Tree-level distribution of a novel insect-pathogen complex and its potential contribution to eastern white pine dieback

Highlights

• A scale insect and pathogen are associated with novel eastern white pine dieback.

• Tree-level distribution of the insect-pathogen complex was assessed.

• Poletimber trees and saplings had the highest insect-pathogen incidence.

• Lower canopy branches and thin-barked areas had the highest incidence within trees.

• Distribution of the insect-pathogen complex mirrors bottom-up tree dieback.

Abstract

Bottom-up branch dieback and sapling mortality of eastern white pine (Pinus strobus L.) has been observed range-wide during the last two decades. Observational studies thus far implicate these symptoms to an insect, the eastern white pine bast scale (Matsucoccus macrocicatrices Richards), and a canker-forming, fungal pathogen, Caliciopsis pinea Peck. The scale insect was historically considered an innocuous herbivore of eastern white pine restricted only to New England and Canada, but is now found in high densities on symptomatic trees, in close association with Caliciopsis canker, and in almost every region where the host grows. We sampled branches and boles of eastern white pines in the southern Appalachians to better understand the distribution of the insect-pathogen complex on individual trees and among size classes. Results indicate distinct patterns, as branches of poletimber, boles of saplings, and branches lowest in the canopy harbored the greatest numbers of bast scales and had the highest proportional Caliciopsis canker area. The incidence of scales and cankers was generally highest on older tissue with high percent lichen cover, but with thinner outer bark. Tree-level distribution of the bast scale and Caliciopsis canker was non-random and in fact mirrored the observed dieback patterns reported for eastern white pine, indicating that these two organisms may be important contributors to tree dieback and mortality in the southeastern USA.

Introduction

Trees are spatially and temporally heterogeneous habitats for animals, with abiotic and biotic conditions varying at multiple strata (e.g., root, bole, branch, twig, cone, and foliage levels). As hosts, structural heterogeneity in trees influences herbivorous communities and populations (Lawton, 1983). Associated with varying tree size, age, and zonation are marked differences in physiology (e.g., tissue type, volume, texture, nutritional quality, and secondary defensive compounds), micro-environmental conditions (e.g., temperature and moisture), and natural enemy load (e.g., predators and parasitoids), which directly or indirectly affect the spatial colonization of herbivores (Lawton, 1983, Ulyshen, 2011, Wardhaugh, 2014). Many studies have investigated differences in herbivore communities within and across trees (e.g., Maguire et al., 2014, Plewa et al., 2017, Weiss et al., 2016), but fewer studies are available that assess such distributions of forest pest populations (e.g., Wardhaugh et al., 2006), including those associated with tree-killing pathogens. An understanding of tree-level colonization patterns may elucidate if a link exists between observed tree symptoms and the contributing pests and pathogens.

A novel dieback phenomenon is posing ecological and economic threats to eastern white pine (Pinus strobus L.) across its entire range in eastern North America (Asaro, 2011, Costanza et al., this issue, Lombard, 2003). The current symptoms are unrelated to known threats of eastern white pine, white pine blister rust (Cronartium ribicola Fisch) and white pine weevil (Pissodes strobi Peck), but rather include a progressive bottom-up thinning of the crown, where lower branches die steadily until the live canopy is reduced to terminal branches and the leader (Schulz et al., this issue-a, Schulz et al., this issue-b). Accompanying this pattern of branch dieback is the presence of characteristic cankers on branches and boles of trees. Severe resin outflow from cankers is common, especially on large diameter trees, which leads to decreased wood quality (Costanza, 2017). The cankers also cause girdling of stem and branches, thus killing trees (Overholts, 1930). Seedlings and saplings are particularly vulnerable to mortality, but the phenomenon has been reported from all diameter classes, thus threatening the resilience and sustainability of eastern white pine as a canopy species in eastern forests (Asaro et al., this issue, Costanza et al., this issue).

A variety of common fungi have been isolated from cankers on symptomatic eastern white pine, with Caliciopsis pinea Peck as the most ubiquitous and virulent species (Cram et al., 2009, Ray, 1936, Schulz et al., this issue-b). A native pathogen primarily of eastern white pine, C. pinea has been known throughout the eastern United States to be associated with sapling and branch mortality (Overholts, 1930, Ray, 1936), but never to an extent that would significantly threaten the health of the host-tree species across its range. Recent studies have established that C. pinea is strongly associated with current eastern white pine dieback and is now considered a main contributing factor throughout the host range (Lombard, 2003, Munck et al., 2015, Schulz et al., this issue-b). The fungal hyphae of C. pinea establish under the tree bark, grow into the vascular cambium, and kill host tissue. This infection results in the steady expansion of necrotic lesions from which annual crops of ascocarps, the distinctive hair-like fruiting bodies, are produced on the external surface of trees (Fig. 1) (Funk, 1963, Ray, 1936). Cankers sometimes coalesce with each other and will girdle branches and young stems (e.g., Fig. 1b). The epidemiology of the disease (Caliciopsis canker, hereafter) is not fully understood, but it has long been speculated that C. pinea requires an infection court in the form of an old lenticel, a natural bark crack, or an insect feeding wound to first colonize a host (Funk, 1963). In 2006, forest health specialists in Virginia discovered a scale insect, known as the eastern white pine bast scale, Matsucoccus macrocicatrices Richards (Hemiptera: Matsucoccidae), along the edge of Caliciopsis cankers; it has been suggested that the bast scale is likely facilitating C. pinea in its initial infection stage (Asaro, 2011, Mech et al., 2013). Historically believed to be a benign sap-sucking insect of eastern white pine, the bast scale is now strongly associated with both the dieback symptoms and the presence of Caliciopsis canker range-wide (Schulz et al., this issue-b).

The eastern white pine bast scale is native to North America and is a specialist on eastern white pine (Richards, 1960). The vast majority of its lifecycle is spent in its feeding stage as a sessile, 2nd instar juvenile: a black, eyeless, and legless cyst (Fig. 2a). With their relatively long piercing-sucking mouthparts (stylet) inserted into the outer phloem (bast), the insect cysts extract sugar-rich, vascular fluids for nourishment (Fig. 2b). Adult insect emergence occurs annually during the spring in the Southern Appalachians (Mech et al., 2013; Whitney pers. obs.), but occurs biennially at higher latitudes, presumably because winter is more prolonged (Watson et al., 1960). Winged males mate with quiescent females, and the females lay eggs in early summer. First instar “crawlers” hatch from eggs in summer and act as the main dispersal stage, hypothesized to utilize the wind to move to new trees, as in other scale insects (Bean and Godwin, 1955, Gullan and Kosztarab, 1997). After locating a suitable feeding site in late summer, often within bark crevices, under lichen, or along the edge of cankers, they insert their mouthparts into the tree and undergo a molt into the 2nd instar cyst (see: Costanza et al., this issue, Fig. 7 for additional lifecycle details). Mech et al. (2013) hypothesized that the feeding wounds created by the eastern white pine bast scale during its cyst stage facilitate C. pinea infection of its host. This proposed pathway of infection is similar to the beech bark disease complex, where two native fungi (Neonectria faginata Lohm. & Watson and N. ditissima Tul. & C. Tul.) exploit the minute feeding wounds of the introduced beech scale (Cryptococcus fagisuga Lindinger), leading to infection and loss of American beech (Fagus grandifolia Ehrh.) (Houston, 1994). No mechanistic work has yet investigated if eastern white pine bast scale feeding behavior aids and/or expedites pathogen infection, and thus it would be premature to attribute this as the cause of the dieback. However, there is correlative evidence to suggest there is an association between the two organisms and that together they contribute to extensive canker formations on branches and bole (Mech et al., 2013, Schulz et al., this issue-b).

Due to their historical reputations as negligible damaging agents, there is currently a paucity of substantive research on the eastern white pine bast scale, C. pinea, and their association (hereby referred to as the insect-pathogen complex). To assist with effective management or mitigation strategies, the basic biology of these organisms must be elucidated, including mechanisms of dispersal, colonization, and the relationship between C. pinea infection and insect feeding. Particularly urgent is the quantitative assessment of their distribution on symptomatic trees to infer where they may be preferentially colonizing. Such information may assist managers to identify particular trees within a stand or specific areas on a tree that are especially susceptible to insect-pathogen colonization for specific control prescriptions.

Our goal was to determine the distribution of both focal organisms, the eastern white pine bast scale and C. pinea, within and across eastern white pine trees. We assessed the incidence of the insect-pathogen complex on branches and boles according to: (1) tree size class (saplings, poletimber, and sawtimber) and (2) vertical distribution within the canopy (lower, middle, and upper crown). Our field observations indicate that intermediate-sized poletimber experience the most severe branch dieback and small saplings experience the most mortality. If the insect-pathogen complex were a driving force behind these symptoms, then the incidence of both organisms would be highest on branches of poletimber trees and on boles of saplings as compared to other size classes. The pattern of branch dieback across size classes also occurs from the bottom up on individual trees. Thus, higher incidence of bast scale and Caliciopsis canker was also expected on branches in the lower, rather than the upper canopy. We also compared incidence of the insect-pathogen complex according to: (3) horizontal distribution along the branches (proximal, medial, and distal), (4) vertical distribution on boles (lower, middle-lower, middle-upper, and upper), (5) branch-section diameter (an indication of tissue age), (6) bark thickness, and (7) percent lichen cover. We evaluated these variables in addition to our main objectives to determine if bast scales and C. pinea may colonize branches from the outside in or inside out, if vertical bole level or bole bark thickness is more of a limiting factor, and if the presence of lichen increases the incidence of colonization.