Insect infestations and the persistence and functioning of oak-pine mixedwood forests in the mid-Atlantic region, USA

Kenneth L Clark; Carissa Aoki; Matthew Ayres; John Kabrick; Michael R Gallagher

doi:10.1371/journal.pone.0265955

. 2022 May 4;17(5):e0265955. doi: 10.1371/journal.pone.0265955

Insect infestations and the persistence and functioning of oak-pine mixedwood forests in the mid-Atlantic region, USA

Kenneth L Clark ^1,^*, Carissa Aoki ², Matthew Ayres ³, John Kabrick ⁴, Michael R Gallagher ¹

Editor: Karen Root⁵

PMCID: PMC9067937 PMID: 35507583

Abstract

Damage from infestations of Lymantria dispar L. in oak-dominated stands and southern pine beetle (Dendroctonus frontalis Zimmermann) in pine-dominated stands have far exceeded impacts of other disturbances in forests of the mid-Atlantic Coastal Plain over the last two decades. We used forest census data collected in undisturbed and insect-impacted stands combined with eddy covariance measurements made pre- and post-disturbance in oak-, mixed and pine-dominated stands to quantify how these infestations altered forest composition, structure and carbon dynamics in the Pinelands National Reserve of southern New Jersey. In oak-dominated stands, multi-year defoliation during L. dispar infestations resulted in > 40% mortality of oak trees and the release of pine saplings and understory vegetation, while tree mortality was minimal in mixed and pine-dominated stands. In pine-dominated stands, southern pine beetle infestations resulted in > 85% mortality of pine trees but had minimal effect on oaks in upland stands or other hardwoods in lowland stands, and only rarely infested pines in hardwood-dominated stands. Because insect-driven disturbances are both delaying and accelerating succession in stands dominated by a single genus but having less effect in mixed-composition stands, long-term disturbance dynamics are favoring the formation and persistence of uneven age oak-pine mixedwood stands. Changes in forest composition may have little impact on forest productivity and evapotranspiration; although seasonal patterns differ, with highest daily rates of net ecosystem production (NEP) during the growing season occurring in an oak-dominated stand and lowest in a pine-dominated stand, integrated annual rates of NEP are similar among oak-, mixed and pine-dominated stands. Our research documents the formation of mixedwood stands as a consequence of insect infestations in the mid-Atlantic region and suggests that managing for mixedwood stands could reduce damage to forest products and provide greater continuity in ecosystem functioning.

Introduction

Throughout the Northeast and mid-Atlantic regions of the USA, intermediate age forests with median tree ages of approximately 70 to 110 years have regenerated following farm abandonment, the cessation of industrial forestry practices such as clearcutting and charcoal production, and a decrease in the occurrence of severe wildfires [1–3]. Disturbance regimes in these forests differ in spatial and temporal scales, and intensity, compared to previous stand replacing disturbances, and are now characterized by insect infestations, disease, windstorms, managed wildland fire, and harvesting [4–7]. Impacts resulting from infestations of native and non-native insects are especially acute in the northeastern US, as they now account for the majority of forest damage [8–11]. On the mid-Atlantic Coastal Plain, oak (Quercus spp.) tree mortality resulting from infestations of L. dispar (Lymantria dispar L.) in oak-dominated stands and pine (Pinus spp.) mortality following infestations of southern pine beetle (Dendroctonus frontalis Zimmermann) in pine-dominated stands over the last decade have far exceeded the area impacted by wildfires, harvesting or windstorms, which were previously the major disturbances in these forests [12–15].

The 445,000 ha Pinelands National Reserve (PNR) in southern New Jersey contains the largest forested area on the mid-Atlantic Coastal Plain. Following the cessation of intensive forest harvesting and charcoaling activities, less frequent wildfires because of suppression activities and changes in forest management practices have facilitated the establishment and persistence of oaks and other mesic hardwoods in the PNR (Fig 1; [12, 16–18]). More recently, oak tree and sapling mortality in oak-dominated stands infested by L. dispar have facilitated the release and regeneration of pines, leading to the formation of uneven-age mixed composition stands. These “mixedwoods” are characterized by neither hardwood nor softwood species exceeding approximately 75% dominance [e.g., 19–22]. Numerous pine-dominated stands established naturally following harvesting, charcoaling, and then repeated severe wildfires early in the 20^th century. Continued wildfire activity and landscape-scale prescribed burning has limited the regeneration of oaks and other mesic hardwoods and resulted in the persistence of pine-dominated stands [12, 16, 17, 23]. Over the last two decades, pine tree mortality as a result of southern pine beetle infestations in previously pine-dominated stands has increased the proportional basal area (BA; m^-2 ha^-1) and biomass of oaks in upland stands, and of hardwoods such as red maple (Acer rubrum L.) and black gum (Nyssa sylvatica Marshall) in lowland stands, also resulting in the formation of uneven-age mixedwood stands (Fig 1; [15, 24, 25]).

Fig 1 — In oak-dominated stands, repeated defoliation by L. *dispar* and differential mortality of oak trees and saplings facilitates the regeneration and release of pine seedlings and saplings. In pine-dominated stands, southern pine beetle causes significant pine tree mortality, while oaks in upland stands and other hardwoods in lowland stands are unaffected. These infestations are favoring the formation of uneven-aged, oak-pine mixedwoods in upland stands, and uneven-aged hardwood-pine mixedwoods in lowland stands.

Insect infestations that target specific softwood or hardwood species have short- and long-term effects on the functioning of forest ecosystems [13, 26–30]. In the absence of infestations or other major disturbance, annual net primary productivity (NPP) of intermediate age forests in the mid-Atlantic region derived from USDA Forest Inventory and Analysis data (FIA; [9]) and FIA-type forest census plots in the PNR range from 3.8 to 4.6 T C ha^-1 yr^-1; estimates for oak-dominated, oak-pine mixedwood, and pine-dominated forests from both sources are similar (S1 Table). Simulated values of NPP for oak-dominated, oak-pine mixedwood, and pine-dominated stands using three different process-based models are consistent with forest census estimates of NPP [31–34]. Estimated net ecosystem production (NEP) by oak-dominated, oak-pine mixedwood, and pine-dominated stands across the region derived from FIA data and model simulations range from 1.2 to 2.3 T C ha^-1 yr^-1 (S1 Table). Derived and simulated NEP estimates are consistent with annual NEP values calculated from eddy covariance measurements of net ecosystem exchange of CO₂ (NEE) during undisturbed years in intermediate age oak-dominated, oak-pine mixedwood, and pine-dominated stands in the PNR [13, 30] (S1 Table).

Short-term impacts of insect infestations on ecosystem functioning of mid-Atlantic forests have been well-characterized using forest census, remote sensing, and carbon flux measurements (e.g., [13, 30, 35]). In addition, several simulation models have captured the overall short-term dynamics of carbon and hydrologic cycling associated with insect infestations in these forests [27, 28, 36]. In summary, defoliators and bark beetles initially reduce the leaf area of susceptible species in infested stands by defoliation or host tree and sapling mortality, immediately reducing photosynthetic activity and autotrophic respiration, which decreases NEE and transpiration [13, 30, 37]. Compensatory photosynthesis by the remaining foliage, which is typically exposed to higher light levels, and the rapid cycling of nutrients from nutrient-rich litter and frass contribute to the maintenance of photosynthetic activity of the remaining foliage and facilitates resprouting of new foliage [38–41]. As a result, total CO₂ assimilation by photosynthesis, expressed as gross ecosystem productivity (GEP), evapotranspiration (Et) and ecosystem water use efficiency (WUE_e), defined as the amount of CO₂ assimilated per unit of water transpired, often recover relatively rapidly following insect damage or other disturbances [42–44].

Repeated defoliation over consecutive growing seasons, extensive bark beetle infestations, and other severe disturbances that result in tree and sapling mortality increase standing dead and coarse woody debris (CWD) on the forest floor. Additional detrital mass contributes to heterotrophic respiration as decomposition occurs, and has led to decadal-scale depressions in annual NEP in some forests of the PNR [29, 30]. Following significant mortality of oaks resulting from repeated L. dispar defoliation of an oak-dominated stand, Renninger et al. [29] estimated that increased release of CO₂ from standing dead and CWD would depress NEP for up to two decades. Flux measurements at this site have documented that NEP has averaged only 0.4 T C ha^-1 yr^-1 over the decade following the peak of oak mortality, representing 22% of pre-infestation values in S1 Table [30]. Similarly, Xu et al. [36, 45] used repeated forest census plots documenting increases in CWD coupled with a process-based productivity model and reported that relatively low annual NEP occurred in oak-dominated stands that had been impacted by L. dispar in the Delaware Water Gap, Pennsylvania, USA.

In addition to increased standing dead and CWD in intermediate age forests, other long-term effects of insect infestations include changes in species composition and age class structure resulting from differential tree mortality and regeneration (Fig 1). How these longer-term changes in composition and structure potentially alter ecosystem functioning in forests of the mid-Atlantic region have not been explored in detail. To evaluate the conceptual model in Fig 1 and understand how compositional and structural changes could affect ecosystem functioning over decadal time scales, we characterized how the most recent infestations of L. dispar and southern pine beetle in the PNR have 1) altered forest composition and age class structure, and 2) how the resulting changes potentially affect NEP, evapotranspiration (Et), and WUEe. We used forest census data collected in plots based on FIA protocols pre- and post-infestation and in comparative insect-infested and control stands to characterize changes in forest composition and structure. Eddy covariance measurements of NEE, energy, and water vapor fluxes in intermediate age oak-dominated, oak-pine mixedwood, and pine-dominated stands were employed to quantify NEP, Et and WUEe pre-, during, and post-infestation.

Materials and methods

Site description

Research sites were located in Atlantic, Burlington, Cumberland, and Ocean Counties in the Pinelands National Reserve (PNR) of southern New Jersey, USA. Oak-dominated, mixed-composition, and pine-dominated stands comprise the upland forests, and lowland forests are dominated by pitch pine (Pinus rigida Mill.), mixed hardwoods, and Atlantic white cedar (Chamaecyparis thyoides (L.) B.S.P). Most stands have regenerated naturally following cessation of timber harvesting and charcoal production towards the end of the 19th century, and severe wildfires throughout the 20^th century [12, 16, 18]. The climate is cool temperate, with mean monthly temperatures of 0.7 ± 2.4 and 24.6 ± 1.1°C in January and July, respectively (mean ± 1 SD;1988–2018; State Climatologist of New Jersey). Mean annual precipitation is 1183 ± 168 mm. Soils are derived from the Cohansey and Kirkwood formations, and upland soils are sandy, coarse-grained, and have low nutrient status, cation exchange capacity, and base saturation, while lowland soils are higher in accumulated organic matter and nutrients [46]. The landscape is characterized by a relatively high frequency of wildfires and prescribed burns compared to other forest ecosystems in the northeastern US; from 2004 to 2016, over 15,000 wildfires burned 36,654 ha and prescribed fires were conducted on 84,096 ha [18, 23, 47, 48]. On average, the annual area burned in prescribed fires now exceeds that burned in wildfires by a factor of two.

L. dispar infestations and forest structure

L. dispar has defoliated primarily oaks in large areas of upland forest throughout southern New Jersey over the last two decades. From 2004 to 2016, total acreage with heavy (50 to 75%) and severe (> 75%) canopy defoliation has totaled 328,700 ha in the four counties studied [49]. The majority of defoliation in a recent infestation occurred from 2005 to 2009, with peak damage occurring in 2007 when approximately 20% of upland forests in the PNR and 68,650 ha in the four studied counties were heavily to severely defoliated [13, 49].

Forest census plots based on FIA protocols [9] were sampled before (2004–2005), during (2007) and a decade after infestations (2018) to document the impacts of L. dispar infestations on forest composition and structure in three intermediate age stands of contrasting species composition in the PNR. Forest census plots were located in an oak-dominated stand at the Silas Little Experimental Forest (39.9156°N, -74.5955°E) in Brendan Byrne State Forest, a mixedwood stand co-dominated by pitch pine (Pinus rigida Mill.) and oaks at Fort Dix (39.9731°N, -74.4341°E), and a pitch pine-dominated stand near the Cedar Bridge fire tower (39.8398°N, -74.3787°E) in the Greenwood Wildlife Management Area, referred to below as “oak”, “mixed” and “pine”, respectively. Permission to access sites was granted through a long-term agreement between the USDA Forest Service and the New Jersey Department of Environmental Protection (NJDEP). Stands were selected to represent the dominant age class (75–95 years) of the three major upland forest types in the PNR, based on FIA data [50]. At the beginning of the study in 2004, the mean age of dominant trees was 90, 74 and 80 years at the oak, mixed and pine stands, respectively. The oak stand was dominated by chestnut oak (Quercus prinus L.), black oak (Q. velutina Lam.), white oak (Q. alba L.), and scarlet oak (Q. coccinea Muenchh.), with scattered shortleaf and pitch pines. The mixed stand was co-dominated by pitch pine and chestnut oak, with scattered white and post (Q. stellata Wangenh.) oaks. The pine stand was dominated by pitch pine, with post and white oak saplings in the lower canopy. All stands had bear and blackjack oaks (Q. ilicifolia Wang. and Q. marilandica Muench.), huckleberry (Gaylussacia baccata (Wang.) K. Koch and G. frondosa (L.) Torr. & A. Gray ex Torr.), and blueberry (Vaccinium spp.) in the understory. Sedges (Carex pensylvanica Lam.), bracken fern (Pteridium aquilinum (L.) Kuhn), mosses and lichens were also present. Further descriptions of each stand can be found in S2 Table and [13, 29, 30, 50].

Forest census measurements were conducted on five circular plots (201 m²) located within 100 m of each eddy covariance tower (described below) that were sampled annually at the oak and pine stands, and periodically at the mixed stand (sampling details are in [13, 30, 51]). In addition, 1-km² grids consisting of 16 FIA-type plots in a 4 by 4 arrangement centered on each eddy covariance tower were sampled periodically [51], with plots that occurred in non-forested areas such as sand roads or fire breaks omitted from these analyses. During each census, species, diameter at breast height (DBH; 1.37 m), height, and crown condition were recorded for all live and dead trees (> 12.5 cm DBH) and saplings (2.5 to 12.5 cm DBH). Allometric equations were used to calculate aboveground biomass and biomass of foliage of trees and saplings (S2 Table; [52–54]). Censuses in the five 201 m² plots at each site were also used to monitor seedling and sapling recruitment and mortality. To estimate stem and foliage biomass of scrub oaks and shrubs in the understory, two to four 1.0 m² destructively harvested subplots adjacent to each 201 m² census plot were harvested during peak leaf area of each growing season, dried at 70°C until dry and then weighed. Further descriptions of each stand can be found in S2 Table and [13, 29, 30].

Southern pine beetle infestations and forest structure

The recent southern pine beetle outbreak in New Jersey started in approximately 2000, and by 2016, approximately 19,500 ha had been infested, resulting in mortality of pitch, shortleaf (P. echinata Mill.), and Virginia (P. virginiana Mill.) pines in pine-dominated stands [14, 24, 55]. Pitch pine dominated lowlands have been impacted to a greater extent than pine dominated upland stands [24].

Forest census plots based on FIA protocols [9] were installed in 10 uninfested and insect-damaged areas in untreated pine-dominated stands of intermediate age, as part of a 51-stand census of southern pine beetle damage conducted throughout the PNR in 2014 and 2015 [24]. Permission to access stands was granted by NJDEP and the appropriate state forest supervisors. Aerial and ground-based surveys conducted by New Jersey Department of Environmental Protection and Dartmouth College researchers were used to locate beetle-damaged areas on public lands (primarily state forests and wildlife management areas), which ranged in size from 0.5 to 35.0 ha and were sampled approximately two to five years following infestation by southern pine beetle [24]. Of the 51 stands, 10 stands were unmanaged and no southern pine beetle suppression activities were conducted in infested areas; census data from these stands were analyzed here because suppression treatments occasionally damaged remaining pine trees and saplings in infested areas [24]. In the remaining 41 stands, southern pine beetle suppression treatments consisted of felling infested trees and saplings and cutting a buffer around the infestation, and then either leaving pine stems in place (“cut and leave”) or hauling logs to a landing zone and chipping them (“cut and chip”). All stands were initially dominated by pitch pine, with shortleaf and Virginia pine also present in some stands. The average age of sampled pine trees was 77 ± 24 years old (mean ± 1 SD) [25]. Upland stands also contained mixed oaks, sassafras (Sassafrass albidum (Nutt.) Nees), and an occasional beech (Fagus grandifolia Ehrh.) and lowland stands also contained red maple (Acer rubrum L.), black gum (Nyssa sylvatica Marshall), American holly (Ilex opaca Aiton), and sweetgum (Liquidambar styraciflua L). Further descriptions of each stand can be found in S3 Table and [24, 25].

Species, DBH, height, and crown position were recorded for all live and dead trees and saplings, and canopy cover was estimated visually for each FIA-type (168 m²) subplot in infested and uninfested areas. Understory height, species composition, and visually estimated cover by species (including tree seedlings) were recorded for each subplot, and pine seedlings were tallied in each subplot when present. Allometric equations based on destructive harvests were used to estimate total aboveground biomass and biomass of foliage of pine trees and saplings in each hsubplot (S3 Table; [24, 53]). Published values were used to estimate biomass and biomass of foliage for oaks and other hardwoods [52, 54, 56].

Leaf area and foliar nitrogen content

Specific leaf area (SLA; m² g dry weight^-1) of foliage of the dominant canopy and understory species was measured with a leaf area meter (LI-3000a, LI-COR Inc., Lincoln, Nebraska, USA) and a conveyer belt (LI-3050c, LI-COR Inc.) using fresh samples of leaves or needle fascicles, which were then dried at 70°C and weighed. Canopy leaf area index (LAI; m² m^-2 ground area) was estimated by multiplying leaf or needle mass calculated from allometric equations for each species by the appropriate SLA value and then summing results for all species. Projected leaf area of pine needle fascicles was multiplied by π/2 to calculate one-sided LAI. Understory LAI at the oak, mixed and pine stands was estimated by multiplying foliage mass of shrubs and oaks obtained from harvested 1.0 m² plots by the corresponding SLA values. Litterfall was collected monthly at the oak, mixed and pine stands when present from two 0.4-m² wire baskets per plot and used to estimate foliage mass and area for periods when extensive defoliation occurred. Relationships between leaf litter mass and SLA were developed for the dominant species using the same protocol used for fresh foliage.

Canopy and understory foliage was sampled for nitrogen concentrations ([N]) at the time of peak leaf area during the growing season at the oak, mixed and pine stands throughout the study. Oven-dry samples of live leaves or needles were ground using a Wiley mill (Thomas Scientific, Swedesboro, NJ, USA) and digested along with appropriate standards using a modified Kjeldahl method [57]. An Astoria 2 Analyzer (Astoria-Pacific International, Clackamas, OR, USA) was used to measure the ammonium concentration of each sample, and results were converted to [N] in foliage samples. Values for [N] of foliage were consistent with those reported in Renninger et al. [58, 59] and Guerrieri et al. [43, 44] for foliage at the oak and pine stands. Nitrogen content (g N m^-2 ground area) in canopy and understory foliage of each dominant species was then calculated by multiplying species-specific [N] by corresponding estimates of foliar biomass. At the stands infested by southern pine beetle, N content of foliage also was estimated using needle or leaf biomass estimates and mean foliar [N] of the dominant species.

Ecosystem functioning of oak-, mixed and pine-dominated stands

Closed-path eddy covariance systems and meteorological sensors mounted on antenna towers were used to quantify net ecosystem exchange of CO₂ (NEE) and latent heat flux at the oak-, mixed and pine-dominated stands. Values were integrated over the appropriate time intervals to estimate daily and annual net ecosystem production (NEP), evapotranspiration (Et), and ecosystem water use efficiency (WUE_e) pre-, during and post-infestation by L. dispar. Near-continuous measurements commenced in 2004 at the oak stand (two years prior to L. dispar infestations) and in 2005 at the mixed and pine stands (one and two years prior to L. dispar infestations, respectively). Eddy covariance systems, meteorological sensors, and data processing methods are described in detail in Clark et al. [13, 30] and in S4 Table. In summary, half-hourly fluxes were calculated from raw 10 Hz flux data using EdiRE [60], and values were rejected when instrument malfunction occurred, during measurable precipitation or when icing occurred, and when friction velocity (u*) < 0.2 m s^-1, which ensured well-mixed conditions. To estimate half-hourly NEE values when we did not have measurements, daytime NEE was modeled by fitting a rectangular hyperbola to the relationship between photosynthetically active radiation (PAR) and NEE at bi-weekly (May) to 3-month (summer; June 1 –August 31) periods. Nighttime NEE was modeled by regressing half-hourly net exchange rates on air temperature using an exponential function. Model parameters and their error terms for the relationships between half-hourly daytime or nighttime NEE and meteorological variables were calculated using SigmaPlot software (Version 12.5, Systat Software, Inc., San Jose, CA, USA). Continuous meteorological data and the appropriate model were then used to fill gaps for periods when fluxes were not measured, and measured and modeled values were summed to estimate daily and annual NEP. Ecosystem respiration (R_e) was estimated using nighttime NEE and continuous half-hourly air temperature during the growing season and soil temperature during the dormant season. Error in gap-filling NEE and R_e was evaluated for daytime and nighttime data using ± 1 standard error (SE) of each parameter used to model half-hourly NEE (see [30] for details). Daily NEP and R_e were summed to estimate daily and annual GEP values for each stand.

Evapotranspiration was estimated from latent heat fluxes calculated using EdiRE. Meteorological measurements were used to calculate available energy, defined as net radiation–(soil heat flux + heat storage terms), and gaps in Et data were filled using linear functions in SigmaPlot [37]. Half-hourly Et estimates were then summed to calculate daily and annual values. Ecosystem water use efficiency (g C kg H₂O^-1) is defined here as the ratio of daily GEP to transpiration [42–44]. Following Clark et al. [42], we used data collected when we assumed the canopy was dry to maximize the contribution of transpiration to Et in these calculations, and days with recorded precipitation and the day following each rain event when precipitation ≥ 10 mm day^-1 were excluded from analyses.

Statistical analyses

All datasets were first tested for normality using Kolmogorov-Smirnov tests, and homogeneity of variances among groups were tested using Levene’s test. Values for BA and aboveground biomass of trees and saplings, leaf area index, and nitrogen content of foliage among stands infested by L. dispar were compared using ANOVA analyses. Comparisons among stands were made with Tukey´s Honestly Significant Difference (HSD) tests that adjusted significance levels for multiple comparisons. Paired sample T-tests were used to compare pre- and post-infestation values within stands. Paired-sample T-tests were also used to compare forest structure variables in infested and uninfested areas in stands that had been impacted by southern pine beetle. Half-hourly values of NEE for daytime and nighttime periods, and daily values of NEP, Et and WUE_e were compared among stands using ANOVA analyses. Because half-hourly and daily values were not independent, we randomly selected 25 subsets consisting of 25 values for each variable, and then tested for differences among stands or time periods [42]. Comparisons among stands were made with Tukey´s HSD tests. All statistical analyses were conducted using SYSTAT 12 software (Systat Software, Inc., San Jose, CA, USA).

Results

L. dispar infestations and forest structure

Prior to L. dispar infestations, BA of trees and saplings was similar at the oak, mixed, and pine stands (Fig 2A and Table 1), while aboveground tree biomass was greater at the oak stand than at the mixed and pine stands (S2 Table). Leaf area was greatest at the oak stand and least at the pine stand during the growing season (Fig 2B). Similarly, N content of foliage was greater at the oak stand than at the pine stand during the growing season, with foliage of oak trees and saplings containing 77%, 51% and 12% of total foliar N content at the oak, mixed and pine stands, respectively (Fig 2C and Table 1). Standing dead tree and saplings and coarse woody debris mass was < 3.1 ± 0.6 t ha^-1 at the three stands at the beginning of the study (S2 Table; see [30] for details).

Table 1. Results of ANOVA and Tukey’s HSD analyses for structural characteristics of forests infested by L. dispar.

Comparison	F_2,12	P	Contrasts	Figure
*Before L. dispar* infestations in 2004 (“Pre” in Fig 2)**
Tree and sapling BA	1.0	NS	NS	2A
Leaf area index	4.6	< 0.05	O > P	2B
N content of foliage	4.4	< 0.05	O > P	2C
*During L. dispar* infestation in 2007 (“Inf” in Fig 2)**
Tree and sapling BA	2.3	NS	NS	2A
Leaf area index	1.6	NS	NS	2B
N content of foliage	0.2	NS	NS	2C
*Following L. dispar* infestations in 2018 (“Post” in Fig 2)**
Tree and sapling BA	3.6	< 0.10	P > M	2A
Leaf area index	0.2	NS	NS	2B
N content of foliage	0.4	NS	NS	2C

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Statistical tests are for tree and sapling basal area (BA), and canopy and understory leaf area index and nitrogen (N) content of foliage in stands before, during and following L. dispar infestations shown in Fig 2. O = oak stand, M = mixed stand, P = pine stand. NS = not significant.

Infestations of L. dispar occurred at the oak stand during the growing seasons of 2006 to 2008. During the peak of defoliation in 2007, leaf area of oaks, pines and understory vegetation was reduced to near zero, and a second partial leaf-out resulted in a total leaf area and foliar N content of only 42% and 40% of pre-defoliation values, respectively (“Inf” in Fig 2B and 2C). Following infestations, oak mortality peaked from 2009 to 2011, and by 2018 oak tree and sapling BA had been reduced by ≈ 40% compared to pre-infestation values. Overstory mortality resulted in the release of pine saplings and establishment of seedlings in the understory, and by 2018 pine trees and saplings accounted for 38% of total BA (“Post” in Fig 2A). Although BA increment of surviving trees at the oak stand was positive, total BA and above-ground biomass were similar at the beginning and end of the study in 2018. Oak mortality reduced stand leaf area and foliar N content, and in 2018, N content of oak tree and sapling foliage was less than pre-infestation values (T₄ = 3.53, P < 0.05), accounting for only 63% of total foliar N content (Fig 2C and Table 2). Oak mortality following L. dispar infestations resulted in a maximum standing dead and CWD mass of 31.1 ± 9.1 t ha^-1 (mean ± 1 SE) in 2011, and by 2018 standing dead and CWD mass was estimated to be 19.0 ± 5.3 t ha^-1 (S2 Table; see [30] for details).

Table 2. Results of paired-sample T-tests for structural characteristics of stands infested by southern pine beetle.

Comparison	T_1,9	P value	Figure
Tree and sapling BA	6.0	< 0.01	3A
Pine trees	6.9	< 0.01	3A
Pine saplings	0.2	NS	3A
Oaks and other hardwoods	1.1	NS	3A
Leaf area index	5.2	< 0.01	3B
Pine trees and saplings	7.7	< 0.01	3B
Oaks and hardwoods	0.4	NS	3B
N content of foliage	6.6	< 0.01	3C
Pine trees and saplings	7.7	< 0.01	3C
Oaks and other hardwoods	0.6	NS	3C

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Statistical tests are for trees and saplings in infested and uninfested areas shown in Fig 3.

At the mixed stand, L. dispar infestations occurred from 2006 to 2008, but in contrast to the oak stand, oak tree and sapling mortality was minor following infestations (Fig 2A). Defoliation by L. dispar reduced leaf area and foliar N content of deciduous species to very low values in 2007 but had relatively little effect on foliage of pine trees and saplings (Fig 2B). By the end of the study in 2018, BA of trees and saplings had increased by 22% compared to values in 2004. Increases in both pine and oak tree BA resulted from growth increments and sapling recruitment, despite some sapling mortality that occurred during the three prescribed fires conducted between 2006 and 2018. Leaf area and N content of foliage during the growing season of 2018 at the mixed stand had increased 15% and 18% compared to 2004, although increases were not statistically significant (Fig 2B and 2C and Table 1).

At the pine stand, oak sapling mortality was minimal following L. dispar infestations (Fig 2A). Partial defoliation of the understory and oak saplings by L. dispar in 2007 reduced understory LAI and N content compared to pre-disturbance periods but had little effect on pine foliage (Fig 2B and 2C). Growth increments of trees and saplings resulted in an increase in BA of 56% between 2004 and 2018. Although prescribed fires were conducted at the pine stand in 2008 and 2013 (see [30] for details), leaf area and foliar N content had increased 50% and 49% by 2018 when compared to 2004, following a longer-term trend of recovery from a severe wildfire that had occurred in 1995 (Fig 2B and 2C).

Southern pine beetle infestations and forest structure

Pine tree basal area averaged 21.8 ± 2.8 m² ha^-1 in areas that were not infested by southern pine beetle in southern New Jersey. Pine trees and saplings in uninfested areas accounted for 75% of total BA, 61% of tree and sapling leaf area and 78% of tree and sapling foliar N content (Fig 3 and S3 Table). Infestations of southern pine beetle resulted in significant mortality of pitch, shortleaf and Virginia pine trees, averaging 92% of pine tree BA, while pine sapling BA was reduced by only approximately 5% in infested areas (Fig 3A). Beetle infestations had little effect on the BA of oak trees and saplings in upland areas or of other hardwood trees and saplings such as red maple and black gum in lowland areas (Fig 3A and Table 2).

Fig 3 — (A) Basal area of pine, oak and other hardwood trees and saplings, (B) maximum leaf area of pines, oaks, and other hardwoods during the growing season, and (C) maximum foliar N content of pines, oaks, and other hardwoods during the growing season in uninfested areas and areas following infestation of southern pine beetle in southern New Jersey. Other hardwoods include red maple (*Acer rubrum* L.), black gum (*Nyssa sylvatica* Marshall), sassafras (*Sassafras albidum* (Nutt.) Nees), sweet gum (*Liquidambar styraciflua* L.), and sweetbay magnolia (*Magnolia virginiana* L.).

Following southern pine beetle infestations, tree and sapling leaf area and foliar N content in infested areas averaged 42% and 26% of values for uninfested areas, respectively (Fig 3B and 3C). While pine leaf area and foliar N content was reduced significantly, leaf area and foliar N content of oaks and other hardwoods were nearly unchanged (Fig 3B and 3C and Table 2). CWD was highly variable in infested areas due to a large proportion of standing dead trees in some stands (S3 Table).

Convergence of forest structure following insect infestations

By the end of the study, changes in stand composition and structure at the oak-dominated stand impacted by L. dispar and at untreated, previously pine-dominated stands infested by southern pine beetle converged on attributes characterizing the mixed stand measured at the beginning of the study. For example, Fig 4 indicates the similarity in relative BA of trees and saplings among the oak stand in 2018 following L. dispar defoliation, the mixed stand at the beginning of the study in 2005, and untreated pine stands following infestation by southern pine beetle.

Fig 4 — Data are from the oak stand before L. *dispar* infestation in 2005 and following tree and sapling mortality in 2018, the mixed stand at the beginning of the study in 2005, and untreated pine-dominated areas following infestation by southern pine beetle and uninfested areas. Oaks and other hardwoods have been combined as “hardwoods”. Arrows indicate the directional changes caused by insect infestations.

Ecosystem functioning of oak-, mixed and pine-dominated stands

Summertime (June 1 to August 31) half-hourly NEE during midday clear sky conditions and daily (24-hour) NEP were greater at the oak stand than at the mixed and pine stands before L. dispar infestations (Tables 3 and 4 and Fig 5A). However, the opposite pattern occurred during the spring and fall seasons; before leaf expansion of oaks and understory vegetation in spring (April to mid-May), half-hourly NEE during midday clear sky conditions and daily NEP were greater at the pine stand than at the mixed and oak stands (Fig 5A and Table 4). Annual NEP was similar at the oak and pine stands, and somewhat lower at the mixed stand before L. dispar infestations, although complete annual data for the pre-disturbance period at the mixed stand were only available for 2005 (Table 5). Daily GEP and WUE_e were also greater at the oak stand than at the mixed and pine stands during the summer, while daily GEP and WUE_e during the spring were greater at the pine stand than at the oak and mixed stands (Figs 5B and 6B). Daily evapotranspiration rates during the summer were similar among stands, with annual values averaging 51% to 62% of incident precipitation (Table 5).

Table 3. Half-hourly net CO₂ exchange (NEE) during spring (April 1 to May 15) and summer (June 1 to August 31) months at the oak, mixed and pine stands.

Season	Half-hourly NEE (μmol CO₂ m^-2 s^-1)
	Oak	Mixed	Pine	Statistics
*Daytime, before L. dispar* infestations**
Spring	0.42 ± 1.68^a	-2.57 ± 2.01^b	-7.05 ± 1.69^c	F_2,72 = 109.0, P < 0.001
Summer	-19.80 ± 4.65^a	-16.18 ± 3.84^b	-15.92 ± 3.73^b	F_2,72 = 7.0, P < 0.01
*Nighttime, before L. dispar* infestations**
Spring	2.32 ± 1.63	1.87 ± 1.52	2.38 ± 1.64	F_2,72 = 0.8, NS
Summer	5.86 ± 2.65^ab	4.80 ± 1.91^a	6.51 ± 2.25^b	F_2,72 = 3.6, P < 0.05
*Daytime, during L. dispar* infestation in 2007**
Spring	0.74 ± 1.91^a	-2.88 ± 1.78^b	-6.28 ± 2.24^c	F_2,72 = 103.9, P < 0.001
Summer	-2.40 ± 2.96^a	-6.72 ± 5.69^b	-10.08 ± 3.34^c	F_2,72 = 29.4, P < 0.001
*Nighttime, during L. dispar* infestation in 2007**
Spring	1.61 ± 1.46	1.72 ± 1.00	2.32 ± 1.63	F_2,72 = 2.4, NS
Summer	3.54 ± 2.54^a	4.01 ± 1.91^ab	5.19 ± 2.40^b	F_2,72 = 4.4, P < 0.05
*Daytime, following L. dispar* infestations in 2018**
Spring	-1.24 ± 2.14^a	===	-8.11 ± 3.23^b	T₄₈ = 8.9, P < 0.01
Summer	-15.90 ± 5.03	===	-14.13 ± 3.55	T₄₈ = 1.4, NS
*Nighttime, following L. dispar* infestations in 2018**
Spring	2.88 ± 2.21	===	2.57 ± 2.20	T₄₈ = 0.5, NS
Summer	6.44 ± 3.57	===	6.19 ± 3.25	T₄₈ = 0.3, NS

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Daytime NEE values are midday values at PAR ≥ 1500 μmol m^-2 s^-1 and nighttime NEE values are during well-mixed conditions when friction velocity (u*) is ≥ 0.2 m s^-1. All values are means ± 1 SD. NS = not significant.

Table 4. Results of ANOVA analyses for ecosystem functioning of the oak, mixed and pine stands.

Comparison	F_2,72	P	Contrasts	Figure
*Before L. dispar* infestations in 2005**
Spring NEP	68.4	< 0.001	O = M < P	5A
Summer NEP	8.6	< 0.001	O > M = P	5A
Spring GEP	42.3	< 0.001	O = M < P	5B
Summer GEP	10.6	< 0.001	O > M = P	5B
Spring Et	25.0	< 0.001	O = M < P	6A
Summer Et	1.0	NS	NS	6A
Spring WUE_e	21.4	< 0.001	O = M < P	6B
Summer WUE_e	14.0	< 0.001	O > M = P	6B
*Following L. dispar* infestations in 2018**
Spring NEP	29.7	< 0.001	O = M < P	5A
Summer NEP	2.8	NS	NS	5A
Spring GEP	19.4	< 0.001	O = M < P	5B
Summer GEP	7.0	< 0.005	O > M = P	5B
Spring Et	14.2	< 0.001	O = M < P	6A
Summer Et	2.2	NS	NS	6A
Spring WUE_e	22.1	< 0.001	O = M < P	6B
Summer WUE_e	1.9	NS	NS	6B

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Statistical tests are for daily net ecosystem production (NEP), gross ecosystem production (GEP), evapotranspiration (Et), and ecosystem water use efficiency (WUE_e) at the oak, mixed and pine stands shown in Fig 5. O = oak stand, M = mixed stand, P = pine stand, NS = not significant.

Fig 5 — Data are presented for (A) daily net ecosystem production, (B) daily gross ecosystem production during late spring (April 1 to May 15) and summer (June 1 to August 31) months. Arrows indicate the directional changes in forest structure and composition following L. *dispar* infestations. Pre-infestation data are adapted from Clark et al. [13, 42].

Table 5. Annual values of net ecosystem production (NEP), gross ecosystem production (GEP), precipitation, and evapotranspiration (Et) at the oak, mixed and pine stands.

Stand	NEP	GEP	Precipitation	Et
	g C m^-2 yr^-1	g C m^-2 yr^-1	mm yr^-1	mm yr^-1
*Before L. dispar* infestations in 2005**
Oak	169 ± 24	1593 ± 58	1100	647
Mixed	137 ± 19	1205 ± 57	1184	607
Pine	173 ± 18	1513 ± 36	1230	757
*During L. dispar* infestation in 2007**
Oak	-246 ± 14	676 ± 46	934	442
Mixed	-20 ± 20	958 ± 52	1135	419
Pine	49 ± 7	1378 ± 43	1052	593
*Following L. dispar* infestations in 2018**
Oak	27 ± 15	1550 ± 43	1397	740
Pine	173 ± 18	1585 ± 48	1580	858

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Data are for years before, during, and following L. dispar infestations. Error terms were calculated from maximum deviations from average values generated using ± 1 SE of parameter values used to gap-fill missing half-hourly daytime and nighttime NEE (see [13, 30] for complete description of gap-filling procedures and error term calculations).

Fig 6 — Data are presented for (A) daily evapotranspiration, and (B) daily ecosystem water use efficiency during late spring (April 1 to May 15) and summer (June 1 to August 31) months. Arrows indicate the directional changes in forest structure and composition following L. *dispar* infestations. Pre-infestation data are adapted from Clark et al. [37, 42].

Changes in the distribution of leaf area and foliar N content at the oak stand following L. dispar infestations coincided with springtime increases in half-hourly NEE during midday when PAR > 1500 μmol m^-2 s^-1 and daily NEP, and reduced summertime half-hourly midday NEE and daily NEP, with values during both periods approaching those previously measured at the mixed stand at the beginning of the study (Table 3 and Fig 5A; post-defoliation values in 2018). Daily GEP during the summer at the oak stand was similar in 2005 and 2018, but daily WUE_e was somewhat lower in 2018 and equivalent to rates measured previously at the mixed stand in 2005 (Figs 5 and 6). In contrast, seasonal patterns of daily NEP, GEP, Et and WUE_e at the pine stand were similar in 2005 and 2018 (Figs 5 and 6).

Discussion

Infestations of L. dispar are delaying successional changes in oak-dominated stands and southern pine beetle infestations are accelerating changes in pine-dominated stands, while having only moderate effects in mixedwood stands on the mid-Atlantic Coastal Plain. In our study, the composition and structure of oak-dominated stands infested by L. dispar and of pine-dominated stands infested by southern pine beetle are converging on those characterizing oak-pine mixedwoods in upland stands and hardwood-pine mixedwoods in lowland stands, with similarly proportioned distributions of BA, leaf area, and foliar N content among oaks or other hardwoods and pines. In the long term, repeated but less severe insect infestations and current fire management strategies, including both wildfire suppression and the extensive use of prescribed fires, will likely favor the persistence of oak-pine and hardwood-pine mixedwoods throughout the PNR, consistent with the conceptual model in Fig 1. These outcomes parallel observations in other mixedwood forests consisting of species with varying susceptibility to insects, which can persist through time because of greater associational resistance to infestations compared to those dominated by a single species or genus [61, 62]. They are also consistent with the theoretical framework proposed by Kern et al. [22], who predicted that insect infestations, a disturbance from above because the canopy is impacted, coupled with low-intensity surface fires, a disturbance from below which promotes the regeneration of shade-intolerant species, would result in the persistence of mixedwood forests through time. Our study further suggests that ecosystem functioning, especially NEP and GEP, will recover relatively rapidly in oak–pine or other hardwood–pine mixedwood stands, as they can be expected to experience less defoliation and/or lower amounts of tree and sapling mortality compared to infestations of L. dispar in oak-dominated stands or southern pine beetle in pine-dominated stands.

Tree species composition and initial foliage quality of canopy species (approximated by foliar [N] in our study) influence the occurrence of the multi-year population outbreaks of L. dispar which result in the extensive mortality of susceptible species [7, 63–65]. In our study, differential mortality of black and white oaks, which have relatively high foliar [N] (≈ 2.1% N; [66, 67]), resulted in increased dominance of chestnut oak (as reflected in increased relative BA) with lower foliar [N] (≈ 1.9% N; [43, 44]). Reduced cover of oak trees and saplings facilitated the growth of pine saplings and the establishment and recruitment of pine seedlings, which have much lower foliar [N] than canopy oaks (1.0 to 1.3% N), and increased leaf area and biomass of understory vegetation [30]. The decrease in BA of susceptible oak species and reduction in oak leaf area, combined with lower mean [N] of canopy foliage because of the increase in pine foliage, will likely reduce the severity of L. dispar infestations in the future [7, 11, 63–65]. This outcome is consistent with observations from oak-pine mixedwood stands, where although infestations occurred and oak trees and saplings were defoliated, cumulative mortality was less extensive. Over time, repeated but less severe insect damage to oaks coupled with pulses of pine seedling establishment and saplings recruitment associated with prescribed fires will delay successional changes and likely result in uneven age mixedwood stands, as proposed in Fig 1.

Extensive pine tree mortality in areas infested by southern pine beetle reported here is similar to their impacts in pine-dominated forests across the southeastern USA [68]. Initial BA of pine trees and saplings in infested stands in the PNR (≈ 22.7 m² ha^-1) was greater than the average BA that can favor the large southern pine beetle aggregations leading to significant pine tree mortality in southeastern USA forests (≈ 18 m² ha^-1) [14, 25, 68]. In contrast, oak trees and saplings in upland stands and other hardwood trees and saplings in lowland stands were essentially unaffected in infested areas, and they were often retained where suppression treatments (e.g., cut and leave, cut and chip) were conducted in the PNR [24], and more recently, further north on the Atlantic Coastal Plain on Long Island, New York, USA [15, 55]. Southern pine beetle rarely impacted pines in oak-dominated stands in upland locations, or in hardwood-dominated stands in lowland locations in the PNR. Similarly, Huess et al. [15] reported that pine mortality was lower in mixed pine–oak stands than in pine-dominated stands following southern pine beetle infestations on Long Island, NY. In our study, BA of pine trees and saplings (≈ 2.5 m² ha^-1) in infested and treated areas was well below the densities that would support future aggregations of southern pine beetles [24, 55, 68]. Overall, southern pine beetle damage can accelerate succession in infested stands on the Atlantic Coastal Plain, also resulting in the formation of uneven age, mixedwood stands, consistent with the conceptual model in Fig 1.

Field measurements and model simulations indicate that daily NEP, GEP and WUEe during the growing season are greatest in oak-dominated stands and daily values in oak-pine mixedwood stands are intermediate between oak- and pine-dominated stands [13, 30]. Daily NEP and GEP during the growing season are strongly correlated with leaf area and canopy N content in forests of the PNR [30, 31, 59, 67], consistent with the relationship between LAI, canopy N content, and NEP during the growing season reported for forests at landscape to regional scales throughout the Northeastern USA [e.g., 35, 69, 70]. Pines and other evergreens in mixedwood and pine-dominated stands, however, are more productive during periods of time when deciduous oaks, other deciduous hardwoods, and many understory species are dormant. Integration of the seasonal patterns of C assimilation by oaks, pines and understory species results in more similar annual rates of NEP, GEP and WUEe among oak-dominated, oak-pine mixedwood, and pine-dominated stands [13, 30; S1 Table]. Thus, the long-term changes in species composition and structure associated with insect infestations may have little effect on forest carbon dynamics and hydrologic cycling at annual time scales in forests of the Mid-Atlantic region. In contrast, short-term carbon dynamics following infestations are strongly influenced by stand species composition. Field measurements and model simulations have documented how insect-driven disturbance and widespread tree and sapling mortality of susceptible species can reduce NEP for at least a decade following infestations [26–30, 36, 45]. Large-scale assessments have documented how differential mortality of oaks caused by L. dispar infestations in oak-hickory forests have reduced or negated net increases in BA and aboveground biomass across the mid-Atlantic region [7, 65, 71]. Because mixedwood stands are more resistant to infestations and sustain less extensive damage, they will likely maintain continuity in ecosystem functioning to a greater extent than oak- or pine-dominated stands during and following insect infestations [61, 62].

Numerous forest tree species in the mid-Atlantic region are tolerant of drought and fire, and many are characterized by regeneration strategies that enhance survival following fires or other disturbances (e.g., epicormic budding in pitch and shortleaf pines, serotinous cones in some pitch pine populations, prolific resprouting in most oaks and red maple) [16, 38, 72]. The use of prescribed fire to promote the regeneration of both oaks and pines is well documented in oak–pine mixedwood stands throughout the mid-Atlantic region [47, 73–77]. In the PNR, the majority of prescribed fires are conducted during the early spring, before oaks and other hardwoods have leafed out, and when pitch and shortleaf pines carry only a single cohort of needles. A seasonal peak in severe wildfires follows later in spring, also occurring before leaf expansion of deciduous species [23, 47, 73, 78]. Mixedwood stands can be less prone to severe wildfires compared to pine-dominated stands during the dormant season, because deciduous oaks or other hardwoods are interspersed between pine canopies, reducing the continuity of crown fuels and the density of ladder fuels [12, 16, 23, 24, 53, 79]. In lowland forest stands, hardwoods such as red maple and sweetgum are less tolerant of fire than many oak species, but the use of prescribed fires and wildfires are less frequent [16, 47, 77]. Overall, the continued extensive use of prescribed fire and wildfire suppression contributes to oak and pine regeneration and likely favors the persistence of oak-pine mixedwood forests, consistent with Fig 1.

Many of the dominant species in oak-pine and hardwood-pine mixedwoods are also considered to be relatively resistant to changes in climate, and are distributed across wide geographical and elevational ranges, can tolerate degraded, resource-limited environments, and some species tolerate extreme ranges in hydrologic conditions (e.g., pitch and shortleaf pines) [20, 72, 80]. A number of the dominant species in the mid-Atlantic region have already displayed increases in productivity and WUE_e, as a result of increased ambient CO₂ concentrations driving reduced transpiration [81, 82] and enhanced photosynthetic assimilation rates [43, 44]. In a previous study using LANDIS II to simulate future interactions of wildfire and climate in forests of the PNR, these factors were predicted to have only moderate effects on productivity of the major tree species, primarily because of their tolerance to drought stress and capacity to recover quickly from wildfires [34, 72].

Finally, our study provides some insight into the value of incorporating oak-pine mixedwoods into management strategies for forests in the mid-Atlantic region. Although mixed composition stands are typically more expensive to manage, they provide a greater variety of forest products when harvested selectively or thinned [20, 83]. As these forests age, simulating natural successional processes (e.g., forest thinning, mortality, regeneration) or delaying them through the use of prescribed fire and other silvicultural management practices would create more resistant forests [84–86]. Over time, treatments including prescribed burning, mechanical thinning, and selective cutting could reduce mortality of commercially important species while stimulating regeneration of key oak and pine species. By diversifying age class distributions and further enhancing forest heterogeneity, multi-aged mixedwoods management strategies may be particularly successful [22, 62, 87]. During and following infestations, lower levels of tree and sapling defoliation result in a more rapid recovery of leaf area and productivity, and reduced mortality decreases the amount of standing dead and coarse woody debris contributing to ecosystem respiration. Thus, one important benefit of mixedwood management is the faster recovery times of NEP to pre-infestation rates following insect infestations, maintaining forest carbon sequestration rates with only minor alterations to hydrologic resources. Forest insects have already shown us how effective such management strategies could be.

Conclusions

Insect damage is now the dominant disturbance in forests of the mid-Atlantic region. Insect infestations that target dominant tree species are altering forest composition and structure, resulting in stands that consist of mixtures of pines, oaks, and other hardwoods. Despite difference in forest composition, FIA data, process-based forest productivity models, and carbon flux measurements indicate that oak-dominated, oak-pine mixedwood, and pine-dominated forests typically have similar NPP and NEP on annual time scales. Oak-pine mixedwood stands may be relatively resistant to future outbreaks of defoliators and bark beetles, reducing economic losses associated with tree mortality, and potentially mitigating the short-term impacts to ecosystem functioning resulting from insect damage, especially carbon sequestration. Management strategies that incorporate oak-pine mixedwood stands may increase the supply of undamaged forest products and provide better continuity in ecosystem services despite projected increases in forest insect infestations associated with changing climate.

Supporting information

S1 Table. Productivity of undisturbed oak-dominated, mixed oak-pine, and pine-dominated forests in the mid-Atlantic region.

Data are net primary production estimated from USFS Forest Inventory and Analysis data (FIA, [9]) and forest inventory plots in the Pinelands National Reserve (PNR, [13, 30]), simulated net primary production using PnET CN, a process-based forest productivity model [30, 31], WxBGC, a second process-based forest productivity model based on BiomeBGC [32], and LANDIS II, a plot-based model that simulates forest composition, succession, disturbance and other ecological processes linked to the CENTURY succession extension (ver. 3) [33]. Estimated net ecosystem productivity is derived from FIA data, simulated using WxBCG and LANDIS II, and calculated from carbon flux measurements in the PNR [13, 30].

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S2 Table. Structural characteristics of the canopy and understory in oak, mixed, and pine stands.

Data are presented for the beginning of the study in 2005 before infestation by gypsy moth, and at the end of the study in 2018. Values are means ± 1 SE. Significance levels were tested using ANOVAs and Tukey’s HSD tests, and values indicated with different superscripts among stands are significantly different.

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S3 Table. Structural characteristics of the canopy and understory in uninfested areas and areas infested by southern pine beetle.

Values are means ± 1 SE. Significance levels were tested using paired sample T-tests, and values indicated with different superscripts among areas are significantly different.

(PDF)

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S4 Table. Meteorological sensors and eddy covariance equipment used to measure turbulence, net ecosystem exchange of CO₂ (NEE) and evapotranspiration (Et) at the oak, mixed and pine stands.

(PDF)

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Data Availability

Most of the carbon and water flux data used in our analyses are already available at the Ameriflux data archive (https://ameriflux.lbl.gov/sites/siteinfo/US-Slt, https://ameriflux.lbl.gov/sites/siteinfo/US-Dix, and https://ameriflux.lbl.gov/sites/siteinfo/US-Ced for the oak, mixed and pine stands, respectively. Much of the forest census data for the three sites impacted by gypsy moth are available from the USDA Forest Service Research Data Archive, Fort Collins, CO: https://www.fs.usda.gov/rds/ archive/.

Funding Statement

Partial support for this project was provided by USDA Forest Service Forest Health and Monitoring Program (https://www.fs.fed.us/foresthealth/) grants NE-EM-F-13-01 to KC and NE-EM-B-12-01 to MA and AK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0265955.r001

Decision Letter 0

Karen Root

4 Jan 2022

PONE-D-21-34003Insect Infestations and the Persistence and Functioning of Oak-Pine Mixedwood Forests in the Mid-Atlantic Region, USA.PLOS ONE

Dear Dr. Clark,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

Your paper addresses the very interesting question of how insect infestations may affect forest composition, carbon dynamics, and hydrological cycling in northeastern forest stands. This is a particularly important question as damage from pests, such as gypsy moths and pine beetles, seems to be increasing. While this could be an important contribution to our approach to managing forests, I agree with the reviewers that the paper has a lot of promise but needs some additional strengthening and clarification. As Reviewer #2 points out, there is a lot of information in the introduction but the purpose is not as clear here as in the discussion. There are some very good recommendations that they make to improve clarity and flow in the introduction. There are a number of places where the descriptions of the different sites surveyed is confusing. Please note some of the issues highlighted by both reviewers throughout the methods and the results. In particular, it is difficult to disentangle the labels for the pine sites that are infested or not by southern pine beetle and treated (managed?) or not. Or is the treatment status ignored for the purposes of your comparisons? Reviewer #2 has provided extensive line by line suggestions that should be carefully addressed.

The discussion repeats a lot of the results but could be strengthened by discussing the broader context and complicating factors such as fire, climate change, and herbivory and reducing the reiteration of the results. Figure 1 is very useful as a framework for the paper and it should be revisited more substantially in the discussion. For example, there is little discussion of differential impacts in uplands and lowlands but rather an emphasis on pine versus oak. I agree with Reviewer #2 that there should be more discussion of fire, especially since fuels were measured (Line 277) for at least some sites. Does fire in these systems both prescribed and wild complicate conclusions about the effects of the infestation and resilience to disturbance? It would be useful to discuss some of the implications of these findings and how they might apply in other contexts.

Both reviewers provide some suggestions to improve the tables and figures. For example, Reviewer #1 suggests more contrast is needed for Figure 6b and should more closely resemble 6a. You might even want to similarly improve the contrast of Figure 5. The figures are generally helpful but there is no description in the figure legends what the arrows on the graphs are indicating.

This paper has a lot of promise and could be a good addition to the literature with some improvements.

==============================

Please submit your revised manuscript by Feb 18 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Karen Root, Ph.D.

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #2: Yes

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Reviewer #1: Great work, just a few minor edits found.

Line 42 would be good to note that it is a decrease in sever wildfires.

Line 59-60 reword, for example: These "mixedwoods" are characterized by neither hardwood nor softwood exceeding 75% dominance.

Line 87 says oak pine mixedwoods, but isn't it also making lowland deciduous pine mixedwoods?

Line 177 you put a ; in 36,654 ha

Line 200-201 would be good to clarify timing by putting year(s) in parenthesis after pre-, during, post-

Line 221 why was it 10-16? were some removed due to location issues?

Line 222 has "(see below)" but doesn't refer to anything, is there supposed to be a Figure?

Tables with sub-sections should have that sub-section header in Bold or Italics to help with reading the table.

Figure 6b would look better with more contrasting colors.

Reviewer #2: Overall, this paper contains a lot of information and data and gets a bit confusing. The authors do not adequately set up the paper in a way that allows the reader to follow the results. However, I think with some tweaking, it could be a really great paper.

**********

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Reviewer #2: No

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PLoS One. 2022 May 4;17(5):e0265955. doi: 10.1371/journal.pone.0265955.r002

Author response to Decision Letter 0

28 Feb 2022

Detailed replies to comments by the Editor:

While this could be an important contribution to our approach to managing forests, I agree with the reviewers that the paper has a lot of promise but needs some additional strengthening and clarification. As Reviewer #2 points out, there is a lot of information in the Introduction, but the purpose is not as clear here as in the discussion. There are some very good recommendations that they make to improve clarity and flow in the Introduction.

Thank you for the encouraging set of comments. We agree with the Editor’s and Reviewer #2’s assessments of the Introduction section, and have reorganized some of these paragraphs in the revised manuscript. Two paragraphs that were not essential to developing the research questions and objectives have been edited; and 1) the paragraph that discussed “associative resistance” has been removed and integrated with the Discussion section, and 2) the paragraph on the productivity (NPP and NEP) of undisturbed oak-dominated, mixedwood, and pine-dominated stands has been condensed, with the extensive Table 1 moved to Supplemental S1 Table.

There are a number of places where the descriptions of the different sites surveyed is confusing. Please note some of the issues highlighted by both reviewers throughout the methods and the results.

We have condensed and moved the sub-section on “L. dispar and southern pine beetle” in the Materials and Methods section. We had intended this to summarize the impacts and spatial distributions of recent infestations in the region, but it was probably more confusing that helpful. We now only describe the spatial extent of the two recent infestations that we studied in Pinelands National Reserve of New Jersey in the appropriate subsection for forest census measurements.

Further, we have reversed the order of presentation of the FIA-type plots sampled pre-, during and post L. dispar infestations for clarity. We have also rewritten the description of the FIA-type plots that were sampled for southern pine beetle infested areas, highlighting that only untreated stands were used in our analyses here (please see comments below).

In particular, it is difficult to disentangle the labels for the pine sites that are infested or not by southern pine beetle and treated (managed?) or not. Or is the treatment status ignored for the purposes of your comparisons?

We first must apologize for a typographic error on the label for pine sites in Figure 4, which from left to right presents the relative basal areas of an oak-dominated stand pre- and post-infestation of L. dispar, a mixed stand at the beginning of the study, and pine-dominated stands post- and then pre-infestation of southern pine beetle, with the changes driven by infestations indicated with arrows. We had inadvertently switched the order of “post-“ and “pre-“ for the pine sites, and have corrected this in the revised version.

Although we measured forest structure in stands that were untreated and had been treated for southern pine beetle infestations (treatments included “cut and leave” and “cut and chip”; detailed in an annual report for the USFS Forest Health and Monitoring program in Clark et al. 2017 [24]), we have only used data from the 10 untreated, naturally occurring infestations here. We omitted data from the sites where suppression treatments were conducted because a major difference between untreated and treated stands is that pine saplings were cut or damaged in the treated stands, and this obscured the impacts of southern pine beetle and the shift to stands that more closely resemble mixedwood composition, as shown in Figure 4. We have rewritten our description of this in the Methods section, and now mention the treatment types explicitly in the Methods section.

Reviewer #2 has provided extensive line by line suggestions that should be carefully addressed.

Reviewer #2 has provided very helpful line by line comments, and we have attempted to address all of these. We feel following these suggestions has improved the clarity of the manuscript, and we appreciate the time Reviewer #2 spent on reviewing our previous draft.

Both the Editor and Reviewer #2 suggested that the Discussion section could be improved by first reducing the reiteration of the Results, and then expanding the broader context and complicating factors. In the original version of the manuscript, we intended to summarize the Results in the Discussion section first, noting that we are presenting a complex set of results that has integrated data from long-term forest census plots, FIA-type sampling, and long-term flux data from three sites that have been variously disturbed by insect infestations and prescribed fires. However, we agree with the Editor and Reviewer #2 and have removed the sub-sections headings and condensed the three sub-sections on impacts of L. dispar and southern pine beetle on forest composition, structure and productivity into three paragraphs. Further, we have expanded linkages to the conceptual model in Figure 1 by referencing this where appropriate, as per the comment below.

Figure 1 is very useful as a framework for the paper and it should be revisited more substantially in the discussion. For example, there is little discussion of differential impacts in uplands and lowlands but rather an emphasis on pine versus oak.

In the original version of the manuscript, we largely limited our discussion to upland systems, because all of our research on L. dispar and the three carbon flux towers are located in upland forest stands. While we believe that a more extensive treatment of lowland forests would be interesting, we felt this would be beyond the scope of our analyses. However, we have expanded our references to southern pine beetle effects in lowland systems throughout the revised manuscript. We also have expanded our discussion of fire return intervals and the fact that hardwood tree species in lowland forests, primarily red maple and black gum, are more fire intolerant than oaks in the revised Discussion section.

I agree with Reviewer #2 that there should be more discussion of fire, especially since fuels were measured (Line 277) for at least some sites. Does fire in these systems both prescribed and wild complicate conclusions about the effects of the infestation and resilience to disturbance?

We have expanded our discussion of fire, which does appear throughout the original version of the manuscript but was not highlighted particularly well.

Your question is an excellent one, and throughout the Discussion of the revised manuscript we have attempted to show that fire, especially the current patterns of extensive use of prescribed fire and wildfire suppression, would tend to reinforce the persistence of uneven age mixedwood stands because it promotes the regeneration of both oaks and pines by reducing understory competition and removing excess litter layer on the forest floor. An abundance of research has been conducted on the effects of low intensity fire in the Pinelands National Reserve and through the mid-Atlantic region that we now cite in the revised manuscript. In addition, we now explicitly cite how the effects of insect infestations and fire are consistent with a recently published conceptual model of mixedwood formation and persistence (Kern et al. 2021 [22]}.

It would be useful to discuss some of the implications of these findings and how they might apply in other contexts.

We have attempted to expand our discussion of the implications of our study throughout the revised Discussion section.

We have used better contrasting colors for Figures 5a and 5b, and 6a and 6b. We have also provided a description of what we intended the arrows to indicate in these two figures. The sentence stating, “Arrows indicate the directional changes in forest structure and composition following L. dispar infestations.” has been added to the legend below Figures 5 and 6.

This paper has a lot of promise and could be a good addition to the literature with some improvements.

Thank you again for supporting our manuscript

Detailed replies to comments by Reviewer #1:

Reviewer #1: Great work, just a few minor edits found.

Thank you.

Line 42 would be good to note that it is a decrease in sever wildfires. We have added the phrase “…and a decrease in the occurrence of severe wildfires [1-3].

Line 59-60 reword, for example: These "mixedwoods" are characterized by neither hardwood nor softwood exceeding 75% dominance. We have reworded this sentence to read, “These “mixedwoods” are characterized by neither hardwoods or softwoods exceeding approximately 75% dominance [e.g., 19-21].”

Line 87 says oak pine mixedwoods, but isn't it also making lowland deciduous pine mixedwoods?

We agree. We believe that Reviewer #1 intended to mean hardwood pine mixedwoods, and so we have added a phrase to mention this. We have also pointed this out explicitly throughout the Discussion section.

Line 177 you put a ; in 36,654 ha. The semi-colon is now a comma in 36,654 ha for the acreage of wildfires from 2004 to 2016.

Line 200-201 would be good to clarify timing by putting year(s) in parenthesis after pre-, during, post-. Thank you for pointing this out. We have added the years in parenthesis for each of these periods.

Line 221 why was it 10-16? were some removed due to location issues?

Yes, some plots fell on paved or sand roads, or in the case of the pine dominated site an unforested fire break. These were either not sampled or omitted from our analyses here. We now state this more clearly in the revised manuscript.

Line 222 has "(see below)" but doesn't refer to anything, is there supposed to be a Figure?

Tables with sub-sections should have that sub-section header in Bold or Italics to help with reading the table.

This statement referred to the flux towers, but we agree this was confusing. We now state “(described below)” to clarify.

Thanks, this is a helpful comment for table presentation. We have reformatted all of the tables with sub-section headers in bold.

Figure 6b would look better with more contrasting colors.

We have increased the contrast in Figures 5 and 6 by lightening the color of the bars indicating water use efficiency values for spring periods.

Detailed replies to comments by Reviewer #2:

This paper looks at successional changes in forests due to outbreaks of SPB and L. dispar.

It appears as though there are a couple different objectives, but those are never clearly stated in the manuscript, so it doesn’t really become clear what the paper is about until the discussion.

There is a lot going on in this paper and, at times, can get confusing to read. The objective in the abstract is to “understand ecological consequences of invasive insects on…..” but that’s pretty vague.

Also, you discuss southern pine beetle which is not an invasive insect under some/many definitions.

Overall, the paper leaves out some major details in terms of objectives and methods. I believe the authors did a massive amount of work on this and simply need to be more specific and intentional in their writing. My other main issue is with consistency in writing and explanations.

These are all very helpful comments. We do agree that this is a complex paper, and have reorganized and rewritten the Introduction section so that our objectives are easier for readers to follow. Following this, we have condensed some of the subheading topics throughout the Methods and Discussion section, for example the “L. dispar and southern pine beetle” section has been condensed into the sections on forest census measurements for L. dispar and southern pine beetle. We have also rewritten much of the Discussion section.

General comments:

Change all instances of “gypsy moth” to Lymantria dispar as the common name is being changed. We have replaced “gypsy moth” with “Lymantria dispar” at first use and “L. dispar” throughout the remainder of the manuscript.

The authors define phrases/words many times throughout the paper while still continuing to spell them out. At the same time, some things are stated but never defined. For instance, ecosystem water use efficiency is define at least 3 times while the authors don’t use the acronym WUE.

We apologize for the inconsistencies. We have defined all terms at first use, then use the correct acronyms throughout the revised manuscript.

Introduction:

The intro feels a bit out of order.

We agree, and as noted above, we have rewritten the Introduction section so that relevant material is covered in such detail, and the development of our questions and then objectives are clearer.

L43: Add commas around “…and intensity” Thank you, this is clearer now.

Remove L52-54.

We have substituted this introductory sentence, and now introduce the Pinelands National Reserve here, as Fig 1 (the conceptual model) addresses forests in the PNR.

L70-71: This sentence implies that the authors are going to discuss vulnerable species somewhere but this doesn’t come up throughout the paper.

We agree with Reviewer #2 that the use of the term “vulnerable” is vague and could be interpreted as meaning the conservation status of a species. Thus, here and on line 509 we have omitted the term “vulnerable” and have reworded to “susceptibility to insect infestations…”

L92: add “primary” to NPP definition OK, now corrected.

L114: This whole paragraph could be much earlier, I think.

We agree because this is a key objective and differs from the Abstract. We have rewritten much of the Introduction of the revised manuscript to address this and comments above.

L122: The authors have not defined NEE yet. We now define “net ecosystem exchange of CO2” before the first use of “NEE”

L137: Define and replace “course woody debris” with CWD

We now define course woody debris as CWD on first use and use CWD throughout the remainder of the revised manuscript. We also report values for the oak, mixed and pine stands, and refer to previously published values. Thanks, this was not clear in the last version.

L146: Remove “…as summarized in the conceptual model in Fig 1” and imply cite (Fig 1) at the end of the sentence. We have shortened this sentence as suggested, thanks.

L147-148: Sounds like this is what the authors are setting up to investigate but this is different than the “objective” in the abstract.

We have reworded the single objective listed in the Abstract so that it is a better description of actual objectives of our study. We have also revised much of the Introduction section.

L153-155: Define these as acronyms and then consistently use the acronyms throughout.

We have now defined all terms and acronyms at first use and used the correct acronyms throughout the manuscript. Again, we apologize for the inconsistencies.

L245: the authors use N for nitrogen here but in other places it is spelled out. Be consistent.

We have used the abbreviation “N” for nitrogen throughout the manuscript, except at first use where it is defined, and when it appears at the beginning of a sentence. Thank you, this is clearer now.

Methods:

There are SDs for precip but not temp. Don’t think SD are needed at all in site descriptions.

In the revised manuscript, we have followed a standard protocol on reporting means and SD’s for air temperature and precipitation, reporting averages over the last 30 years. We have added SD values to the temperature data presented in the text.

The sections on L. dispar and SPB all seems like intro material.

We considered moving these two paragraphs to the Introduction, but believe that they are best shortened and included as part of the Materials and methods section. However, we have removed the general information on susceptible species and only reported the years and extents of these infestations in southern New Jersey, under the descriptions of the forest census plots. This is important information to include somewhere, because it does indicate the extent to which L. dispar and SPB have impacted forests in the Pinelands National Reserve.

L222: If plots were set up in a 4 x 4 arrangement, how could there be 10-16 plots? Should always be 16….

This is true, but some plots were not sampled or not included in the analyses because one or more of the FIA subplots fell on sand roads or disturbed, non-forested areas. We apologize, this was not written very clearly in the previous version.

L226: Capitalize DBH and use throughout. Don’t need 1.27 m as DBH already has a definition.

We have changed all uses of “dbh” to “DBH”.

Height should have (m) after it to show how you measured. How was crown condition assigned? There is no description of crown condition anywhere.

We used the standard Forest Inventory and Analysis protocol for assigning crown classes for trees. These are emergent, dominant, co-dominant and suppressed. We do not present those data here, but would include it in the archived data.

L230: Why is recruitment in here twice? We apologize for this typographical error. This sentence now reads correctly.

L231: What is a clip plot?

These were destructively harvested plots measuring either 1.0 m2 or 0.5 m2 used to determine the aboveground biomass of understory vegetation and saplings. We have reworded this sentence in the revised manuscript.

L251-252: Did you extract data from these papers and then add them to your analyses?

These cited papers had additional [N] data for growing season foliage of the dominant and co-dominant species that we sampled. We compared our results to theirs, and their averaged values were reasonably close to ours.

L254: use [N] instead of spelling out “concentration” each time. Also, is content different than concentration? Again, these things are not well defined.

We now define N concentration as [N] following first use. We also define N content clearly, and use this term throughout the manuscript. Thank you for pointing this out, it is clearer now.

L267: Why use SD instead of SE? Also, this seems like a huge SD!

We used the SD value because that was reported by Aoki et al. in the cited publication.

These values came from tree ring counts of cored trees in stands sampled by Aoki et al., and their sampling occurred in the same stands we report here (their transects were co-located with the FIA type plots we installed and sampled in some stands).

L274: How was cover measured? This is not clear.

Cover was visually estimated from 4 cardinal directions out from the center point of each plot and then averaged for cover of understory vegetation and tree saplings. We have added “visually estimated“ in the text description. We would also include these values in the archived data.

L277: I’m confused as to what fuels have to do with anything. Fuels (like for fires?) have not been brought up at all yet.

We do mention wildfires and prescribed fires early in the Introduction, and effects of fire on species composition are also mentioned when describing the conceptual model in Figure 1 in the revised manuscript. We then return to the effects of fire in the Discussion, where we discuss the importance of fire in the regeneration of pines and oaks, and also describe how mixedwood forests may be less prone to severe wildfires compared to pine-dominated forests which have greater amounts of ladder and crown fuels. We have removed the mention of “available fuels” for pine trees and saplings here because we do not report these values in Table S2, which presents structural characteristics of areas infested by southern pine beetle and uninfested areas. Again, we would report these in the archived datasets.

L285: NEE should be defined earlier and should be the strict definition (i.e., net ecosystem exchange). We have defined NEE at first use in the revised manuscript.

L315: How did you assume it was dry? Were there certain environmental variables you checked beforehand? If so, then it’s not really an assumption per se.

We couldn’t really measure amounts of the water on leaf, needle and other canopy surfaces, so we thought it more accurate to use the term “assumption” here. We followed the protocol in previously published accounts of calculations for water use efficiency, WUEe., and used local half-hourly precipitation data to estimate dry periods.

L321: First time basal area is mentioned. Should be defined as BA with BA being used throughout the rest of the paper.

We have now defined “basal area” as BA at the first use, and now use the term BA throughout the remainder of the manuscript.

L332-334: This should be the first thing in the stats section

This is a good point. We have moved this sentence from the end of the paragraph to the beginning, because this was tested first before proceeding with the statistical analyses.

L323: Software used should be at the end (assuming you used that software for all analyses)

We did use SYSTAT 12 for all of the statistical analyses, and have moved this sentence to the end of the paragraph in the Statistics section.

L330: How many subsets? We have reorganized this sentence for clarity, and now report this value as “25 subsets”.

Results

L339-347: Results are very vague (i.e., “….and CWD were low at all three stands…”). What is “low”?

We have chosen to present the results for L. dispar chronologically, following their impact on

the three stand types because this highlights their differential impact on forest composition and structure. We now present CWD values throughout the Results section in the revised manuscript. Thank you, this was too vague in the previous version.

L372: “Stem increment”? We have substituted the term “BA” for “stem” to be consistent with the use of basal area, and for clarity.

L378-379: Are these values ± SD or SE? We have now defined these values above as SE.

L382: Again, results are vague with “very low” values and no means or other descriptors that let us know what “very low” actually means. We agree that this is vague and have added values to the text for coarse wood.

L400-407: These types of results are not given for L. dispar. This is more what I expect in a results section.

L426: What is “course wood mass”? Do you mean CWD? Yes, and we have changed this to CWD throughout the manuscript. This seems clearer now.

L430-435: Seems like an intro sentence to the discussion.

Discussion

L505-507: Can you generalize this to “insect infestations”? You only looked at one herbivore and one bark beetle…

This is true, and we have rewritten this sentence in the revised manuscript to indicate that we only investigated the effects of the two forest insects.

L509: This is the first time that “vulnerable” has come up again. By vulnerable, do you mean listed or simply susceptible to herbivory? Not really sure what vulnerable means in the context of this paper. We agree, and have omitted the term “vulnerable” throughout the text, because what we intend is “susceptible to herbivory”

Were there any areas that had BOTH SPB and L. dispar?

This is a good question. We observed stands with patches of oaks which likely had been previously impacted by L. dispar (as indicated by larger dead and damaged oak trees) adjacent to SPB stands that had been treated using cut and leave or cut and chip treatments. We sampled the SBP portions of these stands, but unfortunately because treatments had been conducted in the SBP portions of the stands, we did not use that information here because treatments also reduced the basal area and biomass of pine saplings. Perhaps in the next infestations?

L519: First time fire management has been mentioned. Is this related to “fuels” that came up earlier? Or unrelated? Fire really isn’t mentioned elsewhere.

We have attempted to highlight fire throughout the revised manuscript. We have also strengthened the discussion about use of prescribed fires and wildfires in regenerating pine and oaks, and fire-intolerance in some hardwoods. Thank you, this was a very good comment, and we attempted to improve the discussion of fire throughout the revised manuscript.

L533: Are you using N content as a proxy for “foliage quality”? If so, this isn’t defined.

Yes, and we now define this in paratheses in this sentence. Thanks for pointing this out, because it makes our intended use of the N content information clearer.

L599: Add end parentheses to the end of the sentence. OK, thank you.

L602-605: Wildfires are brought up here but, again, it’s not clear whether this was something actually looked at by the authors.

We now provide a number of citations throughout the manuscript that have either investigated the reduced occurrence of wildfires because of suppression activities or simulated the impacts of wildfires on forest composition, structure and ecosystem functioning. We also mention how the pine dominated stand had been burned in a wildfire in 1995, and subsequently in prescribed fires in 2008 and 2013, and that three prescribed fires have been conducted at the mixed pine-oak stand. Further, we have rewritten a paragraph in the Discussion section summarizing the documented the effects of prescribed fire in promoting the regeneration of oaks and pines in the PNR and throughout the mid-Atlantic region. This is important information for understanding the persistence of uneven age mixedwood stands that we did not treat very effectively in the previous version of the manuscript, and we appreciate this set of comments.

Tables and Figures:

Figure 1: Shouldn’t it be “southern pine beetle infestations”? You didn’t look at any other “pine beetles”.

Yes, this is true. We have substituted the term “Southern pine beetle infestations” in Figure 1. We have also changed “Gypsy moth” to “Lymantria dispar” for consistency.

Table 1: Add “(PNR)” to caption after you define Pinelands National Reserve as the authors use PNR in the table but do not define it. We have added “(PNR)” to the end of the last sentence of the caption for Table 1.

Table 2: I don’t know that a column with “figure” is necessary here.

We have left the references to the figures in the Tables because we feel that it will allow readers to find significance levels for statistical tests easily.

Figure 2 caption: This should stand alone. The authors don’t define “Inf” here.

We now define Pre, Inf, and Post in the caption for Figure 2, using the following definition:

“Pre” indicates before infestations, “Inf” indicates during infestation in 2007, and “Post” indicates a decade following infestations.

Table 3: Again, I don’t think a column for figure is necessary. And, since the authors simply report whether p-values are sig or not, this could be done with an * next to the T value instead and take up considerably less space. Table 5: Same comments as above.

Following the comment above, we left the references to the figures in each table. We feel that this will allow readers to find this information more easily.

Check references. Some are abbreviated while others are not. Some journals are abbreviated while others are not. Make sure you are consistent with journal requirements.

We have reformatted the references so that they are consistent with PLoS One instructions. We apologize for this error.

Editorial comments for PLoS One formatting

For Point #1 and the last comment by Reviewer #2, we have paid much closer attention to the proper formatting for PLoS One manuscripts, including the Tables and References.

We now provide information on how we obtained permission to sample sites for both sets of forest census plots. Nearly all lands were New Jersey state forests or wildlife management areas managed by the New Jersey Department of Environmental Protection.

3. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement.

For Point #3, we have removed the funding-related text from the Acknowledgement section in the revised manuscript. We would like our online funding statement to remain unchanged, and read: “Partial support for this project was provided by USDA Forest Service Forest Health and Monitoring Program grants NE-EM-F-13-01 to KC and NE-EM-B-12-01 to MA and AK.”

Thank you for changing this on the online submission form.

For Point #4, we would first like to clarify that some of the information in the manuscript has been previously published, and where we have used previously published information we have provided the appropriate citations. In summary, forest census data and carbon flux data from the three sites used to analyze the impacts of L. dispar previous to 2016 have been published in peer-reviewed publications. Forest census and carbon and hydrologic flux data for the “post” period in 2018 are unique to this manuscript. Similarly, summaries of the forest census data from the stands infested by southern pine beetle have been published in an annual report for the USFS Forest Health program, and in a meeting proceedings in 2020. These are also cited where used in this manuscript. Using this information is essential in setting the documenting the pre-infestation conditions for L. dispar and southern pine beetle, and for documenting some of their impacts through time. The overall conceptual model of mixedwood forest formation and persistence, and the analyses of forest productivity and hydrologic data in the context of mixedwoods is unique to this manuscript.

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PLoS One. doi: 10.1371/journal.pone.0265955.r003

Decision Letter 1

Karen Root

11 Mar 2022

Insect infestations and the persistence and functioning of oak-pine mixedwood forests in the Mid-Atlantic Region, USA.

PONE-D-21-34003R1

Dear Dr. Clark,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Additional Editor Comments (optional):

I appreciate the authors’ thoroughness and thoughtfulness in addressing the numerous comments and suggestions by the reviewers. The revisions have substantially improved the clarity and increased the flow while strengthening the main conclusions of the paper. With these revisions the paper is now suitable for publication and significantly advances our understanding of the complex interactions of insects and forests.

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0265955.r004

Acceptance letter

Karen Root

25 Apr 2022

PONE-D-21-34003R1

Insect infestations and the persistence and functioning of oak-pine mixedwood forests in the Mid-Atlantic region, USA.

Dear Dr. Clark:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. Productivity of undisturbed oak-dominated, mixed oak-pine, and pine-dominated forests in the mid-Atlantic region.

(PDF)

Click here for additional data file.^{(15.2KB, pdf)}

S2 Table. Structural characteristics of the canopy and understory in oak, mixed, and pine stands.

(PDF)

Click here for additional data file.^{(87.3KB, pdf)}

S3 Table. Structural characteristics of the canopy and understory in uninfested areas and areas infested by southern pine beetle.

Values are means ± 1 SE. Significance levels were tested using paired sample T-tests, and values indicated with different superscripts among areas are significantly different.

(PDF)

Click here for additional data file.^{(32.4KB, pdf)}

S4 Table. Meteorological sensors and eddy covariance equipment used to measure turbulence, net ecosystem exchange of CO₂ (NEE) and evapotranspiration (Et) at the oak, mixed and pine stands.

(PDF)

Click here for additional data file.^{(34.8KB, pdf)}

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Submitted filename: PONE-D-21-34003 review.docx

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Submitted filename: Response to Reviewers.docx

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Data Availability Statement

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PERMALINK

Insect infestations and the persistence and functioning of oak-pine mixedwood forests in the mid-Atlantic region, USA

Kenneth L Clark

Carissa Aoki

Matthew Ayres

John Kabrick

Michael R Gallagher

Roles

Abstract

Introduction

Fig 1. A conceptual model of forest composition in intermediate age oak- and pine- dominated stands in the New Jersey Pinelands National Reserve.

Materials and methods

Site description

L. dispar infestations and forest structure

Southern pine beetle infestations and forest structure

Leaf area and foliar nitrogen content

Ecosystem functioning of oak-, mixed and pine-dominated stands

Statistical analyses

Results

L. dispar infestations and forest structure

Fig 2. Effects of L. dispar infestations on forest composition and structure.

Table 1. Results of ANOVA and Tukey’s HSD analyses for structural characteristics of forests infested by L. dispar.

Table 2. Results of paired-sample T-tests for structural characteristics of stands infested by southern pine beetle.

Southern pine beetle infestations and forest structure

Fig 3. Effects of southern pine beetle on forest composition and structure.

Convergence of forest structure following insect infestations

Fig 4. Relative basal area of pine and hardwood trees and saplings.

Ecosystem functioning of oak-, mixed and pine-dominated stands

Table 3. Half-hourly net CO2 exchange (NEE) during spring (April 1 to May 15) and summer (June 1 to August 31) months at the oak, mixed and pine stands.

Table 4. Results of ANOVA analyses for ecosystem functioning of the oak, mixed and pine stands.

Fig 5. Productivity of the oak, mixed, and pine stands before L. dispar infestations in 2005 and following L. dispar infestations in 2018.

Table 5. Annual values of net ecosystem production (NEP), gross ecosystem production (GEP), precipitation, and evapotranspiration (Et) at the oak, mixed and pine stands.

Fig 6. Evapotranspiration and water use efficiency of oak, mixed, and pine stands before L. dispar infestations in 2005 and following L. dispar infestations in 2018.

Discussion

Conclusions

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Karen Root

Roles

Author response to Decision Letter 0

Decision Letter 1

Karen Root

Roles

Acceptance letter

Karen Root

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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Links to NCBI Databases

Table 3. Half-hourly net CO₂ exchange (NEE) during spring (April 1 to May 15) and summer (June 1 to August 31) months at the oak, mixed and pine stands.