Current and Future Insect Threats to Oaks of the Midwest, Great Lakes, and Northeastern United States and Canada

Abstract

Increasing temperatures, prolonged drought, the increased severity and intensity of storms, and other effects of climate change are being felt globally, and long-lived forest tree species may struggle in their current ranges. Oaks (Quercus spp.) have evolved a range of adaptations to dry and hot conditions and are believed to be a “climate change winner” by increasing their suitable habitat. However, a mixture of life history traits and increasing susceptibility to herbivores and xylovores as well as secondary pathogen infections still put oaks at risk of decline. Oak species found in the Midwestern, Great Lakes, and Northeastern United States and Canada are important keystone species with high ecological and economical importance. They are also vulnerable to existing, new, and emerging threats that have the potential to cause mortality across entire stands quickly. Current examples of insect threats include the Lymantria dispar (spongy moth), Agrilus bilineatus (twolined chestnut borer), and Nitidulidae (sap beetles) as disease vectors. Examples of emerging insects of concern include Cynipidae (oak gall wasps) and Enaphalodes rufulus (red oak borer). This study describes these insects, explains their mechanisms of action and the effects on oaks, and explores mitigation strategies for each.

1. Introduction

Anthropogenic climate change not only shifts mean temperatures higher, as it also increases the occurrence and intensity of extreme weather events, including droughts, heatwaves, and heavy rain events. Long-lived forest tree species of economic and environmental importance may be maladapted to these conditions and become increasingly susceptible to predation by insects and herbivores [1]. Opportunistic fungal and bacterial pathogenic infections have the potential to wipe out entire stands quickly, affecting the larger ecosystem [2]. As global temperatures are increasing [3], natural tree species migration is lagging and cannot keep pace to extend ranges into preferred climates to avoid temperature extremes. An ecologically and economically important hardwood genus, the long-lived oaks (Quercus, Fagaceae) move slowly at an unassisted pace of approximately 100 m per year [4,5,6,7,8] due to their heavy seeds [9].

Oaks are an integral species in many ecosystems in the Northeastern, Great Lakes, and Midwestern United States and Canada and were the most common foundation genus before widespread farming and settlement [10]. A host of mammals and birds feed on oak acorns, bark, or new growth and twigs; notable species include white-tailed deer (Odocoileus virginianus), white-footed mouse (Peromyscus leucopus), black bear (Ursus americanus), blue jay (Cyanocitta cristata), and wild turkey (Meleagris gallopavo) [11,12,13]. Ecological studies have found that abundance of black bears is directly correlated to oak populations in the United States, and when acorn yields are low due to disease or low mast years, bears venture further from their home range, leading to potential conflicts with humans in attempts to find other high-fat food sources prior to hibernation [11,14,15].

Quercus is a species-rich genus with a mostly northern hemisphere distribution [16]. The current estimate of species numbers is around 435 [16,17,18], divided into two subgenera and eight sections. Most North American species are classified as white oaks (sect. Quercus), red oaks (sect. Lobatae), and live oaks (sect. Virentes), with a few species representing two other sections: golden cups (Protobalanus) and Pontificate (one species which is found in California and Oregon) [16]. A dated phylogeny of oaks shows high diversification rates since the Pliocene in sections Quercus and Lobatae [19]. This recent diversification has been characterized by sympatric parallel adaptive radiation of Lobatae and Quercus taxa in North America [20]. Oaks have evolved a range of adaptations to dry and hot conditions [21] and, due to that, are modelled to have an increased range of suitable habitat with climate change [22]. However, increasing severe weather events (strong storms and heavy rainfall) and other factors including expanded ranges of herbivores and pathogens may still put oaks at risk [23].

Oaks have a ring-porous xylem system, the result of an evolutionary drought tolerance mechanism. This system is sensitive to freeze–thaw cycles in the spring and autumn, which provides diffuse-porous trees advantages in colder climates across the Northern United States and Canada [24]. Ring-porous trees are often more vulnerable to girdling or wood-boring insects and pathogens that move more easily through outer xylem tissues [25,26]. The ring porosity that somewhat limits the northern range of oaks allows the genus to be well equipped to handle drought stress [21,23]. However, prolonged exposure to drought and conditions at the edge of tolerance levels leave trees vulnerable to opportunistic infection. In addition, increased predation, as animals and insects struggle with their own survival, exposes vulnerable plant tissue to bacterial or fungal entry and further compounds an already dire situation. Though physical and chemical plant defenses, such as tough cell walls, cuticular waxes, and phenolic and terpenoid compounds, respectively, have traditionally been adequate to ensure survival, the migration of animals and insects north as climate temperatures increase has been outpacing that of long-lived trees [27]. As oaks are a long-lived species, the death of large trees can be a slow process, taking a decade or more [28], which can lead to entire stand declines years after environmental or predator stressors were present.

The unique forest ecosystems of the Great Lakes and Northeastern United States and Canada host a wealth of biodiversity for terrestrial and aquatic organisms and are host to several oak species and other mixed hardwood species. Several of the Northeastern states have the highest percentage of forested land in the United States (Maine at 89.46%, New Hampshire at 84.32%, Vermont at 77.81%, and New York at 62.88%), and Great Lakes states also boast heavy forest cover (56% in Michigan, 49% in Wisconsin, and 32% of Minnesota) [25,29]. The Great Lakes region is characterized by humid weather, locally heavy snowfall, and occasional heavy rains and strong storms [30]. With a changing climate, the Great Lakes region is experiencing warmer winters, with increases of more than 0.83 °C observed from 1986 to 2016 [31], as well as an average 42% increase in the time and intensity of rainfall events from 1958 to 2016 [32], and similar trends have been observed in the northeast. Such dramatic changes leave oak trees stressed from temperatures and rainfall amounts outside their preferred ranges, which can then open the door for opportunistic predation. Increasing winter temperatures increases the winter survival of insects, which can have devastating effects, as seen recently with the aggressive outbreaks of mountain pine beetles (Dendroctonus ponderosae Hopkins: Coleoptera: Scolytinae) in the Western United States [33,34]. The range of pathogens and herbivores also increases with more accommodating warmer winters, and increased cold season temperatures simultaneously provide a longer period of fecundity for potentially harmful insects. Here, we focus on several examples of current insect threats to oak stands of the Northeastern, Midwestern, and Great Lakes regions of the United States and Canada: the spongy moth (Lymantria dispar), the twolined chestnut borer (Agrilus bilineatus), the red oak borer (Enaphalodes rufulus), and the sap beetles (Nitidulidae) (which are vectors of oak wilt) (Figure 1). We discuss how these insects harm oak trees and explore what mitigation techniques have been attempted and their varying levels of success, as well as several other insects and oak diseases of current concern. We also discuss several emerging insects of concern: the oak gall wasps (Zapatella davisae, Callirhytis cornigera, and Callirhytis quercuspunctata), and oak borers (Agrilus biguttatus and Agrilus auroguttatus). Additional potential and current threats are also outlined in this paper (

Table 1. Examples of current and potential insect threats to oaks in the Midwestern and Northeastern United States.

Threat	Quercus Species Most Vulnerable	Part of Tree Attacked	Extent of Current Threat	Areas of Concern
Coleoptera
Agrilus auroguttatus (Gold-spotted oak borer) [36,37,38,39]	Quercus agrifolia Q. emoryi Q. hypoleucoides Q. kelloggii	Bark Phloem	Arizona California	Trees in areas susceptible to opportunistic infection Stressed trees
Agrilus biguttatus (Oak splendor beetle) [40,41,42,43]	Q. cerris Q. ilex Q. petraea Q. pubescens Q. robur Q. suber *	Foliage Bark Xylem Sapwood	Not currently found in the United States or Canada	Trees in areas susceptible to opportunistic infection Stressed trees
Agrilus bilineatus (Twolined chestnut borer) [44,45,46]	Q. rubra Q. coccinea Q. alba Q. montana	Bark Phloem Xylem Cambium Foliage	Eastern North America from the Maritime provinces in Canada west to Manitoba and south to Texas and Florida	Areas with oak decline
Agrilus sulcicollis (European oak borer) [47,48,49]	Q. rubra Q. alba Q. affected by L. dispar outbreaks *	Phloem	Great Lakes region	Trees stressed from drought and/or L. dispar infestation
Anoplophora glabripennis (Asian long-horned beetles) [50,51,52,53]	Q. rubra *	Foliage Branches Bark (oviposition)	New England, Ontario, Ohio, South Carolina	Stressed trees
Arrenodes minutus (Oak timberworm) [54,55]	Q. velutina Q. coccinea *	Bark Sapwood Xylem	Within the range of Quercus in North America	Stressed trees Trees in areas susceptible to secondary opportunistic infection Uninfected oaks within and outside the current oak wilt range
Cyrtepistomus castaneus (Asiatic oak weevil) [56]	Q. velutina Q. rubra *	Foliage Root hairs (larvae)	Eastern United States and Canada	Trees in areas susceptible to opportunistic infection
Curculio glandium (Acorn weevils) [57,58]	Q. rubra *	Fruit (acorns)	Widespread in the United States except Rocky Mountain region	Trees in areas susceptible to opportunistic infection
Enaphalodes rufulus (Red oak borer) [44,46,59]	Q. rubra Q. coccinea Q. velutina Q. falcata Q. marilandica Q. phellos Q. texana Q. alba *	Phloem	Ozark mountains, Eastern United States	Areas with oak decline
Nitidulidae (Sap or picnic beetles) [60,61,62,63,64]	sect. Lobatae *	Fresh wounds (0–3 days old) Xylem Foliage Root system	From Texas through the Midwest and upper Southern states, up into the Northeast through New York and into Ontario	Uninfected oaks within and outside the current oak wilt range
Hemiptera
Lycorma delicatula (Spotted lanternfly) [65,66,67,68]	Q. acutissima Q. rubra *	Foliage Phloem Sapwood	Connecticut, Delaware, Indiana, Maryland, Massachusetts, Michigan New Jersey New York, North Carolina, Ohio, Ontario, Pennsylvania, Rhode Island, Virginia, West Virginia	Trees in areas susceptible to opportunistic infection Stressed trees Monocultures
Hymenoptera
Callirhytis cornigera (Horned oak gall wasp) [69]	Q. palustris	Twigs Bark Vascular system Foliage	Eastern and Midwestern United States and Ontario	Trees in areas susceptible to opportunistic infection Stressed trees
Callirhytis quercuspunctata (Gouty oak gall wasp) [70]	Q. palustris *	Twigs Bark Vascular system	Eastern, Midwestern, and Plain states in the United States	Trees in areas susceptible to opportunistic infection Stressed trees
Zapatella davisae (Stem gall wasp) [71,72,73]	Q. velutina	Twigs Bark Vascular system	Coastal New England: Connecticut, Massachusetts, Rhode Island	Q. velutina in neighboring states, stressed trees, possibly other oak species Stressed trees
Lepidoptera
Alsophila pometaria (Fall cankerworm) Paleacrita vernata (Spring cankerworm) [74,75,76,77,78,79]	Q. rubra Q. alba *	Foliage	Widespread in the United States and Canada	Trees stressed by drought
Anisota senatoria (Orangestriped oakworm) [76,80,81,82]	Q. rubra *	Foliage Twigs can suffer dieback	Eastern United States and Canada	Trees in areas susceptible to opportunistic infection Stressed trees
Archips cerasivoranus (Ugly nest caterpillar) [76,83,84]	Q. macrocarpa *	Foliage Twigs involved in tenting	Widespread throughout North America: as far north as the Yukon Territories and as far south as North Carolina	Seedlings Stressed trees
Archips semiferanus (Oak leaf roller) [76,85,86,87]	Q. alba Q. coccinea Q. montana Q. rubra *	Foliage Buds	Eastern United States and Southeastern Canada	Trees in areas with wood borers and other opportunistic predators
Bucculatrix ainsliella (Oak leaf skeletonizer) [76,88,89,90]	Q. rubra Q. palustris Q. phellos *	Foliage	Widespread through the United States and southern Canada	Trees in areas susceptible to opportunistic infection Seedlings Stressed trees
Erannis tiliaria (Linden looper) [76,91,92,93]	Quercus *	Foliage	United States and Canada from the east coast west to Alberta and Utah	Areas with cankerworm infestations Stressed trees
Heterocampa manteo (Variable oakleaf caterpillar) [76,94]	Q. alba *	Foliage	Eastern United States and Canada	Trees in areas susceptible to opportunistic infection Stressed trees
Lymantria dispar (Spongy moth) [95,96,97,98,99,100]	Q. rubra Q. alba *	Foliage	Northeastern North America	Trees in areas susceptible to opportunistic infection Stressed trees Seedlings
Malacosoma disstria (Forest tent caterpillar) [74,76]	Q. virginiana Q. rubra Q. alba *	Foliage Buds	Throughout the United States, most heavily concentrated in the Eastern United States and Canada	Trees in areas susceptible to opportunistic infection

* Denotes oak generalist.

), as well as how future or emerging threats can be predicted, detected, and mitigated before they become devastating. Opportunistic predators are also a concern as trees stressed from drought, temperatures outside their native range, or extreme weather are vulnerable to secondary infection or infestation [35].

2. Lymantria dispar (Spongy Moth)

The native origin of North American spongy moth (Lymantria dispar Linnaeus, Lepidoptera: Erebidae) has been disputed, with most sources pointing to Asia or Europe [100]. Lymantria dispar has been present in the United States since 1869, when captive moths escaped from silk production experiments in Massachusetts [101]. Since then, they have been present in the Northeastern United States and have migrated west to Minnesota, as far north as the Upper Peninsula of Michigan and central Ontario [95,96,97,100]. Though present in warm Southern US climates, L. dispar eggs are also tolerant of prolonged freezing temperatures and can survive temperatures down to −29 °C [102], with studies revealing that higher temperatures or radiant heat from the winter sun on southern/western exposures significantly affects survival [103]. Lymantria dispar has been long noted to be a significant threat to oak species and is still considered to be a significant threat to oak stand survival [104,105].

2.1. Mechanisms

A broad foliar generalist, L. dispar larvae willingly consume the leaves of many plant and tree species [95] and have been a known threat to oak health and growth since the early 1900s [106]. Studies of mixed hardwood stands in New England have found the greatest number of L. dispar caterpillars on Q. rubra and Q. alba [107], with Q. rubra noted to be a preferential food source [108,109]. In addition to the generalist feeding habits, spongy moths have high fecundity; even though adult female moths only live approximately one week, thousands of eggs can be laid and deposited in late summer [100,110]. The larvae hatch in late spring and feed on leaves until midsummer when they pupate. As oaks are a preferred host tree, they subsequently suffer elevated foliar damage as the larvae begin feeding immediately after hatching. Lymantria dispar caterpillars are voracious feeders and can completely denude tree foliage during heavy outbreak years [100]. Outbreaks are cyclical, occurring every five to eight years. Increased defoliation can lead to higher-than-normal concentrations of tannins in oak leaves, which can, in turn, be toxic to L. dispar [111]. While defoliated trees can recover, the resulting stress can affect leaf quality [112] and growth and can lead to tree mortality in subsequent years [108,113,114].

2.2. Threats and Solutions

To reduce the L. dispar population, multiple natural and artificial mitigation techniques have been attempted and employed, including utilizing predator species, viral, fungal, or bacterial methods, insecticides, and manual removal and disposal. In North America, multiple species consume the caterpillars, including bird species, other insects such as forest caterpillar hunter (Calasoma sycophanta) and white-footed mouse (Peromyscus leucopus) [100]. However, predation is not adequate to keep pace with the sheer number of caterpillars during outbreak years, and North American predators may not be as effective in curbing populations as those in the native spongy moth range [98]. The baculovirus Nucleopolyhedrosis virus (NPV) is always present and circulating in populations of L. dispar but is usually not fatal to caterpillars. When caterpillars are stressed during highly competitive outbreak years, or when foliage is in low supply, latent NPV begins to affect larvae and reduces populations by widespread internal cell lysis, one variable in cyclical outbreaks which assists in reducing overall outbreak intensity [115,116]. Studies have found combinations of NPV and Bacillus thuringiensis var. kurstaki (Btk) applications can be effective for killing instars in different developmental stages [117]. Additionally, a fungus native to Japan, Entomophaga maimaiga, has been employed since the early 1900s in North America to quell outbreaks and reduce L. dispar populations. Entomophaga maimaiga consumes caterpillars from the inside, then migrates outward as tissue dies. Spores disperse externally via conidiophores and can infect subsequent L. dispar generations [118]. However, E. maimaiga has limited applicability as a biocontrol as its success is very weather- and environment-dependent: spores require high humidity to reproduce [119,120]. One of the most widely employed and successful techniques in limiting L. dispar populations is the application of Bacillus thuringiensis var. kurstaki (Btk), a bacteria endemic to soil. The active insecticide contains the Cry protein produced by the bacterium and encapsulated in a spore by the bacterium. When consumed, Cry proteins bind to receptors in insect midgut cells and cause cellular rupture. Commonly applied as a foliar spray, Btk is considered very safe for mammals (including humans), birds, and most insects [100] and is effective in controlling populations. Caution must be used as the bacterium can be indiscriminately fatal to Lepidoptera species, and potential benefits should be weighed against ecosystem destruction. In heavy outbreaks, aerial spraying of Btk can be employed [121,122] but, in addition to potential harm of Lepidoptera populations [123], the overall economic cost for this method of dispersal should be considered. Recent studies have found Btk to be less harmful to total Lepidoptera populations than the insecticide tebufenozide [124].

Manual injections of insecticides into the base of a tree under the bark can reduce populations on specific trees, with azadirachtin being a common choice [119]. This method can be time-consuming and manually difficult if multiple trees are targeted. Azadirachtin is produced from oil of Neem tree (Azadiracta indica) seeds but is a broad-range insecticide (non-species-specific) and can kill beneficial indigenous insects [125]. Pheromone traps have been employed for decades in the “Slow the Spread” campaign to reduce L. dispar populations from moving south and west [126], but this method only targets male moths (though some evidence exists female spongy moths in Asia and some in Europe are flight capable and do fly [127,128], it is widely accepted that most North American females do not fly [129,130] and pheromone traps bated with female hormones will not attract them in any case). Such traps are also labor-intensive as traps need to be manually emptied and re-baited frequently. Though pheromone traps can stop the movement of spongy moths beyond the current range, it is not an effective method for reducing larval populations responsible for defoliation in an infested area. The most labor-intensive and time-consuming but safest mitigation method for curbing populations is manually scraping L. dispar egg masses and disposing of them in soapy water [131]. This effectively kills hundreds to thousands of potential L. dispar caterpillars and limits non-target impacts. Though manual scraping is unrealistic for large wooded or forested areas, it can be very effective in reducing populations in small areas. Sticky barrier bands can be applied to tree trunks in the spring [132], but care must be taken to protect birds and other small animals from injury. Burlap bands can also be applied around tree trunks in the summer to trap spongy moth caterpillars, but this also requires frequent checks and manual disposal of the caterpillars caught in soapy water [133]. “Slow the Spread” and other citizen scientist campaigns have been successful in raising awareness and curbing L. dispar infestations in urban areas, but monitoring and mitigation are still required, especially in rural and wilderness areas.

3. Agrilus bilineatus (Twolined Chestnut Borer)

Both bark and wood-boring insects, native and non-native, have been implicated in a number of major oak declines, either as primary or secondary factors [49,134,135,136]. The taxonomic families Cerambycidae and Buprestidae are generally considered the most important wood borers in oaks, along with bark beetles in Curculionidae [135,137,138]. Twolined chestnut borer (Agrilus bilineatus, Coleoptera: Buprestidae) has been commonly documented as an extensive mortality agent among oaks [25,44]. Though so named for its previous status as a pest of chestnut (Castanea dentata), A. bilineatus has a wide range in eastern North America from the Maritime provinces of Canada, west to Manitoba, south to Texas and Florida [45], and is regularly reported reaching outbreak levels in the Great Lakes states [25]. Adult A. bilineatus primarily select damaged, suppressed, or stressed oak trees to lay eggs, from which larvae bore into the bark and construct damaging galleries in the cambium layers, effectively girdling trees. Tree mortality often occurs within two to three years of attack but can occur in the first year [45]. The expansion of L. dispar throughout its range, as well as drought have been frequently linked as inciting factors to subsequent twolined chestnut borer infestation [25,48].

3.1. Mechanisms

Wood borers cause the most damage to trees by feeding on the phloem, cambium, and xylem as larvae, while adults will also consume some foliage. Adults are often attracted to stress volatile chemicals, sometimes within hours of a stress event occurring [139]. The overall time to tree mortality varies between species and events. Periodic stress impacts can also predict outbreaks associated with many wood borers. For example, tree vigor and winter starch reserves in roots are significantly correlated with twolined chestnut borer attacks [140]. Ultimately, different wood borers likely cue to suitable hosts via a range of intra- and interspecific differences in the biochemistry of leaves, bark, and wood, which is impacted by site, stress, and age of host trees. Attraction to a tree is likely within a narrow window of the stress period, not too early (as resistance compounds such as tannins and phenolics may still be present in higher levels) but not too far declined [42,46,139]. The timing in the season or host deterioration may further influence host species selection in these families. For instance, A. bilineatus prefers to develop in at least some live phloem; however, European oak borer (Agrilus sulicicollis, Coleoptera: Buprestidae) (introduced to North America in the Great Lakes region in the 1990s) prefers recently dead phloem for larval development, hence, it is likely not as aggressive of a mortality agent [25,141]. Stressed trees may be susceptible either from drought conditions or other environmental factors, or previous insect attacks, such as L. dispar outbreaks, or multiple combined factors [48,49]. The significant outbreak of the Cerambycid red oak borer (Enaphalodes rufulus, Coleoptera: Cerambycidae) tied to drought in the Ozark Mountains (Missouri, Arkansas, Oklahoma, Kansas) in the early 2000s is unique, though it had never been implicated in major tree mortality previously and is normally found in low population densities of less than one beetle emerging per tree, up to 600 beetle attacks per tree in Q. rubra were reported in 2003, causing significant decline and mortality [59]. Poor crown vigor and reduced defense mechanisms, including reduced ability to produce callus overgrowth, have been most correlated with borer attacks and outbreaks [142,143]. Callus formation has also been reported as an important defense against wood borers [44,46].

3.2. Threats and Solutions

Strong evidence supports the claim that varying stresses to trees are inciting factors leading to an increase in A. bilineatus (and other wood borer) abundance. Wood borers that are currently not strongly correlated with mortality events or considered only of minor concern could be expanding ranges throughout the region or reach outbreak level occurrences more frequently throughout the range of hosts, especially as drought is predicted to increase in the future [116,144,145,146,147]. A looming threat is the little--understood biology and ecologies of many of these insect species, which leads to surprises when optimal conditions create seemingly novel or unanticipated outbreaks, as was the case with red oak borer, leaving managers not fully prepared when such events occur. Overall, there is a continuous need for forest health specialists and taxonomic specialists to help identify novel pests and make reliable information about them accessible [148]. Preventative forest management is the most effective means of mitigation, as any silvicultural action to reduce predisposing stress factors will likely reduce or prevent an infestation. Early removal of recently dead or declining trees (sanitation) is sometimes recommended to limit pest populations from building, however, it will not prevent trees predisposed to declining vigor from eventually being attacked [42,46]. Natural biological control via native parasitoids (such as chalcid wasps, Hymenoptera: Chalcidoidea) and predators (such as woodpeckers i.e., Picidae) can act as a form of limited control [45]. Chemical control can be used on ornamental or high-value individual trees, but once wood borers are in a tree, it is not possible to save infested portions from most wood boring activity. Control of defoliating caterpillars may be a more effective management option for preventing A. bilineatus outbreaks [45]. For many wood borers, limited Integrated Pest Management (IPM) tools are developed with no effective detection tools or pheromones developed or known and limited knowledge of specific resistance or attractant volatiles. Continuous visual awareness, training for professionals, and monitoring in the field are needed.

4. Sap Beetles (Nitidulidae: Coleoptera)

Nitidulid beetles (Coleoptera: Nitidulidae), commonly known as sap or picnic beetles, are oval-shaped insects with clubbed antennae that vary in size from 0.9 to 15 mm in length, depending on species [60]. Nitidulidae feed on sap, flowers, fungi, decaying plant tissue, insects, and carrion; however, diets vary by species [60,61]. Over 4500 species of Nitidulidae can be found worldwide, with 173 species described in North America [61], and roughly 60–70 species are found within the Great Lakes and Midwestern regions [149]. Although most currently present nitidulids are native to the Great Lakes region, multiple species are confirmed vectors of the non-native, fatal fungal pathogen, oak wilt (Bretzeilla fagacearum) [64]. New records of first collections and new introductions of non-native species are seemingly continuously emerging for these often overlooked yet ubiquitous insects tied to a significant oak mortality agent [61,150,151].

4.1. Mechanisms

The majority of oak wilt spread takes place underground through root grafts of adjacent oak trees, however, overland spread from insect vectors can cause new infection centers (Figure 2). Nitidulids, especially the confirmed vectors Carpophilus sayi Parsons and Colepterus truncates Randall, have been shown to carry viable B. fagacearum spores across the landscape [61,152]; however, additional Nitidulidae, such as Glischrochilus fasciatus Olivier, G. sanguinolentus Olivier, G. quadrisignatus Say, and Epuraea corticina Erichson, are often associated with oak wilt fungal mats [153]. The fermenting scent of oak wilt fungal mats under the bark attracts beetles, where feeding and mating take place on the mat and fungal spores are accumulated [62,63]. Oak wilt disease is vectored to healthy trees when contaminated beetles leave the fungal mats and visit fresh wounds on different oak trees to feed on tree sap [152].

4.2. Threats and Solutions

Oak wilt is a significant threat to oak species in the Great Lakes, Northeastern, Midwestern, and Canadian Maritimes regions. The disease was first discovered in Wisconsin in 1942 [64,154], and the current range extends through Minnesota, Wisconsin, Michigan, down through Ohio and Pennsylvania, and across the United States south to Texas. Pockets of oak wilt have also been detected in the Carolinas, New York, and recently for the first time in Ontario, Canada [155]. All oaks are susceptible to oak wilt; however, the red oak group (sect. Lobatae) is particularly susceptible with its ring-porous cells being absent [156,157,158,159]. Fungal mats are less commonly found on species in sect. Quercus and are not found in sect. Virentes [152]. Preventative measures are in place to reduce the spread of oak wilt, including protocols and regulations on harvesting and pruning during the oak growing season to reduce the spread from overland vectors entering wounds [160,161]. When oak wilt is detected, management options are available to eradicate infected trees to reduce further spread. Additionally, knowing the signs and symptoms of oak wilt can be useful so rapid treatment can be conducted to reduce the spread of oak wilt underground or overland. Control of the native nitidulid beetles is not feasible due to their ubiquitous nature and the sheer number of species that are likely visiting oak trees. However, surveying trapped nitidulidae can be a critical method for the early detection of the oak wilt fungus in new areas, increasing rapid response actions [63,162]. Refining effective methods for trapping Nitidulidae and testing for the oak wilt fungus is increasingly important as early detection tools are crucial to limit environmental and economic damage from this disease [155,163].

Figure 2. The cycle of oak wilt infection and Nitidulidae. (A): Nitidulidae carrying the oak wilt fungal pathogen Bretzeilla fagacearum spreads the fungus to healthy oak trees, (B): oaks displaying characteristic signs of oak wilt: widespread crown dieback and leaf tissue necrosis, (C): further example of oak crown dieback and fungal hyphae mats under the outer bark layer, (C1): oak trees with oak wilt can spread the pathogen to adjacent stand trees via underground root grafts causing healthy trees (C2) to become infected (C3) and continue spreading the infection to other adjacent trees (C4), (D): Nitidulidae beetles attracted by the fermenting scent of oak wilt hyphae mats congregate to feed and mate, (E): Nitidulidae carrying the oak wilt fungal pathogen Bretzeilla fagacearum spread it to additional trees and the infection cycle continues.

Figure 2. The cycle of oak wilt infection and Nitidulidae. (A): Nitidulidae carrying the oak wilt fungal pathogen Bretzeilla fagacearum spreads the fungus to healthy oak trees, (B): oaks displaying characteristic signs of oak wilt: widespread crown dieback and leaf tissue necrosis, (C): further example of oak crown dieback and fungal hyphae mats under the outer bark layer, (C1): oak trees with oak wilt can spread the pathogen to adjacent stand trees via underground root grafts causing healthy trees (C2) to become infected (C3) and continue spreading the infection to other adjacent trees (C4), (D): Nitidulidae beetles attracted by the fermenting scent of oak wilt hyphae mats congregate to feed and mate, (E): Nitidulidae carrying the oak wilt fungal pathogen Bretzeilla fagacearum spread it to additional trees and the infection cycle continues.

5. Additional Current Threats

Though many insects do not specifically preferentially target oaks, they can still cause harm or introduce pathogens that can further weaken stressed trees. Primary threats to trees are herbivores, while secondary threats include viral, fungal, or bacterial infections. Native defoliators like the forest tent caterpillar (Malacosoma disstria, Lepidoptera: Lasiocampidae) and fall cankerworm (Alsophila pometaria, Lepidoptera: Geometridae) are generalist feeders but prefer oaks when available [74,75,76], causing significant defoliation in oak-dominated stands, which then in turn make trees more susceptible to additional pests and pathogens. Currently found in the Great Lakes/Midwest region in southern Ohio (and previously introduced and eradicated in other locations in the region), Asian long-horned beetles (Anoplophora glabripennis, Coleoptera: Cerambycidae) preferentially consume leaves and branches, and oviposit eggs in the bark of many hardwood species in North America [164,165,166]. In heavy infestations, trees will be girdled or have their heartwood destroyed, which can lead to fatality. Oviposition pits also allow entry for pathogens or other herbivores, which cause additional damage [164]. Multiple introductions in new locations of this insect pest mean that continuous monitoring and awareness programs are warranted.

5.1. Enaphalodes rufulus (Red Oak Borer)

Red oak borer (Enaphalodes rufulus, Coleoptera: Cerambycidae), historically, was only considered a minor pest in oak trees and not recognized as a secondary agent in oak decline [38,129,157]. A sequence of forest management history, drought and regional climatic patterns led to the dramatic emergence of this native species as a more aggressive, novel agent that had not caused noticeable tree mortality in the past [142]. Enaphalodes rufulus is native to the Eastern United States and likely matches the range of its preferred host species: Q. rubra, Q velutina, and Q. coccinea (sect. Lobatae) [167]. Though the seemingly rare series of events that led to the red oak borer outbreak in the Ozarks is not anticipated again soon, E. rufulus is now considered a much more significant threat to oaks in the United States and Canada. This may be exacerbated by a changing climate that may impact tree defense mechanisms [144,145,146].

5.2. Leaf Miners

Leaf miners of multiple orders are known to utilize multiple species, including Quercus, as hosts and cause tunneling, skeletonization, and other extensive leaf tissue damage [168]. Though this is rarely fatal, infestations can cause widespread defoliation and tree stress, as well as allowing entry routes for pathogens. The variable oakleaf caterpillar (Heterocampa manteo, Lepidoptera: Notodontidae) and the orange-striped oakworm (Anisota senatoria, Lepidoptera: Saturniidae) cause widespread foliar damage in late summer. An oak generalist, H. manteo prefers Q. alba, and outbreaks have been known to occur since the 1950s in Maine and appear in cycles that are rarely severe enough to require mitigation [94]. Anisota senatoria is also an oak generalist but prefers Q. rubra and has similar cyclical infestation patterns [76]. Oak leaf rollers (Archips semiferanus, Lepidoptera: Tortricidae) are oak generalists, which skeletonize leaves while larvae consume buds and leaf tissue. Insecticide mitigation is best applied during the egg or larval stages before foliar damage becomes widespread but is likely only feasible on individually, severely impacted trees or orchard plantings [85]. As cold temperatures in the winter assist with controlling populations of leaf miners, warming winters and prolonged periods without freezing temperatures observed with climate change could cause more regular and extensive infestations.

5.3. Weevils

Acorn weevils (Curculio glandium, Coleoptera: Curculionidae) oviposit in acorns by boring holes, which are subsequently healed by callus tissue (which also protects the developing egg and subsequent larvae) [57]. Though this is not fatal to the tree itself, acorn weevil larvae consume most of the acorn fruit and can damage the embryo, which affects tree reproductive rates [58]. As very few acorns avoid mammal or avian predation and find suitable environments to develop into mature trees, a heavy acorn weevil year can greatly affect oak stand populations. The invasive Asiatic oak weevil (Cyrtepistomus castaneus, Coleoptera: Curculionidae) feeds preferentially on Q. velutina and Q. rubra [56] and has been causing oak damage in the Ozark Mountains since its introduction in the 1930s. Asiatic weevils are leaf edge feeders and can cause extensive leaf damage in years of heavy infestation. Another weevil, the oak timberworm (Arrenodes minutus, Coleoptera: Brentidae) prefers Q. velutina and Q. coccinea (though they will attack other species) and finds areas of exposed sap beneath oak bark and bores single holes (“pin holes”) to oviposit [54]. The larvae enlarge the pin holes to larger wounds as they grow and age, and previously used holes are sometimes used for several years. Holes that expose sapwood cause the most damage to trees [55].

5.4. Lycorma delicatula (Spotted Lanternfly)

Spotted lanternfly (Lycorma delicatula, Hemiptera: Fulgoridae) is not considered a predominant threat to oaks but is an indiscriminate feeder [65] and will attack oaks if preferential food sources are unavailable [66]. Oaks are also capable of hosting L. delicatula through its lifecycle [67]. This invasive planthopper consumes the phloem of immature bark and leaves behind wounds from which sap flows. The fecundity of the spotted lanternfly leads to infestations and excessive wounding, which attracts opportunistic insects and opens channels for secondary infections to enter [169]. It is projected to find ample hosts as it continues to invade the Midwest and Great Lakes regions from the Northeast where it is currently located [169,170,171]. Lycorma delicatula is especially concerning in areas with Prunus and Vitis industries as infestations can decimate fruit yields and cause heavy economic losses [68].

5.5. Sudden Oak Death

In addition to oak wilt, sudden oak death has caused fatality in oaks in California and parts of Oregon. It is caused by a type of pathogenic water mold (Phytophthora ramorum) and decimated populations of Q. agrifolia (sect. Lobatae) and Notholithocarpus densiflorus (Fagaceae) in California [172,173]. Sudden oak death is a cause for concern as spores can spread by air, water, or on animals and humans and spread to new host trees through open wounds [174]. We have included mention of these two significant pathogens in with insect threats as oak wilt is vectored by Nitidulidae, and the combination of wounds from herbivore infestation and infection from P. ramorum can have widespread and devastating consequences to oak stands. Multiple states have periodically led large monitoring surveys for P. ramorum and have detected infected host plants moved in nursery stock but have not yet found sudden oak death disease in trees, yet it remains a significant concern [175,176].

6. Emerging Threats

With changing temperatures and other climatic conditions, insects which affect oaks in areas of North America or the world may be introduced to new areas and become problematic. Just as L. delicatula is currently expanding its range relatively quickly and is a large threat to commercial crops and fruits, an invasive species that targets oaks could be the next threat whose range expands rapidly and causes ecological disturbance and economic damage. Insects of known concern include oak gall wasps and multiple wood- or bark-boring beetles, while additional opportunistic secondary pests and pathogens can also threaten oak stand survival.

6.1. Oak Gall Wasps

Oak gall wasps (Hymenoptera: Cynipidae) parasitize oak tissue to deposit their eggs, thus forming a gall. In most cases, oak galls do not harm the overall health of the tree and usually only result in additional nutrients directed to the gall [177], though the exit created by emerging female wasps in twig galls can leave openings for opportunistic infections. Trees with extreme numbers of galls may undergo crown dieback [178]. The horned oak gall wasp (Callirhytis cornigera, Hymenoptera: Cynipidae) primarily targets pin oaks (Q. palustris, sect. Lobatae) [69], while the gouty oak gall wasp (Callirhytis quercuspunctata, Hymenoptera: Cynipidae) is more indiscriminate in its oak predation [179]. A newly discovered species of North American oak gall wasp, the stem gall wasp (Zapatella davisae, Hymenoptera: Cynipidae), parasitizes Q. velutina exclusively and deposits eggs in twigs [70]. Several generations of this species can be found in twig galls throughout the autumn and winter, which can cause twig node damage and widespread tissue damage due to disruption of the vascular system of the tree. In instances of widespread infestation, full tree dieback can occur up to three years after initial parasitism [70]. Similar to other species of gall wasps, exit holes from Z. davisae can leave trees susceptible to secondary infections.

Currently, Z. davisae is found in coastal New England, including Massachusetts, Rhode Island, and Connecticut [71,72], with little evidence of it having spread to other areas. However, with transfer of wood or other incidental items containing Z. davisae, there is a possibility that the species could be moved beyond New England. Currently, there is debate whether significant Q. velutina dieback coincident to Z. davisae outbreaks may also be from an opportunistic fungal pathogen Botryosphaeria spp., which may take advantage of wasp exit holes to enter tree tissue [70]. No specific mechanism of insects or other parasitism to the newly discovered oak gall wasp has yet been observed that could be used as a biologic control [71]. However, there is also no clear reason for heavy outbreak years followed by later population decreases of Z. davisae, and it has been postulated this may be from increased native insect predation [72]. For chemical mitigation, the insecticides of abamectin, imidacloprid, or bidrin applied into sapwood are effective treatments for other gall wasps, including the horned oak gall wasp and the gouty oak gall wasp, and should have similar efficacy with Z. davisae [69]. For Z. davisae in particular, treatments with imidacloprid or emamectin benzoate reduced the number of cavities in new growth, lowered leaf damage, and resulted in lowered branch mortality (which can lead to fewer instances of total dieback) [73]. For large infestations of oak gall wasps, foliar sprays of chlorpyrifos or bifenthrin have success but also indiscriminately kill other native beneficial insects and should be used with caution [69]. In most forested stands, it is unlikely that these types of treatments would be economically or ecologically feasible.

6.2. Oak Borers

The oak splendor beetle (Agrilus biguttatus, Coleoptera: Buprestidae) is an oak generalist currently found in Europe and Africa, as well as western Middle Eastern countries and Asia. A. biguttatus has been linked to the convergence of pathogens and pests responsible for acute oak decline (AOD) in Europe and is on watch lists for accidental introduction into the United States through wood importation and packing materials [40]. A. biguttatus is considered a secondary pest, selecting trees which are already stressed or have breached bark, and prefers trees with thickened bark (particularly those with south-facing surfaces), which puts old growth oak stands at particular risk [42]. Oviposition occurs in areas of broken bark and hatched larvae bore deeper into the tree, feeding off cambium. Throughout the larval stages (which can be one to two years), wood boring continues and elongates, which can girdle and kill the host tree [43]. Adult beetles exit from large D-shaped holes and consume tree foliage. As symptoms of AOD include dark sap exuding from bark cracks in mature oak trees [180], the large exit holes left by A. biguttatus can contribute to further bacterial or other pathogenic infection entering already-stressed trees [181]. As cool and warm cycles are required for larval development, it remains to be seen how climate change will affect the lifecycle of A. biguttatus and its population overall [41]. Mitigation techniques to stop the spread of A. biguttatus further into Europe, Asia, and Africa and onto other continents include preventing the movement of firewood, sanitization of exported wood and packing materials, insecticides, removal of affected twigs, limbs, or trees, and biocontrol measures including woodpeckers [42,43].

The gold-spotted oak borer (Agrilus auroguttatus, Coleoptera: Buprestidae) is a western North American species with a small native range in Arizona but has been introduced and spread in southern California (likely brought in by human transport [182]) and causes significant mortality to coast live oaks (Q. agrifolia) [36,39]. Agrilus auroguttatus has caused one hundred percent mortality of oaks in some areas and could likely establish on a number of other oak species, particularly those in sect. Lobatae, if introduced elsewhere [183]. To date, no laboratory testing has been conducted with this species to determine the suitability of eastern oaks, thus, uncertainty remains and A. auroguttatus remains on a number of invasive species watch lists for the Eastern United States [184]. Trees attacked by A. auroguttatus produce excessive sap and tend to be larger-sized mature trees [37]. In its native range, A. auroguttatus has been reported on Emory oak (Q. emoryi) and Q. hypoleucoides (sect. Lobatae) (silverleaf oak), as well as coast live oak (Q. agrifolia), canyon live oak (Q. chrysolepis, sect. Protobalanus), and California black oak (Q. kelloggii, sect. Lobatae) [182]. It has been hypothesized that this species is so successfully attacking California oaks by colonizing non-coevolved trees with low host resistance in a region with limited natural insect enemies [182]. Natural biological control shows little prospect thus far at being effective [39]. As another wood borer that is difficult to manage directly, monitoring, quarantines, and prohibiting movement of firewood are the recommended management options [37,38,39].

7. Conclusions

Predicting the next key threats to oaks of the Northeastern, Midwestern, and Great Lakes regions of the United States and Canada will be an ongoing task, compounded by rapid changes in winter temperatures, greater intensity of storms, and other fluid variables. As the adage goes, we also “don’t know what we don’t know”—in other words, we can watch for issues we know are current or emerging threats but have little knowledge about many potential unknown or unexpected threats. A question that may help oaks to better cope with new pests and changing microclimates is whether oaks change secondary metabolites across latitude gradients, and will this affect insect predation? Secondary metabolites that dominate in oaks in more southern provenances could provide advantages to oaks in northern regions with warmer overall temperatures and especially warmer winters. Knowing these advantages could aid in developing assisted migration strategies to ensure oak species survival, and knowledge of what secondary metabolites are successful in curbing predation of herbivores in warm climates can also assist in finding optimal defense strategies for oaks. This may also lead to answers regarding variation of resistance or tolerance which exists within and between populations of the same oak species, and beneficial adaptations could be used to benefit a broader range of oaks [185]. Of particular note is A. bilineatus, which has a multitude of hosts in the United States and Canada on which to feed and could explode in population with a suitable climate with a major impact on Quercus and other hardwood species [47,186]. Monitoring the magnitude and method of spread should be closely monitored to compare to Agrilus expansion elsewhere.

The largest question remains: how can we predict the next key threat to oaks? The United States Forest Service maps current and potential hazards [187], but it is still difficult to predict the next big threat. Mapping and predictive modeling may be one way to address the probability of emerging threats to a certain area or region [188,189,190]. One barrier is simply knowing the current state or locations of insect or pathogen threats, particularly in rural or wilderness areas, which are sparsely visited. Though modeling may assist with predicting threats in such areas, implementing citizen scientists to detect herbivory damage and new movement of species as “boots on the ground” could also be immensely beneficial. However, this will require more targeted education and awareness campaigns. Local agencies could provide posters of potential threats to our forests, raise awareness through publications in local newspapers and newsletters, perform outreach at public spaces like libraries, Farmer’s Markets, or Community Gardens, and provide paths to document insect species movements (similar to what we have seen with L. dispar and L. delicatula in multiple citizen scientist web platforms and mapping databases). Data from such efforts could also lead, in turn, to better predictive modeling as herbivore movement is better documented and understood. Funding for non-targeted trapping and identification of insects in longitudinal and latitudinal sections could provide a broader picture of current insect species and population densities. For example, the emerald ash borer (Agrilus planipennis, Coleoptera: Buprestidae) is native to China and East Asia but first received widespread recognition as an invasive insect in Michigan in the early 2000s after it caused dieback and huge economic loss in ash trees (Fraxinus spp.) [191,192]. It has been postulated by dendrochronological studies that A. planipennis was actually present in the United States for a number of years before 2002 (even as far back as 1997) [193] and evaded detection, only becoming noticeable when it caused a significant amount of mortality in rows and rows of street trees. There could easily be enough oak stand density to see similar devastation in areas of the United States and Canada. Remaining vigilant of new and emerging threats with a combination of predictive modeling, citizen scientist observations, and continuing mitigation and remediation of current threats will help assist oak survival as we face fluid and vast ecological changes globally.