursery plants damaged by Hylastes ater (Paykull, 1800) [129], suggesting this insect could act as a carrier, with Hylastes spp. also considered as carriers in California [128]. The pathogen F. circinatum has been isolated from Pissodes radiatae (Hopkins, 1911) (Coleoptera: Curculionidae) collected with sticky and funnel traps near infected trees in California [30,128]. Similar results were reported by Storer et al. [127], who found a low phoresy rate of the PPC fungus on these weevils. Several other cone insects seem to facilitate the entrance of F. circinatum into the host plant as wounding agents. An association between the weevil Pissodes nemorensis (Germar, 1824) (Coleoptera: Curculionidae) and PPC has been suggested in the USA [114,130]. In South Africa, such association was predicted [131] based on a similar interaction previously demonstrated between P. nemorensis and D. pinea [132].

2.2.3. Cone Insects Fusarium circinatum is known to infect cones [133,134], and therefore cone insects are potential vectors of PPC. Although there is no confirmation of cone insects vectoring F. circinatum, a few species were identified as carriers, namely Conophthorus radiatae (Hopkins, 1915) (Coleoptera: Curculionidae) and Ernobius punctulatus (LeConte, 1859) (Coleoptera: Anobiidae) in California [120,128,135]. E. punctulatus requires an entry tunnel previously made by another insect (e.g., C. radiatae) and transmission of inoculum between both species was already suggested by Hoover et al. [136]. Thus, E. punctulatus would not increase the infestation rate if C. radiatae had already introduced the pathogen into the cone. However, if the latter does not transmit the pathogen, E. punctulatus may enter the cone (using the entry tunnel made by the weevil) and introduce the pathogen [137]. Furthermore, cone beetles could promote a more efficient infection because this would take place deeply into the cone and, therefore, moisture on the cone surface would not be a requirement [138]. Conelet abortion and seed deterioration caused by PPC has also been associated with feeding by L. corculus, Tetrya bipunctata (Herrich-Schäffer, 1839) (Hemiptera: Scutelleridae) and Laspeyresia spp. (Lepidoptera: Tortricidae) [115], although these associations should be further clarified.

2.2.4. Sucking Insects An association between spittlebugs and the PPC pathogen has been reported in California. In ﬁeld samplings, Storer et al. [139] found that shoots with spittlebugs (Aphrophora canadensis Walley 1928) (Hemiptera: Aphrophoridae) feeding were more likely to develop PPC than shoots without feeding, while in a controlled experiment the incidence of PPC on shoots of potted P. radiata trees depended on the presence of spittlebugs [139]. Correll et al. [128] found the PPC pathogen on specimens of Aphrophora permutata Uhler 1875, suggesting these insects could act as carriers of the pathogen and not solely as wounding agents.

2.2.5. Predators Some predatory insects are thought to be carriers of the PPC pathogen in California [4]. The genus Lasconotus (Coleoptera: Zopheridae) includes cylindrical beetles which predate on bark beetles in their galleries [140], where they may get the propagules of F. circinatum [141]. In a study performed by McNee et al. [135], the phoresy rate for Lasconotus pertenuis (Casey, 1890) in two locations in California (USA) was 37.5% ± 7.8% and 16.1% ± 1.9%. Storer et al. [127] mentioned that these beetles have the capacity to transmit the pathogen into bark beetle galleries free of the pathogen, although experiments fulﬁlling Leach’s postulates [142] have not been conducted yet. Forests 2019, 10, 627 10 of 23

Larvae of Medetera spp. (Diptera: Dolichopodidae) are frequently found under the bark of trees, acting as bark beetle predators. However, only one reference has been found involving species from this genus in the spread of the PPC pathogen [127], and, once again, Leach’s postulates have not been met yet. Enoclerus sphegeus Fabricius 1787 (Coleoptera: Cleridae) is a predator of bark beetles which has been related to the spread of F. circinatum in California [127]. The authors report the potential of this species to transmit the pathogen into the bark beetle galleries free of the pathogen, similarly to L. pertenuis and Medetera spp. discussed above.

3. Insect-Mediated Spreading of PPC in Nurseries and Forests The potential role of insects in spreading or facilitating the PPC diﬀers according to the pest’s capacity to damage pine seedlings and/or young and adult trees, host resistance, environment, and human activities [128]. In this section, we discuss the insect-mediated spreading of PPC in relation to the diﬀerent phases of forest stand development, from seeds and seedlings to mature stands.

3.1. Nurseries Nurseries play an essential role in the PPC spread at a regional scale, because the disease may be effectively dispersed with infected planting stock. In nurseries, potential sources of fungal inoculum are the soil and other growth media, used containers, weeds and irrigation water, as well as seeds. Pine seeds are known to be prone to contamination by F. circinatum and transfer of seeds is a major pathway for the long-distance spreading of PPC [143]. The seeds may be infected early during their development: the fungus has been found to cause mortality of female flowers and mature strobili, and may infect and destroy gametophyte tissues of pine seeds [144]. Nevertheless, the same authors conclude that in many seed lots, the seed contamination by F. circinatum is restricted to the outer seed coat of otherwise healthy, viable seeds, and that actual infection and destruction of endosperm and embryos may occur only rarely. Cone and seed-associated insects can have strong impacts on seed production, but, in general, their influence in PPC dispersal is not well studied or is assumed to be secondary, as already discussed in the previous chapters. Seeds that are contaminated in the forest or seed orchards may be brought to the nurseries to obtain seedlings. The nursery seedlings are particularly vulnerable for insects that damage the developing root system, with the succulent foliage also providing an attractive feeding substrate for defoliators. The development of seeds to seedlings can last one or two years, with the nursery plants exposed to a variety of stressful factors such as adverse soil proprieties, high air humidity promoting the growth of pathogenic fungi or insect pests. Sandy and silty soils with high humidity can be favourable for insects such as Melolontha spp. (Coleoptera: Scarabaeidae), the larvae of which forage underground on roots of different tree species. Other common scarabeid insects may be involved in spreading of PPC in nurseries, including species of the genera Rhizotrogus, Amphimallon, Anomala, Polyphylla, and Phyllopertha, which have polyphagous root eater larvae (grubs) and defoliator (on broadleaved species) adults. The root and collar eaters can easily get in contact with mycelium and spores of Fusarium on infected soil [145]. Root eaters can be abundant, and cause significant economic impacts in agriculture, horticulture, viticulture, and forestry, namely the cockchafers Melolontha melolontha (Linnaeus, 1758) and Melolontha hippocastani (Fabricius, 1801) [146]. In Poland, damage by grubs in nurseries and young plantations resulted in economic losses up to 7 M € in 2006 [147–149]. Other insects that cause damage in nurseries include wireworms (Coleoptera: Elateridae; e.g., genera Agriotes and Selatosomus), tenebrionids and phytophagous dipterans [146]. Wireworms of click beetles (Coleoptera: Elateridae), with the most common species belonging to the genus Agriotes in Europe, are less aggressive than grubs, yet important in nurseries where they damage the seedlings in early developmental stages [150]. Feeding damage by larvae of Otiorhynchus sulcatus (Fabricius, 1775) (Coleoptera: Curculionidae), which results in visible wilting and mortality, is frequently observed in nursery seedlings, while roots are also damaged by Gryllotalpa gryllotalpa (Linnaeus, 1758) (Orthoptera: Forests 2019, 10, 627 11 of 23

Gryllotalpidae)—one of the most conspicuous orthopteran forest pests [151]. Altogether, we can conclude that there is a widespread, abundant and diversiﬁed array of insect species, which can, directly or indirectly, favor the establishment and spreading of F. circinatum in European nurseries.

3.2. Forests In many countries, the weevil H. abietis is the most destructive pest of pine plantations, as it can destroy up to 50%–100% of seedlings in recent plantation [152–156]. Weevils of the genus Pissodes are generally considered less aggressive, although P. castaneus can cause damage while feeding on the collar of young pine trees, whereas Pissodes piniphilus (Herbst, 1797) and Pissodes pini (Linnaeus, 1758) infest the aboveground parts of older trees [80]. Other common insects with high potential to spread PPC are scarabeid beetles of the genus Melolontha, which can devastate entire young plantations of coniferous species [157]. The regeneration and maturation feeding of Hylastes species (H. ater and Hylastes cunicularius (Erichson, 1836)) occurs around the root collar, killing seedlings, and sometimes destroying whole plantations [86,158]. Moreover, Hylobius spp. and Hylastes spp. may spread the disease at long distance, as these insects have been found at distances between 43 and 171 km of the nearest plantations [159,160]. Insects that infest weakened trees through regeneration feeding on twigs and buds usually do not cause major damage, but their larvae may severely damage the water and nutrient transporting tissues when feeding under the bark of the trees [161]. The importance of bark beetles and wood-boring insects increases on older forests, and while most species attack weakened trees as secondary pests, some are able to primarily attack pines. Climate stress (intense winds, severe droughts, fires, floods, etc.), other pests (including invasive species), and anthropogenic activities (unsustainable silviculture, pollution, etc.) are the most important factors which contribute to the occurrence of bark beetle outbreaks [162–165]. Shoot-feeding beetles infest the crown causing growth losses, and engraver beetles, with their associated fungi, can cause significant tree mortality [166]. Due to extreme weather conditions, bark beetle outbreaks have reached an unprecedented distribution and intensity in many countries, leading to severe alterations in forest ecosystem processes [5,123,167–171]. Pines have been affected by these outbreaks especially in areas where they have been planted out of their natural ecological (historical) range [172]. Recent dramatic outbreaks of Dendroctonus ponderosae (Hopkins, 1902) affected more than 1.2 M ha of Pinus contorta var. latifolia Engelmann in Central USA [173], whereas Dendroctonus armandi (Tsai and Li, 1959) has killed 300 M m3 of Pinus armandii Franch. in China since the 1970s [174]. In Europe, severe attacks of T. piniperda has been reported to reduce forest productivity up to 45% of annual increment in Scandinavia [175], with losses of up to 72 M €/year in the Basque Country [176]. At the interface of the Mediterranean and Maritime zones, I. sexdentatus affected 37.9 M m3 of P. pinaster forest after the passage of the hurricane “Klaus”, with additional damages reported on P. radiata forests in the Basque Country [177]. In Russia, a large outbreak of the defoliator Dendrolimus sibiricus (Tschetverikov, 1908) (Lepidoptera: Lasiocampidae) affected 2.5 M ha of Pinus sibirica (Du Tour) and other conifers [165]. Forests affected by repeated attacks by pests and diseases, or from other abiotic-induced problems, are therefore more susceptible for F. circinatum establishment, not only by the lower vigor of the trees but also by the presence of multiple insects of various trophic guilds, which can, isolated or combined, act as vectors (sensu lato) of the PPC pathogen.

4. Spatial and Temporal Aspects of Insect-Mediated Transmission of PPC A thorough consideration of the spatial and temporal aspects related to insect–host interactions may help to foresee the risk of insect-mediated spreading of PPC, and to design appropriate intervention measures and sustainable management strategies for nurseries, plantations and natural forests. In all these environments, the transmission of F. circinatum by insects occurs across different spatial and temporal barriers, which can be classified as “filters” sensu [178]. “Encounter filter” determines if, Forests 2019, 10, 627 12 of 23 to what extent, the pest or pathogen finds the potential host, and “compatibility filter” determines their success after the contact with a host is made. The degree of spatial mobility of the carrier or vector insects is one of the crucial factors affecting the risk of insect-mediated spreading of F. circinatum to potential hosts at a landscape level. Pine shoot beetles (Tomicus spp.) can carry the spores of F. circinatum [179], which develop fast inside the breeding tunnels and infect larvae, pupae and adults [5]. The ability to feed on different shoots during their maturation-feeding phase favors the further spread of the fungus. They are also known to be good flyers, with an average dispersal distance ranging from 250 to 400 m, with some individuals being able to fly up to 2 km [180,181]. The mean flight distance for Ips spp. has been reported to be around 1.5–2 km, and a small percentage of adults can fly more than 5 km [182,183], while for O. erosus mark–recapture trials have suggested flight distances between 100 and 500 m, with some individuals recaptured up to 4–10 km from the release point [184]. The relatively large beetles of the genus Monochamus are also capable of moving long distances. Hernández et al. [185]; Más et al. [186]; David et al. [187] and Etxebeste et al. [188] found high within-population variability of flight performance in M. galloprovincialis with a mean distance of 16 km flown over the lifetime of the beetle. Maximum flight distance of about 5.5 km was reported for Monochamus sutor (Linnaeus, 1758), with mean distances ranging between 1.2 and 1.7 km [189]. Insect-mediated encounters between pines and F. circinatum are also strongly determined by the temporal and spatial patterns in the development of insect populations. Environmental factors, especially temperature, are key determinants of this synchrony [190]. Because insects are ectothermic, their development and reproduction are readily affected by changes in temperature regimes. For instance, voltinism may increase due to the climate-change related temperature elevations, potentially multiplying the encounters between pines and F. circinatum propagules. Multivoltine populations of Ips typographus (Linnaeus, 1758) have already been observed in spruce forests of high altitude and latitude areas [191]. The climate impact on voltinism is also illustrated by the case of T. destruens, which in the Mediterranean coastal pine forests has two breeding periods, one before winter and another from February to June [15,192]. Temporal patterns in host susceptibility are often related to phenological (seasonal) changes [193], e.g., bud burst [194] with the transition from juvenile phase to maturity. These patterns are often accompanied by variation in the nutritious quality and defensive chemistry and anatomy, which are a part of the “compatibility filter”. For instance, Erbilgin and Colgan [195] studied Pinus banksiana (Lambert) responses to multiple enemies and defense inducers, reporting that although the constitutive monoterpenes were higher in the phloem of juvenile trees, the phloem of mature trees had a much higher magnitude of the defense induction. Changes in nutritional and defensive chemistry that occur in the host during the phenological development are expected to affect phytophagous insects, in particular species feeding or developing on annual shoots, such as shoot feeders and sucking insects. For instance, R. buoliana, which is particularly damaging on P. nigra and P. sylvestris [196], could be responsive to host phenological stage: the larvae, after an initial period spent mining in the needles, penetrate into the shoots through the buds and begin to bore a feeding gallery to complete their development [93]. To date, the only report on the association between Rhyacionia spp. and F. circinatum is by Matthews [116], who referred to seedlings in nurseries. Considering the feeding habits of the moth, its involvement in the spread of PPC could be mainly due to its potential role as a wounding agent. Forest management can modify various spatiotemporal aspects related to insect-mediated spread of PPC. This could involve bottom-up effects on plant quality (e.g., through fertilization), influencing the “compatibility filter”, or top-down impacts of stand characteristics (e.g., through thinning operations), influencing the habitats for the natural enemies of the carrier or vector insects [197]. Management for even-aged monocultures may provide insects with concentrated resources and thus effectively support local population growth, whereas the complexity of a mixed forest can make it more difficult for the insect pests to find the host trees [198]: thus, the species composition can effectively regulate Forests 2019, 10, 627 13 of 23 the “encounter filter”. In general, by acknowledging the complex spatiotemporal aspects, e.g., through modelling approaches, we may be able to significantly improve our predictive and responsive capacities and develop targeted management strategies to suppress the insect-mediated spread of PPC.

5. Conclusions • Numerous insect species that commonly occur in pine nurseries and forests throughout Europe and elsewhere have the potential to spread PPC as either vectors, carriers or wounding agents. Most of the evidence is, however, circumstantial and ambiguous, and in order to accurately model the spreading risk of PPC, more detailed information is required on the effective capacity of the different species to act as vectors. Such information can only be achieved through extensive field and laboratory studies. • The importance of insect-mediated distribution of PPC also varies in different stages of forest development and forestry systems. The young seedlings, found in high densities in nurseries and plantations, attract different feeding guilds of insects than the old trees with large stem biomass and thick bark. Thorough understanding of the insect ecology and biology while they develop on trees in nurseries and in different stages of forest development will help to develop integrated pest management strategies to minimize the insect-mediated spreading of PPC. Effective pest control is important especially in nurseries, which have a crucial role in the regional spreading of PPC. • It is clear that different feeding habits and life style of the insect species influence the risk of insect-mediated spreading of PPC. The phoretic rate, the ability to move between habitats (e.g., flight distances), seasonal timing, duration and location of feeding activities, fungal guilds involved in phoretic interactions, population fluctuations and type of damage/wounds caused by the insects differ markedly between species and feeding guilds, and should be carefully considered when modelling the risk of PPC spreading to new areas.

Author Contributions: Writing: M.F.-F., P.N., J.W., D.L.M., A.V.S., M.P., D.C., P.M.-Á., J.M.-G., E.J.M.-A., A.A., G.E.M.C., S.D.S. and C.Z.; review: M.F.-F., P.N., J.W. and J.J.D.; editing: M.F.-F. and A.A. Funding: This study was made possible through the project “Etiology, Epidemiology and Control of Fusarium circinatum” sponsored by the Ministry of Rural, Marine, and Natural Environment, and with the support of the Government of Cantabria. This article is based upon work from COST Action FP1406 PINESTRENGTH (Pine pitch canker strategies for management of Gibberella circinata in greenhouses and forests) supported by COST (European Cooperation in Science and Technology) and project AGL2015-69370-R funded by MINECO and FEDER. This work is a contribution of URGENTpine (PTDC/AGR-FOR/2768/2014) funded by Fundação para a Ciência e a Tecnologia, I.P., through national funds, and the co-funding by the FEDER (POCI-01-0145-FEDER-016785), within the PT2020 Partnership Agreement and Compete 2020. Thanks for financial support are due to CESAM (UID/AMB/50017/2019), to FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. FCT also supported J.M.-G. (SFRH/BPD/122928/2016). P.N. would like to thank funding by the Fundação para a Ciência e Tecnologia—FCT (contract IF/00471/2013/CP1203/CT0001), Portugal. D.L.M.’s contribution was also supported by The Russian Foundation for Basic Research (Grant No. 17-04-01486). A.V.S.’s contribution was also supported by the Center for collective use of scientific equipment "Renewable resources, energy sources, new materials and biotechnology (SPbFTU)" (Project 2019-0420). Acknowledgments: We want to thank Martin Muller, Jaime Aguayo, Katarina Adamcikova, Kaljo Voolma, Stanley Freeman, Panos Petrakis, and Svetlana Markovskaja for their contribution in the collection of references related to the PPC disease. Conflicts of Interest: The authors declare no conflict of interest.

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© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). Review Pine Pitch Canker and Insects: Regional Risks, Environmental Regulation, and Practical Management Options

Mercedes Fernández-Fernández 1,2,*, Pedro Naves 3 , Dmitry L. Musolin 4 , Andrey V. Selikhovkin 4,5, Michelle Cleary 6 , Danut Chira 7, Marius Paraschiv 7, Tom Gordon 8 , Alejandro Solla 9 , Irena Papazova-Anakieva 10, Tiia Drenkhan 11, Margarita Georgieva 12, Aliye Altunisik 13, Carmen Morales-Rodríguez 14, Mara Tabakovi´c-Toši´c 15, Dimitrios N. Avtzis 16 , Georgi Georgiev 12, Danail D. Doychev 17, Sterja Nacheski 10, Tarik Trestic 18, Margarita Elvira-Recuenco 19 , Julio J. Diez 2,20 and Johanna Witzell 6 1 Department of Agroforestry. ETSIIA Palencia, University of Valladolid, Avenida de Madrid 44, 34071 Palencia, Spain 2 Sustainable Forest Management Research Institute, University of Valladolid-INIA, Avenida de Madrid 44, 34071 Palencia, Spain 3 Instituto Nacional de Investigação Agrária e Veterinária, INIAV, Av. da República, Quinta do Marquês, 2780-505 Oeiras, Portugal 4 Department of Forest Protection, Wood Science and Game Management, Saint Petersburg State Forest Technical University, Institutskiy per., 5, 194021 St. Petersburg, Russia 5 Department of Biogeography and Environmental Protection, Saint Petersburg State University, 13B Universitetskaya Emb., 199034 St. Petersburg, Russia 6 Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, P.O. Box 49, SE-230 53 Alnarp, Sweden 7 National Institute for Research and Development in Forestry “Marin Dracea”, Bras, ov Station, 13 Clos, ca Str.,

500040 Bras, ov, Romania 8 Department of Plant Pathology, University of California, Davis, CA 95616, USA 9 Institute for Dehesa Research (INDEHESA), Ingeniería Forestal y del Medio Natural, Universidad de Extremadura, Avenida Virgen del Puerto 2, 10600 Plasencia, Spain 10 Faculty of Forestry, University “Ss Cyril and Methodius”-Skopje, Goce Delcev 9, 1000 Skopje, Republic of Macedonia 11 Institute of Forestry and Rural Engineering, Estonian University of Life Sciences.; Kreutzwaldi 1, 51014 Tartu, Estonia 12 Forest Research Institute, Bulgarian Academy of Sciences, 132 St. Kliment Ohridski Blvd., 1756 Sofia, Bulgaria 13 Department of Plant Protection-Phytopathology, Akdeniz University, 07070 Campus Antalya, Turkey 14 Department for Innovation in Biological, Agro-food & Forest Systems (DIBAF), University of Tuscia, Via S. Camillo de Lellis, snc, 01100 Viterbo, Italy 15 Institute of Forestry, 11030 Belgrade, Serbia 16 Forest Research Institute, Hellenic Agricultural Organization Demeter, 65, 57001 Thessaloniki, Greece 17 University of Forestry, 10 St. Kliment Ohridski Blvd., 1797 Sofia, Bulgaria 18 Faculty of Forestry, University of Sarajevo, Zagrebaˇcka20, 71000 Sarajevo, Bosnia and Herzegovina 19 Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Centro de Investigación Forestal (INIA-CIFOR), 28040 Madrid, Spain 20 Department of Plant Production and Forest Resources, University of Valladolid, Avenida de Madrid 44, 34071 Palencia, Spain * Correspondence: mff[email protected]; Tel.: +34-979-108-392

Received: 11 June 2019; Accepted: 25 July 2019; Published: 1 August 2019

Abstract: Pine pitch canker (PPC), caused by the pathogenic fungus Fusarium circinatum (Nirenberg and O’ Donnell), is a serious threat to pine forests globally. The recent introduction of the pathogen

Forests 2019, 10, 649; doi:10.3390/f10080649 www.mdpi.com/journal/forests Forests 2019, 10, 649 2 of 34

to Southern Europe and its spread in Mediterranean region is alarming considering the immense ecological and economic importance of pines in the region. Pines in forests and nurseries can be infected, resulting in severe growth losses and mortality. The pathogen is known to spread in plants for planting and in seeds, and results from recent studies have indicated that F. circinatum may also spread through phoretic associations with certain insects. With this review, we aim to expand the current understanding of the risk of insect-mediated spread of PPC in diﬀerent parts of Europe. Through the joint action of a multinational researcher team, we collate the existing information about the insect species spectrum in diﬀerent biogeographic conditions and scrutinize the potential of these insects to transmit F. circinatum spores in forests and nurseries. We also discuss the impact of environmental factors and forest management in this context. We present evidence for the existence of a high diversity of insects with potential to weaken pines and disseminate PPC in Europe, including several common beetle species. In many parts of Europe, temperatures are projected to rise, which may promote the activity of several insect species, supporting multivoltinism and thus, further amplifying the risk of insect-mediated dissemination of PPC. Integrated pest management (IPM) solutions that comply with forest management practices need to be developed to reduce this risk. We recommend careful monitoring of insect populations as the basis for successful IPM. Improved understanding of environmental control of the interaction between insects, the pathogen, and host trees is needed in order to support development of bio-rational strategies to safeguard European pine trees and forests against F. circinatum in future.

Keywords: pine pitch canker; vectors; carriers; wounding agents; agro-climatic risk zones of the European and Mediterranean Plant Protection Organization; environmental factors; management; control; legislation compliance

1. Introduction Pine pitch canker (PPC), caused by the ascomycete fungus Fusarium circinatum (Nirenberg and O’Donnell), is a severe disease of Pinus spp. and Pseudotsuga menziesii (Mirb.) Franco [1]. The disease, which can lead to severe damage and even mortality of seeds, seedlings, and large trees, was recently introduced into Europe, where its currently known distribution is limited to the Mediterranean and Southern Europe (Spain, Portugal, France, and Italy [2]). Multiple factors determine the risk of further spread of F. circinatum in Europe, namely the presence of susceptible conifer hosts, climatic conditions, and diverse human-mediated activities (e.g., attempts to adapt to climate change by northward transfer of southern provenances or unintentional spreading from nurseries). In addition, phoretic associations between F. circinatum and some insect species have been demonstrated and other insects may create infection courts by wounding the trees [3–5], indicating that insects may significantly contribute to the spread of the pathogen. In this group of potential spore-transmitting insects are included the vectors that carry the pathogen (visiting susceptible plant hosts and capable of successfully transmitting the pathogen to plants not yet infected); the carriers (carrying inoculum from diseased plants which they visited before or on which they have developed); and the wounding insects (facilitating the pathogen to enter the host plant via damages caused by the feeding on shoots, twigs, and cones or due to their entrance holes in the bark and maternal galleries in the phloem). Möykkynen et al. [6] developed a model simulating the spread of F. circinatum in Europe, suggesting that the fungus is likely to disseminate to pine forests in Northern Spain and Southwest France, close to the existing affected areas. Although the authors considered the possible flight distance of the insects in the model, they did not discriminate between insect species or consider their European distribution ranges. Forests 2019, 10, 649 3 of 34

The presence or absence of possible vectors of F. circinatum and their local abundance has not been investigated in detail in earlier studies. Yet, because insects are likely to play a significant role in the spreading of PPC, these aspects should be included in assessments of the risks of PPC in Europe. Several potential insect vectors, such as pine shoot beetles (Tomicus spp.) and twig beetles (Pityophthorus spp.), are widespread and abundant in pine forests throughout Europe. There are, however, variations in the prevailing forest insect species between the different European biogeographic regions, which can shape the potential risk of F. circinatum establishment, dispersal, and impact. The activity of insects is strongly and directly affected by abiotic conditions, such as the temperature and humidity regimes, which may also influence the ability of the trees to resist insect attacks (e.g., drought stress may increase the vulnerability of trees to insect damage). An additional factor influencing not only the insects’ environment (e.g., the age structure and species composition of the forests), but also the possibilities to control their populations through different interventions, is the forest management approach (FMA) that is practiced in the area [7]. The prevailing FMAs are largely dependent of, and differ across, the biogeographic regions, setting the practical and regulative frameworks for the different interventions to control the insects [8,9]. For instance, in areas dedicated to nature conservation, interventions are restricted; whereas in areas dominated by intensive management, a broader spectrum of control methods is applicable. Thus, the biogeographic regions and FMAs create a complex framework for the activity of the potential vector insects and for their management, shaping the risk of PPC spread in Europe. This framework should be considered when optimizing bio-rational control strategies against vector insects. The goal of this review is to expand our understanding of the risk of PPC spread in different parts of Europe, considering the activity of potential vector insects (sensu lato) across the different biogeographic conditions and forest management approaches, and exploring the possibilities to control the vector insects through different pest management options. Specifically, we compiled information about the predominant forest insect pests (including those typical for plantations and nurseries), gathering information also from “grey literature” (e.g., publications in native languages, academic thesis, reports, working papers, and government documents). Data collection was made separately for European biogeographic regions, using the agro-climatic classification suggested by Bouma [10], which divides the European and Mediterranean Plant Protection Organization (EPPO) region into four prevailing agro-climatic zones (Mediterranean, Maritime, North-East, and Central), while comparing the dominant climate conditions which affect pest/host interrelationships. We then summarize the regulative effects of abiotic environment on the three partners of the interaction (insects, pathogen, and host trees), and discuss the practical possibilities for sustainable management of vector insects across different forest management regimes, using a classification of forest management approaches by Duncker et al. [8] and Hengeveld et al. [9] as a guideline.

2. Potential Spore-Transmitting Insects in the Biogeographic Regions

2.1. Mediterranean Agro-Climatic Zone The Mediterranean zone comprises the countries (or parts of countries) around the Mediterranean Sea, together with The Republic of North Macedonia and Portugal. This region is characterized by its mild and relatively wet winters, and warm and dry summers [10]. This is one of the world’s recognized “hotspots” of biodiversity and a major center of plant diversity, as approximately 10% of the world’s higher plants can be found in this area, representing only 1.6% of the Earth’s surface [11]. Forests 2019, 10, 649 4 of 34

The Mediterranean basin is particularly vulnerable to the expansion of PPC, due to favorable climatic conditions, presence of various conifer hosts, and high diversity and abundance of possible insect vectors. Of the ca. 350 species of bark beetles (Coleoptera: Curculionidae) known to occur in Western Europe [12], 42 species live only or mainly on Mediterranean conifers, and are mostly associated with pines [13]. Although some species are endemic and have restricted distribution, others are found in several countries or in the entire Mediterranean basin, including primary forest pests such as pine shoot beetles (Coleoptera: Curculionidae) of the genus Tomicus, which are known plausible vectors of F. circinatum [14]. Tomicus destruens (Wollaston, 1865) is the most thermophilic species of its genus [15] and it thrives in coastal areas of circum-Mediterranean countries [16], causing pine mortality from Portugal in the west [17,18] to Lebanon in the east [19]. A sister species, Tomicus piniperda (Linnaeus, 1758), is abundant and widespread in Southern Europe, frequently infesting pine stands in several countries [20,21], and also considered a major pest. This species attacks shoots when callow adults emerge and flies to nearby tree crowns for maturation feeding. Through this feeding on current year shoots, T. piniperda can effectively transfer F. circinatum into living tissues of pines, which makes this insect particularly dangerous as a vector of F. circinatum and results in a high risk for the establishment of the disease wherever Tomicus beetles are present [14]. A high risk is also associated with twig beetles (Pityophthorus spp.) (Coleoptera: Curculionidae), a large group of similar species with analogous ecological characteristics. Considered secondary forest pests with negligible economic impacts [22,23], more than 20 species and sub-species of twig beetles occur in Europe, widely spread in the Mediterranean basin and mainly associated with conifers [24]. In Spain, Pityophthorus pubescens (Marsham, 1802) is known to be associated with F. circinatum [2,25,26], and therefore it can be assumed that other congeneric species may similarly act as vectors of the fungus elsewhere in Europe. Exotic twig beetles have successfully established in Europe, e.g., Pityophthorus juglandis Blackman, 1928 in Italy [27] and Pityophthorus solus (Blackman, 1928) collected at a Pinus radiata D. Don sawmill in Northern Spain [28], which constitutes an additional risk for novel alien’s species associations with F. circinatum in Europe. Europe´s Mediterranean zone is rich in alien bark beetles [29], which could potentially vector F. circinatum; one example being Hypothenemus eruditus Westwood, 1936 found in Northern Spain [30]. Other noteworthy bark beetles in the Mediterranean zone are Ips and Orthotomicus species, many of which have been associated with high pine mortality or reduced forest health following drought episodes or forest fires [13]. Species associated with pine mortality include Ips sexdentatus (Börner, 1776) [31–35], Ips acuminatus (Gyllenhal, 1827) [36], and Orthotomicus erosus (Wollaston, 1857) [37,38]. Areas prone to repeated forest fires are at particularly high risk for the dissemination of F. circinatum, with the scorched and burned trees attracting pyrophilous (“fire loving”) bark and wood boring beetles, which can locally reach high population levels (e.g., [31,32,37,39]). Cone-associated insects are ecologically and economically important in the Mediterranean region, with species such as Pissodes validirostris (C.R. Sahlberg, 1834) (Coleoptera: Curculionidae), Dioryctria mendacella (Staudinger, 1859) (Lepidoptera: Pyralidae), and Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) considered primary pests of cones and edible seeds of Pinus pinea Linnaeus and other pines [40,41]. These three species are widespread and abundant in southern Europe. Originally North American, L. occidentalis is of particular interest, as it has demonstrated enormous ecological adaptability by establishing on available habitats across the entire European continent within a decade [42–44] after its original detection in Italy in 1999 [45,46]. In most countries, rapid spread and increasing population density were observed shortly after detection. Although this heteropteran demonstrates high reproductive and dispersal capabilities and is able of flying long distances, it also benefits from human-mediated translocation on conifer hosts with eggs, nymphs, and adults on them [47]. The feeding activity of adults and nymphs causes the abortion and infertility of seeds [48–50], leading to significant economic impacts for forestry, which are particularly important for Pinus pinea cone production in the Mediterranean area. Since the introduction of L. occidentalis, the production of the later pine nuts has decreased sharply in Italy and in other European countries [51]. Forests 2019, 10, 649 5 of 34

The presence of insects has been suggested as one of the causes of the massive conelet abortion before ripening (known as the “dry cone syndrome”), observed with increasing frequency in southern Europe [52]. Furthermore, in Europe, L. occidentalis is associated with the native fungus Diplodia pinea (Desm.), a pathogen that also affects seed and cone production [53,54]. Overall, this widespread and damaging insect may contribute to the spreading of F. circinatum through its feeding activity (which may provide gates of infection for the pathogen). Its association with multiple conifers (mainly pines, but also species of genera Abies, Calocedrus, Cedrus, Cupressus, Juniperus, Picea, Pseudotsuga, and Tsuga [49]), and its enormous adaptability and ecological plasticity, result in an extremely well-succeeded exotic pest affecting Europe’s conifer forests. Another about 20 insect species are associated with cones of pines in the Mediterranean basin, including members of the families Anobiidae (Coleoptera), Cecidomyiidae (Diptera), Pentatomidae (Hemiptera), Olethreutidae, Pyralidae, and Tortricidae (Lepidoptera) [40,55]. The role of these species in spreading of F. circinatum is unknown, but their feeding habits, polyphagy within pines and other conifers, abundance, and widespread distribution imply risks, which need to be evaluated. Insects associated with nurseries and young pine plantations need to be considered for their risk. In the Mediterranean zone, special attention should be given to Pissodes castaneus (De Geer, 1775) (Coleoptera: Curculionidae), a thermophilous pine weevil which feeds on the inner bark and cambium of several pine species. Although, in general, European pine weevil species are generally considered secondary pests [56], this species is known to have a significant economic impact by causing mortality in regenerating stands and young (4–15-years-old) trees [57–59]. It can also be found on older trees and even in pine stumps [60,61]. The beetle usually attacks conifers which have been weakened by other abiotic or biotic agents [60,62]. In Italy, P. castaneus has been found damaging pine trees previously weakened by the scale, Matsucoccus feytaudi Ducasse, 1941 (Hemiptera: Margarodidae) [63], and in Spain it has been found after fires [64]. In contrast, in the south of France, this insect appears to be a primary pest of Pinus pinaster Aiton, without other agents associated [65]. The damage, polyphagy within pines, widespread distribution, and ability to attack trees of different ages, implies a higher risk for the dissemination of F. circinatum in areas where pine weevils (Coleoptera: Curculionidae) are abundant. Several other insects can be regarded as potential indirect vectors of F. circinatum, including species which experience population outbreaks affecting the health condition of pine forests. This is the case for sawyer beetles of the genus Monochamus, with five European species colonizing pines and other conifers which are weakened or recently killed by other insects or by abiotic factors [66,67], including forest fires [39,68,69]. In such situations, sawyer beetle populations can rapidly increase and exhibit unusual aggressive behavior [70,71]. Maturation feeding of millions of insects causes branch dieback, defoliation, and tree weakening, which predisposes the trees to subsequent attacks by other pests and diseases [72]. A comparable situation was reported from Portugal, where the pine sawyer Monochamus galloprovincialis (Oliver, 1795) (Coleoptera: Cerambycidae) was the vector of the pine wood nematode Bursaphelenchus xylophilus (Steiner and Buhrer, 1934) (Nematoda: Parasitaphelenchidae) and experienced an enormous increase of its population after the pest was introduced, hazarding the sustainability of P. pinaster forests ecosystems [73]. Moreover, the presence of a large number of dead and dying pines gave rise to outbreaks of bark beetles such as O. erosus, I. sexdentatus and T. destruens [18,74], which affected the sanitary condition of the pine forests. Another risk species is the pine processionary moth, Thaumetopoea pityocampa (Denis and Schiffermüller, 1775) (Lepidoptera: Notodontidae), considered the most damaging defoliator of pines [75], and widespread in Mediterranean forests, southwestern Europe, and the Balkan Peninsula [76]. This moth can be extremely abundant and exhibits periodic outbreaks with a cycle of seven to nine years [77], causing severe and/or repeated defoliations, resulting in a severe growth reduction, tree decline, and even pine mortality [78–80]. These outbreaks favor the attack by other pests such as bark beetles [17,60], and can indirectly favor the dissemination of F. circinatum in affected areas. Forests 2019, 10, 649 6 of 34

In conclusion, there are several insect species with the potential to weaken pines and disseminate PPC in the Mediterranean basin. Some of them are known to cause severe, periodic or chronic damage to pines. Any activity of these insects should thus be considered a factor that directly or indirectly increases the vulnerability of pine forests to PPC in the Mediterranean region.

2.2. Maritime Agro-Climatic Zone The Maritime zone comprises areas north of the line from the coastal zone of south-west France, the south border of Switzerland and Austria, west of the border between Austria and Hungary, west of the border between Czech Republic and Slovakia, and west of the river Oder between Poland and Germany. It also includes Ireland, southern parts of Sweden and Norway, and the United Kingdom. Climatically, this region is characterized by moderately cool or cold winter and fairly mild summer temperatures, with relatively wet winters and wet to occasionally dry summers [10]. The climate is strongly conditioned by the Gulf Stream, which keeps mild air (for the latitude) over northwestern Europe in the winter months, especially in Ireland and the United Kingdom. Several potential conifer hosts of F. circinatum occur in Europe´s Maritime zone, including important species in the natural and planted forests such as Pinus cembra Linnaeus, Pinus mugo Turra, Pinus nigra Arnold, Pinus sylvestris Linnaeus, and Pinus contorta Douglas, with the climatic conditions being suitable for the development of PPC [81,82]. While F. circinatum has already been reported within the Maritime zone in France, it is currently considered eradicated there [83]. In surveys of pine and Pseudotsuga menziesii (Mirb.) plantations and conifer nurseries in Germany, Sweden, Switzerland, and Austria, the pathogen has not been found. However, Möykkynen et al. [6] modeled the spread of the pathogen from specified points of entry such as harbors and infected nurseries with a 100-year simulation, assuming new arrivals and infestations of F. circinatum in France, Benelux countries, Germany, and Poland. They concluded that the highest risk of establishment was in central France and Northern Germany. The closeness of the zone to the Mediterranean zone where risk of PPC is high, the presence of susceptible hosts, and climatic conditions that allow disease establishment emphasize the importance of careful monitoring of the situation in this zone. Moreover, several possible insect vectors of F. circinatum occur in the region and need to be considered when assessing the risk of PPC spread in the Maritime zone. Some of the most important vectors of PPC that are active in the Maritime zone are the pine shoot beetles. Tomicus piniperda is one the most destructive pine shoot pests in this zone, where it has been reported in several countries, e.g., Germany [84], Switzerland [85], Sweden [86,87], and Austria [88]. Tomicus minor (Hartig, 1834), also known to vector ophiostomatoid and ambrosia fungi, is also widespread across many countries in the Maritime region. In northern European forests, T. piniperda and T. minor depend almost exclusively on P. sylvestris as a host, with emerging adults feeding on vital shoots for maturation, causing considerable growth loss, and mature adults reproducing in the stems of weakened trees, slash or logs. As secondary colonizers of the stems of trees, their abundance can increase substantially following major disturbance events in the forest (e.g., windstorms) [89,90]. The common occurrence in the entire geographic range of P. sylvestris, large ecological plasticity, and a life cycle with two different periods of dispersal (the longer reproductive “spring flight” and the shorter maturation flights), combined with a destructive mode of action on pines, ability to fly several kilometres [90,91], and a demonstrated capacity to transmit blue-stain fungi, makes pine shoot beetles potential vectors of PPC throughout the Maritime region, similarly to the Mediterranean zone. Engraver beetles (Coleoptera: Curculionidae) of the genus Ips are known as vectors of the pitch canker pathogen in California [3]. Several species of these bark beetles have been reported in Europe’s Maritime zone, causing damages to conifer forests and plantations—in particular to the Swiss pines in Germany, Switzerland, and Austria [92]. Most damage reports come from Ips typographus (Linnaeus, 1758) and I. sexdentatus in Austria, Denmark, Norway, and Sweden [93–96]; I. acuminatus in Switzerland [97]; and Ips amitinus (Eichhoff, 1871) in Sweden [98]. As compared to their impact on pine forests, engraver beetles tend to cause more severe problems in Picea abies (Linnaeus) Karst. stands Forests 2019, 10, 649 7 of 34 in the Maritime region. For instance, attacks by I. typographus on P. sylvestris have been reported to be rare, mainly resulting of switching from nearby attacked P. abies trees [99]. This bark beetle has also been found to have a low preference for P. contorta [96]. On the other hand, another bark beetle, Pityogenes chalcographus (Linnaeus, 1761) that often occurs with I. typographus, commonly colonizes cut trees or parts of trees of the native P. sylvestris [100,101], and it has also been found to have a higher preference for P. contorta [96]. While these beetles might not be the primary concern as PPC vectors in the Maritime region, their involvement in dissemination cannot be excluded, especially in pine stands or nurseries near storm-felled spruce forests. Frequently occurring beetles in mid-aged and mature P. sylvestris tree stands of the Maritime region are also the pine weevils (Coleoptera: Curculionidae), such as Pissodes piniphilus (Herbst, 1797) and Pissodes pini (Linnaeus, 1758). These weevils oviposit under thin bark and have been shown to carry spores of resin top disease fungus, Endocronartium (Peridermium) pini (Willd.) Y. Hirats [102], indicating their capacity to transmit fungal diseases. In Germany, pine weevils have been reported after defoliations by the moth Lymantria monacha (Linnaeus, 1758) (Lepidoptera: Erebidae) [103]. The larvae of this species feed on pine needles. Some of the common moths causing damage on pine include Rhyacionia buoliana (Denis and Schiffmüller, 1775) (Lepidoptera: Tortricidae), which prefers two-and three-needled pines (P. sylvestris, P. mugo, and P. nigra). It destroys growing shoots and buds and it is problematic, especially in nurseries and young forests. Important defoliating pests with potential to transfer PPC or weaken pines in the Maritime region are also diprionid sawflies (Hymenoptera: Diprionidae), such as Neodiprion sertifer (Geoffroy, 1785), Microdiprion pallipes (Fallen, 1808), and Gilpinia virens (Klug, 1812) [104–106]. Their larvae cause damage on needles (young or older, depending on species). Although young and otherwise vital trees have good capacity to recover from defoliation, repeated infestations can weaken the trees, and wounds provide gates to pathogen spores, increasing the vulnerability of the trees to PPC infections. The PPC disease has been reported to spread within nurseries very rapidly, causing devastating losses [107]. The simulation model of Möykkynen et al. [6] predicted that the spread of the pathogen would affect nurseries in most of the Maritime zone. Insect vectors are likely to contribute to, and magnify, this risk. One of the most common pests of pine in nursery-produced pine plants and in reforestation areas is the weevil Hylobius abietis (Linnaeus, 1758) (Coleoptera: Curculionidae) [108]. For example, in Southern Sweden it causes significant economic losses every year, and problems may increase due to the tightened regulations regarding the use of insecticides in nurseries and in the forest production certified by the Forest Stewardship Council (FSC) [109]. The insect is attracted to clear-cuts, where the adult feeds on the stem bark of young seedlings, frequently killing newly planted seedlings. By wounding plants, it provides gates for the pathogen. Other insects associated with pine nurseries are the pine weevil P. castaneus and the bark beetle Hylastes ater (Paykull, 1800) (Coleoptera: Curculionidae), both of which have been reported in Germany, Austria, and Switzerland [28,110], and present local risk of disseminating the pathogen. To conclude, the insect fauna of the Maritime zone includes several species that are highly potent vectors for PPC. While the risk of PPC in the countries in this zone may still be relatively small due to cooler climate, it is possible that the earlier simulations and prognoses [6] have underestimated the risk by not taking into consideration the activity and dynamics of the all these insects. In the changing climate, the Maritime zone may also experience environmental changes [111] that make the conditions more favorable for many potential vector insects (e.g., by allowing several generations to develop during one growth season, [112]), and for the pathogen. Forests 2019, 10, 649 8 of 34

2.3. Central Agro-Climatic Zone The central zone comprises the countries of Bosnia-Herzegovina, Bulgaria, Croatia, Hungary, ◦ Moldova, Romania, Russian Federation south of 50 N latitude, Slovakia, Slovenia, Serbia and Montenegro, Turkey, and Ukraine, except the Mediterranean coastal zones. Moderately continental climate prevails in parts of the region, with local plant species adapted to grow in cold and relatively dry winters, and warm and dry to occasionally wet summers [10]. The territories close to the Black Sea coast extending from Sochi (Russia) to Sukhumi (Abkhazia), and further southwards in Georgia, are characterized by a humid and milder climate, with winter temperatures above freezing [113,114]. In the Central zone, a range of conifer hosts and climate conditions occur, which are suitable for the establishment and expansion of F. circinatum. The heterogeneous climatic conditions exist due to the contrasting influence of the continental and Mediterranean climate and the diverse landscapes, with extensive plains coexisting with mountain ranges. The mountains and valleys act as barriers or channels for air masses, often causing sharp contrasts in weather over relatively small temporal and spatial scales. Annual precipitation can be quite high in some regions, with mountain summits in southwestern Serbia receiving up to 1500 mm of annual precipitation. Snow cover can occur from late November to early March. The native and exotic pines commonly found in the region include P. nigra, P. sylvestris, P. mugo, P. peuce Griseb., and P. heldreichii (H. Christ), with P. nigra and P. sylvestris being the most abundant species due to planting activities. In Bosnia and Herzegovina, lack of protective measures due to economic constrains influenced the health condition of the forests, leading to the appearance of diseases and pests, and with significant economic and ecological losses in pine forests [115]. In Serbia, adverse climatic conditions (snow, ice, and strong winds) have been reported to damage P. nigra and P. sylvestris plantations, creating favorable conditions for the development and reproduction of many pine-feeding insects, such as bark beetles [116]. Similar observations have been reported also from Bulgaria [117–119] and Bosnia [115,120], where bark beetles are a key concern for the health status of local coniferous forests. The most important bark beetles associated with pines in the central zone are I. acuminatus, I. sexdentatus, T. piniperda, T. minor, and Orthotomicus laricis (Fabricius, 1792) [116,121–126]. The engraver beetle I. acuminatus appears to be the most aggressive species in the region, being locally widespread and found mainly in P. sylvestris plantations, where it causes significant economic damage due to its ability to attack healthy trees [116,119]. The related I. sexdentatus is also widely distributed in P. nigra and P. sylvestris plantations, colonizing the lower part of the host’s main trunk, while Ips mannsfeldi (Wachtl, 1879) is a more localized species which attacks mainly P. nigra stands in Bulgaria [119]. The pine shoot beetles of the genus Tomicus are also economically important pests and potential vectors of F. circinatum in the region [127–129], attacking healthy trees. They are widely distributed in P. sylvestris and P. nigra forests, and outbreaks of these insects are frequently observed in different regions of Bulgaria [118] and in neighboring countries. Other important bark beetles in the region include O. laricis, which is relatively abundant in P. sylvestris, P. nigra, and P. peuce stands, while O. erosus is found on several different pine species in Bulgaria [119] and in Bosnia and Herzegovina [129]. The bark beetles Pityogenes bidentatus (Herbst, 1784) and Pityogenes bistridentatus (Eichhoff, 1878) attack branches of multiple pine species and other conifers [116], being common in the region. On the roots, H. ater and Hylastes attenuatus (Erichson, 1836) are also common [125,126,129]. Moreover, other bark beetle species, such as Carphoborus pini Eichhoff, 1881 and Crypturgus numidicus (Ferrari, 1867) were also found in some areas [129]. Forests 2019, 10, 649 9 of 34

Longhorn beetles (Coleoptera: Cerambycidae) may also have local importance as vectors of F. circinatum in the Central zone. This family includes M. galloprovincialis, which develops on several pine tree species, mainly on P. sylvestris, P. nigra, and P. strobus Linnaeus. It is relatively local in mountainous areas of Bulgaria [130–132]. Other common species of pine sawyers, Monochamus sutor (Linnaeus, 1758) and Monochamus sartor (Fabricius, 1787), develop mainly on P.abies, and occasionally on firs and pines [131]. Other cerambycids that occur in the region include Acanthocinus griseus (Fabricius, 1792) and Acanthocinus aedilis (Linnaeus, 1758), which are relatively abundant in Bulgaria [131] in association with P. sylvestris, P. nigra, P. peuce, and P. strobus [132]. Phaenops cyanea (Fabricius, 1775) (Coleoptera: Buprestidae) is associated with pines. The larvae of this species develop between the bark and sapwood, damaging the phloem and leading to rapid weakening of the host. The attacks may cause rapid death of the trees, and severe outbreaks may profoundly change the state of the pine stands. This beetle is widespread and abundant in Bulgaria [133], being considered a destructive xylophagous pest both in pine plantations and in urban green areas [134,135]. Adding to the risk of PPC spread in the Central zone, L. occidentalis has recently colonized suitable habitats also in this region of Europe (e.g., [120,136,137]). In Bosnia and Herzegovina, the species has been found on Pinus heldreichii Christ, a rare mountainous pine species with a restricted natural distribution. In recent decades, pine weevils have been frequently found in young pine plantations due to neglected sanitary conditions in the region, namely on P. nigra, P. sylvestris, and P. strobus plantations. In Serbia, H. abietis, P. castaneus, and H. ater are reported as the most frequent and dangerous pests in plantations [121], while other species of the genus Pissodes such as P. pini, P. piceae (Illiger, 1807), P. piniphilus, and P. castaneus, as well as H. ater, damage pines in nurseries and young conifer plantations in Bulgaria [134]. Hylobius abietis has been reported causing damages on seedlings in several countries in the mid of 20th century, but more recent surveys are missing [138–143]. Rhyacionia buoliana is also reported to cause damage in pine plantations in Serbia and Bosnia, often leading to permanent crookedness of the main trunk and formation of multiple terminal shoots. On the Kozara Mountains, Preslica (Doboj) and lldjak (Visegrad) in Bosnia, R. buoliana has been found in high population densities, causing considerable reduction in height growth and density of P. sylvestris, P. nigra, and P. contorta plantations and forests [144]. Similar to other European regions, defoliating insects affect the forest’s health state in the Central zone. Thaumetopoea pityocampa is an important pine defoliator in the sub-Mediterranean climatic areas of Bosnia and Herzegovina, where the species in mainly associated with black pine [145], and in Bulgaria, where the negative economic and environmental impact of this pest has been increasing in recent decades [126]. Other defoliating insects with regional importance include Dendrolimus pini (Linnaeus, 1758) (Lepidoptera: Lasiocampidae) in the even-aged P. sylvestris stands in Bosnia [120], and sawflies N. sertifer and Diprion pini (Linnaeus, 1758) (Hymenoptera: Diprionidae); the first species abundantly widespread in Serbia and Bulgaria, while the second one is mainly reported from Bosnia and Bulgaria [120].

2.4. Northeast Agro-Climatic Zone The Northeast zone includes Poland, the Baltic countries, Ukraine, Belarus, Finland, and Russia ◦ north of 50 N latitude. The dominant climate is continental, with cold and relatively wet winters, and hot and dry summers [10]. In the area north of Odessa-Krasnodar-Sochi-Sukhumi line, extremely ◦ ◦ high summer temperatures of up to 50 C and low winter temperatures down to −40 C are found, resulting in conditions that are not appropriate for F. circinatum, which requires relatively mild temperatures for its development and for the germination of its spores [146]. Forests 2019, 10, 649 10 of 34

Bark beetles are common in the Northeast zone [147–149]. Some of them are well known vectors of ophiostomatoid fungi [150–153], indicating the potential to act as possible vectors also for F. circinatum. Tomicus piniperda and T. minor are local pests of P. sylvestris [154–157]. In warmer regions of Ukraine, Crimea, Georgia, the Western Caucasus, Russia, and Abkhazia, T. destruens is also present, mainly associated with Pinus brutia var. pityusa (Steven) Silba [158–160]. In 2014, this bark beetle was recorded in Sochi (South-west Russia) on P. pinea plants imported from Western Europe [161]. Several bark beetle species occurring in this region are potential vectors of F. circinatum, including Polygraphus poligraphus (Linnaeus, 1758), I. sexdentatus, and I. acuminatus. In southern Finland, I. acuminatus has been associated with the killing of P. sylvestris after hot and dry summers, which has resulted in an increased susceptibility of pines to insect damage [162]. Yet, the most important forest pest in this zone is I. typographus, which is inherently associated with P. abies [163,164]. In recent years, there have been reports of numerous outbreaks by I. typographus, e.g., in Poland’s Białowie˙za forest, the cyclic outbreaks of this pest have been occurring over the last decades, with an extremely severe mass outbreak enduring since 2012 [165]. Mass mortality of conifers caused by I. typographus benefits other bark and wood boring beetles, leading to a decline on the forest´s health status and, thus, increasing the risk for the spread and establishment of F. circinatum. A large number of species from the genus Pityophthorus, associated with pines, are also present in this zone, such as Pityophthorus glabratus (Eichhoff, 1878) and Pityophthorus pini (Kurentsov, 1941) [154, 156,157,166]. Another important and aggressive local forest pest is Dendroctonus micans (Kugelann, 1794) (Coleoptera: Curculionidae), affecting both young and old P. sylvestris trees [167,168]. Usually, D. micans colonizes healthy trees, but it will also attack trees that are stressed by logging damage, frost, snow, wind, lightning, poor soil nutrition or drought [169]. Similarly, P. cyanea (Fabricius, 1775) is considered an important pest of pines weakened by dry and hot summers [170], and can be a locally important pest in the Northeast agro-climatic zone [36]. Another species that benefits from availability of weakened trees is the longhorn beetle M. galloprovincialis, which is widely distributed in Russia and Ukraine [154,156,157,171]. By wounding the trees, this species can create points of entry for F. circinatum. In Poland, these beetles have been found to carry a blue-stain fungus Ophiostoma minus (Hedgc.) Syd. and P. Syd. [172], and introduction of pathogens through the cuts on the bark made by females of Monochamus spp. has been documented in coniferous stands in the Karelian Isthmus in Russia [173]. Pine weevils of the genus Pissodes are important pests on young pines in the Northeast zone, being widely distributed in the Baltic countries, Poland, Ukraine, Russia, and Finland. The most common species are P. castaneus, P. pini, and P. piniphilus [94,166,174]. Pissodes castaneus is one of the most dangerous pests of P. sylvestris plantations and natural regenerations in the Baltic region. Pine bark beetles of the genus Hylastes are also important local pests of pine seedlings, with the insects mining short galleries inside the cambium of the young pines and causing their decline or even death. There are several species present in the region, including H. ater, H. attenuatus, Hylastes brunneus Erichson, 1836, Hylastes cunicularius Erichson, 1836, Hylastes linearis Erichson, 1836, and Hylastes opacus Erichson, 1836 (Coleoptera: Curculionidae) [154,157,166,168,175,176]. The most important local pests of seedlings and plantations in the Northeast zone are the pine weevils Hylobius pinastri (Gyllenhaal, 1813) (Coleoptera: Curculionidae) and H. abietis [154,157,166,171, 177,178]. These pine weevils are widespread, abundant, and economically harmful pests in young plantations in boreal coniferous forests across the northern Palearctic region [58,179]. While H. pinastri prefers P. abies [180], H. abietis is common on pines, being an important pest of young pine stands [181] and recently felled-trees [182] throughout its distribution range in Europe, northern Asia, and Japan. It has also been found to vector the pathogenic fungi Heterobasidion parviporum Bref. and D. pinea [183,184], as well as for the saprotrophic fungus Phlebiopsis gigantea (Fr.) Jülich [185]. In Poland, H. abietis has also been found transmitting the ophiostomatoid fungi Leptographium procerum W.B. (Kendr.) M.J. Wingf. and Ophiostoma quercus (Georgev.) Nannf. to P. sylvestris seedlings [174]. Its abundance, frequency Forests 2019, 10, 649 11 of 34 as a damaging agent on pines, and recurrent association with pathogenic fungi increase the risk of it becoming associated with F. circinatum. Among the sucking insects, Aradus cinnamomeus (Panzer, 1806) (Hemiptera: Aradidae) has local importance in some regions of the Northeast zone, while the invasive L. occidentalis is widespread in suitable habitats across the region—including southern Poland [43], Ukraine, and Russia [186]—and has been locally expanding its range over the recent years [187]. This species actively flies from one pine to another to feed and breed, and during these activities, it can act as a vector for fungi. Another insect associated with cones is the pine weevil P. validirostris, which has been found damaging pine cones in several countries of the Northeast zone [157,166,188,189]. Numerous defoliating insects are common in Europe’s Northeast zone. The most important are the sawflies D. pini and N. sertifer (Hymenoptera: Diprionidae) and Acantholyda posticalis pinivora Enslin, 1918 (Hymenoptera: Pamphiliidae); and the moths Panolis flammea (Denis and Schiffermüller, 1775) (Lepidoptera: Noctuidae) and Bupalus piniaria (Linnaeus, 1758) (Lepidoptera: Geometridae) [154, 157,166,171]. The regular mass outbreaks of these insects cause significant damage in P. sylvestris forests. These species, along with T. pityocampa in the regions with warmer climate, can weaken pine stands during several years and increase the vulnerability of pines to attacks by bark and longhorn beetles. In Estonia, trees defoliated by B. piniaria are often subsequently attacked by T. piniperda and T. minor, followed by Pissodes piniphilus, and root-rot diseases caused by Heterobasidion annosum (Fr.) Bref and Armillaria spp. (Fr.) Staude [190]. The outbreaks of the defoliator pests frequently cease with the collapse of their populations. For instance, B. piniaria population peaks are often followed by high mortality caused by the entomopathogenic fungi Beauveria bassiana (Bals.) Vuillemin and Metarhizium anisopliae Metchnikoff (Sorokin) [191]. Overall, in the Northeast zone, there are several insect species with high potential to promote the spread of F. circinatum in forests, nurseries, and plantations. However, the harsh environmental conditions are likely to be suboptimal for F. circinatum, suppressing its establishment in this zone. Nevertheless, the annual mean temperatures are projected to rise in this century worldwide, with the largest warming occurring in Northern Europe during the winter months [111]. This can favor not only the PPC pathogen, but also the establishment and spread of several native and exotic insect pests by affecting their distribution, phenology, activity, and voltinism [192].

3. Environmental Attributes Influencing the PPC Disease Spreading Each agro-climatic zone is characterized by a specific regime of environmental, abiotic conditions, which are likely to profound influence in the interaction between F. circinatum, the insects, and the host pines. For instance, abiotic variables influencing insect during development from larva to adult may determine the proportion of individual beetles to become vectors, carriers, or wounding agents of F. circinatum (Table 1). Forests 2019, 10, 649 12 of 34

Table 1. Eﬀect of environmental factors and silvicultural measures on insects associated to the pine pitch canker (PPC) disease.

Insect species Factor Effect Location (host) References ◦ ◦ Temperature 17 C during the summer and 0 C during the winter months benefit Europe (Pinus spp.) [193] Fire Colonization of trees with less than 25% intact foliage South and central Sweden (Pinus sylvestris)[194] Tomicus piniperda Increased colonization Central Spain (Pinus pinaster and Pinus nigra)[31] Snow-breaks Stump colonization Central Sweden (Pinus sylvestris)[195] Artificial pruning Pruned trees more heavily attacked than unpruned trees Sweden (Pinus sylvestris)[196] Water stress Increase outbreaks Europe (Pinus sylvestris)[197] Tomicus minor Main period of dispersal in spring, when temperatures Temperature ◦ Worldwide [198] exceed 12 C in the shade Temperature Warm and dry climates Spain (Pinus spp.) [15] Tomicus destruens T. destruens has been found to preferentially attacking non-stressed pines Water stress Greenhouse (Pinus pinaster)[199] during its shoot feeding phase and to have increased fitness as a result ◦ Rhyacionia frustrana is unable to sustain flight below 9.5 C Temperature Temperature influences phenology and voltinism. Reduced male longevity during Eastern US (Pinus spp.) [200–202] Rhyacionia spp. warmer portions of the year Light Attacks of R. frustrana increase if the shade is removed Eastern US (Pinus spp.) [203] ◦ 12.2 and 35 C, lower and higher thresholds for larval development, Portugal (Pinus pinaster)[204] respectively Monochamus Temperature During hot years, larval development is faster and results in earlier galloprovincialis Portugal (Pinus pinaster)[205] emergences ◦ −7 C, threshold of mean minimum temperature in winter for beetle survival Europe (Pinus spp.) [206] Elevation 1590 m threshold for beetle survival Pyrenees (Pinus uncinata)[206] Ips sexdentatus Fire Increased colonization Central Spain (Pinus pinaster and Pinus nigra)[31] ◦ 6 and 14 C, for spring emergence and brood development, respectively South-eastern Alps (Pinus sylvestris)[207] Ips acuminatus Temperature ◦ At 18 C flight starts Central Spain (Pinus sylvestris)[208] Stressed seedlings less attacked but more girdled Drought New Zealand (Pinus radiata)[209] Hylastes ater than non-stressed seedlings Catches decrease with increasing elevation. Beetles caught at north-facing Elevation and aspect than at south-facing sites towards the end of the flight season in autumn, South Island, New Zealand (Pinus radiata)[210] leading to an extended flight period at northerly aspects Soil preparation, soil scarification and Reduces seedling attack and plant mortality Southern Sweden (Picea abies)[211,212] physical protection of plants Water stress Significantly greater girdling in water stressed plants Central Finland (Pinus sylvestris)[213] Hylobius abietis P fertilization Increases the attack of seedlings Northwest Spain (Pinus pinaster)[214] Earlier emergence, shortened generation time, favor univoltine life cycles, Increments of temperature Southern England (Pinus sylvestris and Pinus nigra) [212,215] and increase weevil populations and damages to transplants Temperature sum at the location and Central Sweden (Picea abies, Pinus sylvestris, Directly and inversely related to weevil damage level, respectively [212] age of clear-cut at the time of planting and Pinus contorta) Forests 2019, 10, 649 13 of 34

Nevertheless, the detailed effects of different environmental variables on this interaction during the development of PPC disease are challenging to describe, because of the spatial and temporal dynamics that are typical for these factors and for the multiple biotic interactions involved. Because different interactions are likely to occur simultaneously in the affected trees and stands, it is difficult to identify which factors significantly affect the epidemiology. At the landscape level, abiotic factors have a strong influence on the distribution and abundance of potential spore-transmitting insects, and thereby on the potential rate at which pitch canker is spreading. A survey performed in California reported the severity of PPC associated with landscape type and geographic factors [216]. Among other causes, differences in disease intensity between inland and coastal locations were attributed to differences in the abundance of insects that vectored the disease and/or served as wounding agents. For example, the spittlebug Aphrophora canadensis (Walley, 1928) (Hemiptera: Aphrophoridae) is more common in coastal areas than in inland [216], and since it causes wounds associated with F. circinatum infections [217], its occurrence may have contributed to greater disease severity near the coast. Temperature regime has a profound effect on most biological interactions. Ambient temperature can directly influence the insect (activity, metabolism), the fungus (sporulation, germination), or the host (defensive metabolism). It is well documented that certain external temperature thresholds have ◦ to be reached before insects emerge and fly (10 C for the early flier T. piniperda), but their feeding ◦ activity is also modified by temperature [218]. As the air temperature increases to 25 C and above, bark beetles become more active and move energetically, and this likely increases the probability that the spores of F. circinatum on the exoskeleton of the insects are scraped onto the surface of feeding wounds. Temperature can also have an impact on a micro-scale within and around the feeding gallery, although the quantity of viable spores delivered by an insect to a feeding groove is probably the most critical factor in whether or not infection of the phloem, pith, and ultimately the entire branch, takes place. High level of humidity around a feeding gallery may enhance the probability of infection [219] and it even reduces the number of spores needed for infection (see below). For bark beetles such as Pityophthorus spp. that create only shallow wounds, the frequency of infection will likely be strongly influenced by the availability of ambient moisture or high humidity [220]. In contrast, other bark beetles that tunnel deeper into healthy tissue, such as Conophthorus radiatae (Hopkins, 1915) (Coleoptera: Curculionidae), can deliver inoculum to sites where the germination of the spores is less influenced by ambient conditions. This distinction should be incorporated into risk models, which are generally based on climate and assume that ambient conditions will have a determinative effect on the infection process. The presence of viable spores in the environment and their movement with insect vectors are crucial factors in PPC epidemiology, which is strongly affected by the environmental factors. The airborne inoculum of F. circinatum could be used as a proxy of the potential risk of transmittance. In northwest Spain, airborne spores have been found to have a permanent occurrence throughout the whole year, with a slight trend to be higher after low air temperatures and low leaf wetness [221]. Neither air humidity nor rainfall had a significant impact on spore abundance in the air [221]. However, passive deposition of inoculum may be supported by rainfall, as the rain drops trap the aerial spores and can deliver it to the wounds. In California (USA), more spores were detected in months colder than June and July [222] and sea fog alleviated the water deficit during dry periods in summer, enhancing the ◦ fungal sporulation [223]. The pathogen’s demand of temperatures around 20 C, and the limiting effect of extremely high temperatures for developing fruiting structures such as phialides and sporodochia, ◦ may determine the abundance of F. circinatum air spores. Inman et al. [146] revealed that at 20 C, the germination of spores was more than 20%. However, the presence of water on the host surface does not favor the development of fructification structures [221]. Thus, optimal conditions for sporulation appear to be different from those needed for spore germination, creating difficulties when describing PPC disease spread by insects. Forests 2019, 10, 649 14 of 34

The number of spores that are required for infection probably depends, at least in part, on the species of pine, its genetic level of resistance, and also its seasonal susceptibility. It is estimated that some twig beetles (Pityophthorus spp.) carry less than ten F. circinatum spores per individual [224], whereas Ips spp. were found to carry as many as 300 spores [225]. An additional factor in the success of disease transmission is the amount of inoculum carried by insect vectors, which depends on the insect size and the extent to which F. circinatum colonizes and sporulates on the walls of each pupal chamber. This, in turn, is probably influenced by the length of time the beetle remains within the chamber and environmental conditions. From a total of 118 T. piniperda specimens collected in northern Spain between May and July from P. radiata trees with symptoms of pitch canker disease, F. circinatum was isolated with 15, 13, 15, and 33% success from larvae, pupae, F1 adults, and parental adults, respectively [14]. More individuals will carry the pathogen if environmental conditions are likely to favor the development of F. circinatum in pupal chambers and feeding galleries. Mycelial growth rates in vitro ◦ ◦ ◦ ◦ were highest at 25 C and progressively decreased at 20 C, 15 C, and 10 C, and spore germination was ◦ ◦ also reported to occur more rapidly at 20 C than at 10 C[146]. It is suggested that low temperatures during spring will inhibit sporulation in pupal chambers and very hot temperatures during the summer will inhibit sporulation in feeding galleries (e.g., those of T. piniperda), since F. circinatum does not ◦ survive above 50 C[226]. The summer-emerging adults of Pityophthorus spp. may be less effective vectors than the spring-emerging adults, because the time spent in pupal chambers in summer may be brief, with little time for the developing adult to come into contact with spores. Tomicus piniperda adults are especially active in June, often residing within a shoot for less than two weeks. In contrast, by late summer (e.g., September), fewer beetles—and even fewer newly attacked but empty shoots—are found [227], indicating that T. piniperda adults are less likely to infect new trees in late summer. Several abiotic factors, such as water deficit, fire, and fertilization, may influence the susceptibility of the trees to insect attacks [31,194,228,229]. In some circumstances, these factors may be related to increased damage caused by F. circinatum. For instance, an association between drought and rapid spread of the disease has been observed in Florida [230] and California (USA), with high mortality of stands situated on soils with poor water holding capacity [231]. Susceptibility to PPC increases during water stress, waterlogging or shallow soils, especially when trees are planted at high-stand densities [1]. Fire-damaged stands may attract large numbers of primary bark beetles such as T. piniperda and I. sexdentatus [31,194] (Table 1), which increases the chances of outbreaks and disease transmission. As these insects are dependent on host trees with reduced vigor for successful reproduction, a feedback between insect population and PPC disease is expected. Outbreaks of pitch canker have also been associated with use of poultry manure [232], applications of high levels of chemical fertilizers [233,234], and nitrogen emissions from air-conditioned chicken houses [235]. Heavy fertilization may make pine tissues more succulent, facilitating the entry of the fungus, suppressing defensive mechanisms such as phenolic metabolism [236] or increase the attraction of insect vectors or insects causing suitable infection courts for the pitch canker. The effect of beetle host selection of beetles under different drought stress and nutrient availability regimes is probably mediated by the environmentally induced changes in resin duct characteristics, as reported elsewhere [229,237], but this needs to be tested in the pitch canker disease epidemiology. More information is also needed about the impacts of heat stress and fires on tree susceptibility to insects and F. circinatum infection.

4. Management Options to Control the Potential Spore-Transmitting Insects

4.1. Management Options The reported management options against potential insect vectors of PPC fall to four basic categories: Mechanical control (including silvicultural operations), chemical control (including both synthetic insecticides and natural and low risk chemicals), semiochemical control (including pheromones), and biological control (using parasites or predators or natural resistance of the tree). Forests 2019, 10, 649 15 of 34

While a comprehensive exploration of these categories is beyond the scope of this review, the following sections provide a brief presentation of each category, with selected examples from literature.

4.1.1. Mechanical Control Management of potential insect populations through mechanical measures includes sanitary measures and utilization of silvicultural operations to manipulate stand structure and conditions in a way that may suppresses vector insect populations. The successful application of these methods requires a good knowledge of the targeted and non-targeted environmental effects of the measures. For instance, storage of fresh logging residues and freshly cut stumps can attract pine weevils to close-by regeneration areas, and should therefore be avoided [238]. Scarification and uprooting of stumps for increased biomass uptake has been suggested as a means to reduce substrate for H. abietis, although contrasting results have also been obtained [238,239]. In pine wilt-affected zones in southern Portugal, the felling and removal of dead and dying trees during the winter months is used to prevent emergence of M. galloprovincialis carrying the pine wood nematode, thus preventing new infections of healthy pines. This process, although expensive and time consuming, is the most successful way to control pine wilt disease [73]. Silvicultural practices that improve tree vigour have been successfully applied to reduce stand susceptibility to damage from bark and wood-boring insects, which often exploit trees of low vigour [7]. For instance, Wermelinger [240] and Göthlin et al. [241] propose the preventive elimination of reproduction substrate for bark borers, such as the remains of wood existing in the forest or the felling of infested trees. These measures can be very effective and increase the mortality of the bark beetles up to 93% when the colonized trees are eliminated before the emergence of the beetles, and the infected logs are removed from the forest. Mechanical control of bark and root borers of the genus Pissodes involves removing infested branches and destroying them to reduce populations [242]. In some studies, however, the method resulted in high costs and unsatisfactory results [243]. Yet, in specific circumstances, it could be an efficient method [244]. In the EU, the interest in mechanical solutions is likely to further increase since the use of insecticides in forests is increasingly regulated, due to risk of non-targeted effects on environment (e.g., on pollinator populations) and on human health. For instance, in Sweden, insecticide containing a neonicotinoid imidacloprid was used in control of H. abietis until 2018, but after EU Commission prohibited use of this compound [245], the use of pesticides to control H. abietis is being phased out and replaced by combinations of stem coatings and silvicultural countermeasures [246]. In mechanical control of H. abietis, collars or coatings can be used to prevent the insects from reaching the bark. One of the newest methods against attacks by H. abietis was developed in Sweden and involves the automatic treatment of seedlings with wax and sand that prevents insects from consuming the bark of the seedlings [247]. The product utilizes knowledge from behavioral studies that showed how sand with a grain size less than 0.2 mm stops H. abietis feeding as the grains enter in between its mandibles. In addition, forest managers apply a variety of damage-reducing measures, such as site preparation followed by an optimal choice of planting spot, timing of planting, plant type, and plant size to protect the plants [212].

4.1.2. Chemical Control The EU has strict regulations about use of pesticides in all plant production, including forest tree nurseries and forest settings. For instance, several of the chemicals that have earlier been reported in the USA as active components in control of T. piniperda (chlorpyrifos, lindane, cyfluthrin, bifenthrin, esfenvalerate, lambda-cyhalothrin, and carbaryl [248]) are not approved for use as pesticides in the EU or their approval is soon expiring. Recent changes in relevant EU regulations include, e.g., prohibition of neonicotinoids which were used in control of H. abietis (see above). This development directly implements EU Directive 2009/128/EC [249], which aims at sustainable use of pesticides in the EU and reduction of the risks and impacts of pesticide use on human health and the environment. The same Forests 2019, 10, 649 16 of 34 directive promotes the use of integrated pest management (IPM) and of alternative approaches or techniques, such as non-chemical alternatives to pesticides. While the applicability of insecticides as solutions to suppress potential PPC vector insects may be restricted in the future, the topic has received considerable interest in earlier research. While chemical control can cause negative effects on the forest´s biodiversity and human activities, in some cases, it may be the only effective option to control the pests. For instance, the flat bug A. cinnamomeus is a serious pest of pines in Northern Europe, causing remarkable growth delays [250]. The only option to control this species consists of chemical treatments with insecticides [251]. In other cases, chemical treatments are considered as just one of the several components of IPM. For example, it has been reported that control of shoot feeders (Tomicus spp., Monochamus spp.) includes forest sanitation measures in order to reduce the amount of material available for reproduction, the use of trap trees (logs) for attracting adults, and the use of insecticides to control feeding in shoots [252]. The effectiveness of chemical treatments may vary considerably. The chemical control of bark and root borers (Pissodes spp.) can be carried out in small trees (four years), and consists of spraying insects with insecticide [253]. According to these authors, significant reductions in attacks were achieved due to the mortality of the insects when synthetic pyrethroids were used. Iede et al. [254], meanwhile, mention that the chemical approach is not very effective, even in the case of treatments with fenitrothion (only authorized outside the EU) because insects often hide in the ground or in the cracks of the bark. On the contrary, Fraser and Heppner [255] reported good results when injecting the stem of P. strobus, the first year after application. It should, however, not be forgotten that just like for any chemicals, resistance against insecticides may appear in the insect population after long-term and repeated exposure [41]. Chemical control requires the use of different substrates treated with insecticides that insects will come into contact with. Especially in forests, the use of chemicals is challenged by the difficulty of applying the compounds to the right place and at the right time. Earlier, aerial spraying was an option to spread the insecticides to forests, but this method is banned in EU countries [256]. Preventive trunk injection of insecticides is an alternative method to control forest and urban pests, and although being labor-consuming and expensive, it can successfully protect healthy trees against insect pests for several years [257–259]. Trap trees have been used as devices to expose engraver beetles (e.g., I. sexdentatus; O. erosus; Hylurgops palliatus (Gyllenhal, 1813) (Coleoptera: Curculionidae); H. eruditus; and Hylurgus ligniperda (Fabricius, 1787) (Coleoptera: Curculionidae)) to insecticides. To increase attractiveness, they can be baited with commercial pheromones placed directly on the trees [260] or inside devices, such as tripods widely used in some countries [261]. Another chemical method for mass suppression of bark beetles consists of using insecticide-immersed nets to protect logs or wood stocks. These nets are made of synthetic textile fiber imbibed with insecticide (usually pyrethroids) which is applied on the surface of the trees, creating a mechanical barrier for beetles that want to colonize the logs. Because of the contact with the insecticide from the net, the beetle is intoxicated and dies very quickly [262]. The insecticide nets are also used to cover wood infested with the pine wood nematode (B. xylophilus) for transport in trucks, in order to prevent the dissemination of the nematode and of its insect vector [74]. One way to apply chemicals is the use of toxic bark (fir or pine bark of 30 cm x 30 cm containing insecticides and adhesives), which has been tested against H. abietis. Pine weevils are attracted by the smell of the fresh bark and are poisoned. However, the method requires a lot of work and it is only widely used in Eastern Europe [59,260]. Insects may also be difficult to treat with chemicals because of their spatial location inside the tissue. For instance, the main challenge in chemical control against Monochamus spp. is how to apply the insecticide so that it is effective against xylophagous larvae. Similarly, cone insects (P. validirostris, L. occidentalis) are not readily exposed to chemicals due to their feeding inside the cones, where they are difficult to detect. Yet, the most well-known control methods of P. validirostris are chemical treatments [41]. So far, no specific chemical control methods are known for L. occidentalis but insecticides such as dimethoate, carbaryl, synthetic pyrethroid, and permethrin used to control other insects can Forests 2019, 10, 649 17 of 34 provide protection for pine cones [263–266]. In addition, the same authors suggest that visual traps (which emit light at visible wavelengths and inflected wavelengths) would be effective for mass capture of adults.

4.1.3. Semiochemical Control Other types of chemicals with significance in pest control are semiochemicals, which are chemical compounds that many insects release and use in intra- and interspecific communication [267]. The olfactory system of insects is advanced, allowing them to detect volatile signals from congeneric individuals and trees, which then guides their behaviors, such as oviposition or host selection. Thus, semiochemicals can be used in pest monitoring or control, e.g., in pheromone traps. For example, for the genus Ips, in order to be efficient, the couple of one trap and one bait must capture on entire season thousands of adult insects [268]. A mixture of a volatile host compounds, alpha-pinene, ipsenol, and 2-methyl-3-buten-2-ol has been patented as an attractant for M. galloprovincialis adults [269], and later improved by Álvarez et al. [270] by adding a thin layer of Teflon in the traps and collection jars to prevent the escape of the individuals. The traps have to be installed in early summer near susceptible areas and must be periodically inspected. However, despite being effective for monitoring their use for mass-control of the insect populations, they still require substantial improving [271]. To capture engraver beetles, pheromone traps are also placed early in the spring, before the beginning of the flight of the insect, and are kept in the field until the end of their flight period [272]. For good results, long-term pheromone lures (four to five months) or the replacement of the lures with shorter release periods (a few weeks) is recommended. The pheromone method has been reported to be ineffective against H. abietis, even when a large number of traps were used (100 traps/ha) [273]. Encouraging results have also been obtained with the development of pheromone baits to catch twig beetles such as P. pubescens. For example, Lopez et al. [274] obtained good results in the Basque Country (Spain) using combinations of (E)-(+)-pityol and its racemic form, (E)-(±)-pityol. Moreover, the authors suggest using it as a potential mate-finding disruptor in the field due to its strong attractive effect. Some authors state that this method has some limitation, saying that pheromone traps capture only between 10–15% of bark beetles [275], which at some point could lead to a reduction in competition between beetles and the prolongation of the gradation period. A special case of this method is represented by the anti-pheromones (anti-aggregative) which act like repellents for some Ips and Tomicus species [276].

4.1.4. Biological Control Use of natural enemies (parasites or predators) as biological control agents to control insect pests may provide sustainable solutions for control of several potential vector insects. Wegensteiner et al. [277] listed for Ips, Tomicus, and Orthotomicus species, more than 400 natural enemy species, which include birds (mostly, woodpeckers), Coleoptera (around 165 species), Diptera, Hemiptera, and parasitoids (mostly, Braconidae and Pteromalidae; Hymenoptera), as well as other pathogens such as viruses, bacteria, fungi, and algae. One of the best-known biological solutions in the control of forest insects includes the use of virus to suppress the population of the pine sawﬂy, N. sertifer [278]. In several other cases, promising results have been obtained, and detailed knowledge about biological systems is developing. For instance, the biological control of Tomicus spp. includes the use of the predator Thanasimus formicarius (Linnaeus, 1758) (Coleoptera: Cleridae), the threshold ﬂight temperature of which closely matches that of T. piniperda. Moreover, T. formicarius is attracted by host volatiles such as alpha-pinene, and it is commonly associated with T. piniperda throughout Eurasia, causing high levels of mortality [279–281]. Another predator is Rhizophagus grandis Gyllenhal, 1827 (Coleoptera: Monotomidae) that has been used to control D. micans through inundation of stands with R. grandis at the leading edge of infested areas [169]. For the genus Ips, the most promising results were obtained using synthetic formulation of entomopathogenic fungi, such as B. basiana, which was demonstrated to cause a high level of mortality through release the insects captured in the pheromone traps after infecting them with the fungus [282]. Forests 2019, 10, 649 18 of 34

In particular, for I. sexdentatus, the bacteria Pseudomonas fluorescens Migula was demonstrated by Sevim et al. [283] to express insecticidal toxins affecting the beetles. In Spain, Beauveria pseudobassiana (Bals.) Vuill. was isolated from naturally infected M. galloprovincialis and the numbers of egg-laying wounds, eggs laid, live larvae after five days, and larvae entering the xylem after six months were significantly reduced in inoculated females, pointing to horizontally-induced reduction of progeny. These results validate the potential of the isolated B. pseudobassiana strain as an important natural population regulator [284]. In controlling H. abietis, several biological methods have been tested, such as the use of natural enemies (Braconidae, Hymenoptera) and nematodes (Steinernema carpocapsae (Weiser, 1955); Nematoda: Steirnermatidae) that have worked well in the United Kingdom [285]. Other studies mention the effectiveness of the use of entomopathogenic fungi, such as Metarhizium spp. [286] or Beauveria spp. [287]. Integrated pest management of scarabeids (Melolontha melolontha (Linnaeus, 1758), Polyphylla fullo (Linnaeus, 1758), and Amphimallon solstitiale (Linnaeus, 1758); Coleoptera: Scarabaeidae) in nurseries through biological control (parasitoids, predators, and pathogens), pheromone and food lures are desired instead of using insecticides [288]. Leptoglossus occidentalis is another species for which there are biological pest control programs, such as the use of the parasitoid Gryon pennsylvanicum (Ashmead, 1893) (Hymenoptera: Scelionidae) [289]. Yet, laboratory tests have not yielded positive results on the eggs of L. occidentalis [290]. On the contrary, Barta [291] managed to inoculate artificially in the laboratory the fungi M. anisopliae and Isaria fumosoresea (Wize) Brown y Smith, obtaining good results in adults. Successful results have also been obtained with predators of insect species of other insects such as Ooencyrtus pityocampae (Mercet, 1921) (Hymenoptera: Chalcidoidea), which generally parasitizes T. pityocampa [292].

4.2. Compliance of Management Options with Legislation and Forest Management Approach Application of any methods to control or manage insect vectors in forests, plantations or nurseries should ensure compliance with the relevant EU and national regulation for plant protection. This is important, especially when considering the use of chemicals or living organisms to control the potential vector insects. For instance, the European Commission must approve any active substance that is used in a plant protection product in the EU. In practice, any attempts to control or regulate insect populations through interventions will also have to be planned and executed within the frameworks of the prevailing FMAs. Duncker et al. [8], as well as Jactel et al. [293,294], determine FMAs that are dominating in the different regions of Europe and vary in terms of management goals and intensity. They differentiate five main approaches: –FMAI: Nature reserves. In these areas, all interventions are basically prohibited, but control methods could be permitted in specific cases to avoid destruction of the valuable habitat that often is of limited size; –FMAII: Close-to-nature forests. In these forests, interventions should mimic natural processes and chemical pest control can only be applied if major threats spread from the surrounding stands; –FMAIII: Combined objectives forests. Chemical pest control can be used in major outbreaks that are introduced from the surrounding stands or place them at risk, but minor outbreaks should not be treated with pesticides. Natural pest control methods are preferred, and the goal is to increase resilience, e.g., by greater use of mixed species stands; –FMAIV: Even-aged forests, where the interventions support biomass (timber) production goals. Chemical treatments are allowed, although they should be kept to a minimum, silvicultural measures such as whole tree extraction are allowed; –FMAV: Short rotation forests include stands where intensive management aims for maximum biomass production, e.g., through fertilization, and chemicals are used in pest and weed control. Hengeveld et al. [9] developed the classification further, presenting how the FMAs of Duncker et al. [8] could apply for P. pinaster, P. sylvestris, other pine species (Pinus spp.), and Pseudotsuga spp. across different biogeographic regions. In general, their analysis suggests that FMAIII and Forests 2019, 10, 649 19 of 34

FMAIV were most applicable approaches for pines and Pseudotsuga spp. across the different regions, i.e., possibilities to apply different interventions, including chemical treatments, to control insect pests of pines are generally high. In particular, a broad spectrum of possible interventions seems to be applicable for P. pinaster in Atlantic and Mediterranean regions, and for Pseudotsuga spp. in Atlantic, Mediterranean, and Continental regions where these species are considered highly amenable for the more intensive forest management approaches (FMAIII–FMAV). On the other hand, their analysis also indicates that FMAI and FMAII (with the highest restrictions in interventions) were applicable mainly for P. sylvestris, and especially in Atlantic and Continental regions (corresponding approximately to the Maritime and Central zones in the classification of Bouma [10]). This suggests that the practical possibilities to restrict the spread of PPC to P. sylvestris populations through vector insect control may be limited in these areas. Thus, new research on natural processes (e.g., insect behavior and inter-species interactions) is urgently needed to develop future-proofed, environmentally sound solutions to suppress the activity of vector insects without chemicals.

5. Conclusions Overall, our analysis highlights the potential of a diversified community of native and exotic forest insects found in Europe, which can vector and/or favor F. circinatum, emphasizing the need to include the insects’ distribution patterns and local population dynamics in greater detail in future simulations of PPC spread. Future research efforts should focus on testing the actual capacity of the most probable vector insects to actually carry PPC spores, and to transmit the disease in laboratory and field conditions. More knowledge is also needed to improve our understanding of the environmental control of the dynamic interaction between the insects, the pathogen, and host trees, so that the management methods can be effectively adapted to the changing climate. Currently, the combined threats due to climate change and new pests are often missing in the decision support systems in forestry. These systems should therefore be updated with comprehensive pest risk modules that also consider the interactions with changing climate (e.g., the changed patterns in geographic distribution and in voltinism). In future forestry, promising avenues may use forest management models based on species mixtures [295] that utilize landscape level patterns in biodiversity. On the other hand, for instance, the risks associated with new thinning regimes [296] need to be carefully evaluated to understand their consequences for insect pests and vectors. A thorough consideration of prevailing FMAs and EU and national level regulations is necessary for design of realistic and integrated intervention strategies against vector insects in different regions. Pathway-oriented strategies, rather than those based on quarantine lists should be considered when designing efficient and rapid intervention strategies against insects. Careful monitoring of the populations of potential vectors is also recommended regionally, in order to develop more rigorous risk assessments that include the dynamics of the local insect fauna. Considerable resources would, however, need to be allocated to this activity. The integrated management of PPC should include management of insect vectors in both forests and nurseries. It should focus on minimizing the need of chemical control, while intensifying the measures based on natural processes and biological control, in order to support bio-rational strategies that ensure effective suppression of further establishment and dissemination of F. circinatum in Europe.

Author Contributions: Writing: M.F.-F., P.N., D.L.M., A.V.S., M.C., D.C., M.P., T.G., A.S., I.P.-A., T.D., M.G., A.A., C.M.-R., M.T.-T., D.N.A., G.G., D.D.D., S.N., T.T., M.E.-R., J.J.D., and J.W.; review: M.F.-F., P.N., and J.W.; editing: M.F.-F. Funding: This study was made possible through the project “Etiology, Epidemiology and Control of Fusarium circinatum” sponsored by the Ministry of Rural, Marine, and Natural Environment, and with the support of the Government of Cantabria. This article is based upon work from COST Action FP1406 PINESTRENGTH (Pine pitch canker strategies for management of Gibberella circinata in greenhouses and forests) supported by COST (European Cooperation in Science and Technology) and project AGL2015-69370-R funded by MINECO and FEDER. P.N. was funded by the Fundação para a Ciência e Tecnologia—FCT (contract IF/00471/2013/CP1203/CT0001), Portugal. D.L.M. was partially funded by The Russian Foundation for Basic Research (Grant No. 17-04-01486). A.V.S. was partially funded by the Center for collective use of scientiﬁc equipment "Renewable resources, energy sources, new materials and biotechnology (SPbFTU)" (Project 2019-0420). Forests 2019, 10, 649 20 of 34

Acknowledgments: We want to thank Drs Martin Muller, Jaime Aguayo, Katarina Adamcikova, Kaljo Voolma, Stanley Freeman, Panos Petrakis, and Svetlana Markovskaja for their contribution in the collection of references related to the PPC disease. Conﬂicts of Interest: The authors declare no conﬂict of interest.

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