an interdisciplinary approach to better assess global

copy The Author 2016 Published by Oxford University Press All rights reserved For Permissions please email journalspermissionsoupcom

Tree Physiology 36 421ndash427doi101093treephystpw005

An interdisciplinary approach to better assess global change impacts and drought vulnerability on forest dynamics

Marc D Abrams13 and Gregory J Nowacki2

1307 Forest Resources Building Department of Ecosystem Science and Management Penn State University University Park PA 16802 USA 2Eastern Regional Office USDA Forest Service 626 E Wisconsin Avenue Milwaukee WI 53202 USA 3Corresponding author (aglpsuedu)

Received November 4 2015 accepted January 9 2016 published online March 3 2016 handling Editor Danielle Way

Studies of tree physiology within and outside the USA have historically focused on the impacts of environmental factors such as light water and nutrients and more recently on the global change factors of increasing CO2 ozone and air and soil temperature on various tree species ( Kramer and Kozlowski 1979 Norby et al 1999 Hoeppner and Dukes 2012 Chung et al 2013) One thing that has plagued tree physiology research is the limited scope and breadth of most individual studies This normally involves measuring a few physiological parameters in response to a few treatments or environmental factors over a relatively short period of time in nonreplicated field or greenhouse settings with a small number of individuals and species although these issues are certainly not limited to tree physiology ( Hurlbert 1984) Nevertheless these studies have been invaluable in characterizing the ecophysiological attributes of many tree genera and species worldwide ( Abrams 1990 Burns and Honkala 1990 Prasad et al 2007ndashongoing Peters et al 2015) Fortunately past limitations have been greatly improved upon over the last quarter century by network site initiatives like FACE AmeriFlux and FluxNet allowing global scaling of physiological and leaf data from many sites in various forestvegetation types across several continents ( Schulze et al 1994 Kattge et al 2011 Norby and Zak 2011 Boden et al 2013 Ali et al 2015) In addition analysis and synthesis of the numerous small-scale studies and the upscaling of these data have led to huge advances of our understanding of plant form and function at the global level ( Reich et al 1997 Wright et al 2004) Large data syntheses have produced more accurate predictions of global primary productivity and future climates and the role of plant physiology and dynamic vegetation feedbacks in the climate response ( Kattge et al 2009 Philippon-Berthier et al 2010)

Significant accelerations of learning and scientific advances often take place when science of one field is combined with another ( Linkov et al 2014) In a recent study we attempted to expand the knowledge of climate change human impacts and land-use legacy by merging the fields of tree physiology and forest ecology ( Nowacki and Abrams 2015) This came forth from the realization that the distribution and dominance of each tree species corresponds to an ecophysiological expression and that long-term change in forest ecosystems is directly relatable to the underlying physiological attributes of component species This analysis can provide a more robust assessment of the role and impacts of the most important drivers of forest dynamics namely climate change and land-use history This method also elucidates ecophysiological changes at the forest type and forest biome level by capitalizing on extensive and long-term forest survey records The results of that study indicate (i) that vegeta-tion changes since European settlement in the eastern USA are caused to a greater extent by anthropogenic alteration of distur-bance regimes (eg clearing for agriculture wood harvesting introduction of nonnative pests and diseases and fire suppres-sion) than by climate change and (ii) that current vegetation reflects human influence and disturbance history more than the current environment These findings are a very important coun-terpoint to the idea of steady-state response to environment that is embedded of many current vegetation models including cli-mate envelope models and Dynamic Global Vegetation Models ( Cramer et al 2001 Iverson et al 2008) The findings also contradict the conclusion of some that climate is the major driver of post-European vegetation change in our study area (cf Pederson et al 2015) This includes evidence that increases and decreases in moisture in the recent and more distant past affected forest composition and biomass ( Gustafson and

Commentary

by guest on April 18 2016

httptreephysoxfordjournalsorgD

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Tree Physiology Volume 36 2016

Sturtevant 2013 Pederson et al 2014) However land-use alterations can mediate changes in forest composition that run counter to climate trends including the increase in some drought-tolerant trees during periods of increasing precipitation ( Abrams and Nowacki 2015) Indeed at present tree mortality trends across the eastern USA are more closely linked to stand characteristics (products of forest history and subsequent stand development sensu Oliver and Larson 1996) than climate vari-ables ( Dietze and Moorcroft 2011)

Our approach involves categorizing tree speciesgenera into temperature shade tolerance (intolerant intermediate and toler-ant) and pyrogenicity classes based on their known life history and physiological characteristics ( Nowacki and Abrams 2015) Temperature classes were established using actual temperature data from the Climate Change Tree Atlas ( Prasad et al 2007ndashongoing) Tree species were sorted by the average temperature within their ecological range (US distribution) and divided into four temperature classes (cold = 41ndash66 degC cool = 67ndash107 degC warm = 108ndash139 degC and hot = 140ndash198 degC) To assess level of disturbance tree genera were categorized by shade tolerance (intolerant intermediate and tolerant) and pyro-genicity (pyrophilic and pyrophobic Burns and Honkala 1990 Table 1) Tree survey data from pre-European settlement and present-day were tallied by temperature (cold cool warm and hot) shade tolerance (intolerant intermediate and tolerant) and pyrogenicity (pyrophilic and pyrophobic) and change per-centages were calculated for each class For the purpose of this article we expanded the ecophysiological classes to include drought tolerance and tree longevity (Table 1) Drought toler-ance classes were adapted from Peters et al (2015 Appendix

Supplemental Table S2) who used community assemblages of eastern US tree species and drought tolerance characteristics assessed from literature We chose three longevity classes short-lived (lt100 years) intermediate-lived (100ndash250 years) and long-lived (gt250 years) based on the range and distribution of the typical age of mortality for major eastern US tree species compiled by Loehle (1988) These classifications were applied to 190 tree-census datasets that compared pre-European settle-ment (original land survey data dating back to the 1600s) and current vegetation conditions in the eastern USA expressed as percent changes in the abundance (relative density or impor-tance value) of arboreal vegetation ( Nowacki and Abrams 2015) Importance value is typically calculated by combining or averaging speciesrsquo relative frequency density and dominance (basal area) Here we expanded this comparative analysis to five ecophysiological categories as a more robust set to relate compositional changes to known climate (temperature and drought) or disturbance (land-use) phenomena (Tables 1 and 2 Figure 1) The Palmer Drought Severity Index (PDSI Figure 1) a measurement of dryness based on precipitation and tempera-ture ( Alley 1984) was used to assess past drought conditions Zero depicts normal conditions whereas more negative num-bers indicate increasing drought and more positive numbers indicate increasing wetness (pluvials)

The Euro-American settlement period (asymp1500 onward) spans two major climatic periods the Little Ice Age (sim1400ndash1850) and the Anthropocene (after 1850) as well as two major anthro-pogenic disturbance periods the catastrophic disturbance era from 1600 through the 1930s (moving east to west across eastern North America) and the fire suppression era after 1940

422 Abrams and Nowacki

Table 1 Common eastern North American tree genera classified by temperature shade tolerance pyrogenicity drought tolerance and longevity (adapted and expanded upon from Nowacki and Abrams 2015)

Major tree genera Common name Temperature preference Shade tolerance Pyrogenicity Drought tolerance Longevity

Abies Balsam fir Cold Tolerant Pyrophobic Intolerant ShortAcer Sugar maple Cool Tolerant Pyrophobic Intolerant LongAcer Red maple Warm Tolerant Pyrophobic Moderate IntermediateBetula Birch Cold Intolerant Pyrophobic Moderate IntermediateCarya Hickory Warm Intermediate Pyrophilic Tolerant IntermediateCastanea Chestnut Cool Intermediate Pyrophilic Moderate IntermediateFagus Beech Warm Tolerant Pyrophobic Moderate LongFraxinus Ash Cool Intermediate Pyrophobic Moderate IntermediateJuniperus Red cedar Warm Intolerant Pyrophobic Tolerant LongLarix Tamaracklarch Cold Intolerant Pyrophobic Moderate IntermediatePicea Spruce Cold Tolerant Pyrophobic Intolerant IntermediateNorthern Pinus Northern pine Cold Intolerant Pyrophilic Tolerant LongSouthern Pinus Southern pine Hot Intolerant Pyrophilic Tolerant LongPopulus Aspen Cold Intolerant Pyrophilic Moderate ShortPrunus Cherry Warm Intermediate Pyrophobic Moderate IntermediateQuercus Oak Warm Intermediate Pyrophilic Tolerant LongThuja Cedar Cold Tolerant Pyrophobic Intolerant LongTilia Basswood Cool Tolerant Pyrophobic Moderate IntermediateTsuga Hemlock Cool Tolerant Pyrophobic Intolerant LongUlmus Elm Warm Intermediate Pyrophobic Moderate Intermediate



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Tree Physiology Online at httpwwwtreephysoxfordjournalsorg

(Figure 1) The transition from the Little Ice Age to the Anthro-pocene generally corresponds to progressively increasing annual temperatures and the lessening of drought based on the PDSI The catastrophic disturbance era includes the disease-based Native American pandemic that effectively started with Colum-busrsquo first voyage to the New World ( Ramenofsky 2003)

Global change impacts and drought vulnerability 423Ta

ble

2

Rela

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ean

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t to

pres

ent-da

y) in

the

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e (d

ensi

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port

ance

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ue in

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enth

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) of

arb

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with

in s

even

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or fo

rest

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(the

num

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ed in

par

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ing

chan

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in th

e ec

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orie

s of

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sha

de to

lera

nce

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ught

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e an

d lo

ngev

-ity

cla

sses

(ba

sed

on c

hang

es in

spe

cies

abu

ndan

ce)

in the

eas

tern

USA

(ad

apte

d fro

m a

nd e

xpan

ded

upon

Now

acki

and

Abr

ams

20

15

) T

he c

hang

es in

dro

ught

tol

eran

ce a

nd lo

ngev

ity w

ere

cond

ucte

d at

the

genu

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vel o

nly a

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in T

able

1

Regi

onVe

geta

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Tem

pera

ture

ΔTo

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Fire

ΔD

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ht Δ

Long

evity

Δ

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Maj

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Hot

Into

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ter

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eIn

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Inte

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lLo

ngIn

ter

Shor

t

Nor

thea

st o

ak-p

ine

(10)

Ace

r (20)

Bet

ula

(5)

Que

rcus

(minus1

5) C

asta

nea

(minus6)

Fag

us (minus3

)minus1

17

minus15

0minus1

minus16

18

minus24

25

11

7minus1

83

minus2minus1

Cen

tral

oak

-pin

e (3

3)

Acer

(7)

Juni

peru

s (3

)Q

uerc

us (minus1

7)

Pin

us

(minus4)

Cas

tane

a (minus

3)

minus23

minus1minus4

minus3minus1

08

minus22

18

minus19

minus20

minus15

31

Gre

at L

akes

oak

-pin

e (1

8)

Ace

r (9)

Car

ya (

3)

U

lmus

(3)

Que

rcus

(minus2

4)

1minus8

50

3minus1

51

0minus2

32

10

17

minus23

minus16

91

Nor

thea

st c

onife

r-no

rthe

rn

hard

woo

ds (

10)

Ace

r (19)

Pru

nus

(5)

Be

tula

Que

rcus

(4)

Fagu

s (minus

23

) T

suga

(minus

8)

Pic

ea (minus5

)0

9minus1

10

51

1minus1

86

minus8minus1

36

5minus8

33

Gre

at L

akes

con

ifer- n

orth

ern

hard

woo

ds (

29)

Ace

r (14)

Pop

ulus

(1

1)

Fra

xinu

s (3

)Ts

uga

(minus1

8)

Fag

us

(minus7

) B

etul

a (minus

6)

21

minus60

02

minus79

minus12

minus15

14

minus2minus1

3minus3

12

Gre

at L

akes

pin

e- no

rthe

rn

hard

woo

ds (

33)

Que

rcus

(13)

Pop

ulus

(

12)

Ace

r (12)

Pinu

s (minus

29

) T

suga

(minus

10

) F

agus

(minus4

)minus1

30

10

0minus1

69

4minus2

0minus6

19

minus16

minus16

minus11

5

Subb

orea

l con

ifers

(31)

Popu

lus

(15)

Fra

xinu

s (5

) A

cer (

5)

Pinu

s (minus

18

) L

arix

(minus

13

) B

etul

a (minus

3)

minus84

20

minus15

21

1minus1

minus15

9minus1

6minus1

0minus1

22

0

Figure 1 Climatic data and two major land-use periods for the eastern USA including temperature anomaly for the northeastern USA and PDSI from three sites north and three sites south of the tension line The PDSI data from the three northern locations were in Vermont Michigan and Wisconsin while the three southern sites were in Virginia south central Pennsylvania and Kentucky The temperature and PDSI data were obtained from Mann et al (2009) and the North American Drought Atlas (httpiridlldeocolumbiaeduSOURCESLDEOTRLNADA2004pdsi-atlashtml) respectively Temperature data were extracted from the paleoclimate dataset reconstructed by Mann et al (2009) covering grid cells in the eastern USA



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and largely ran its course through eastern tribes by 1800 It also co-occurred with active westward migration of Native American populations Emblematic of the catastrophic disturbance era was the lsquoGreat Cutoverrsquo which arose slowly along the Atlantic Sea-board in the mid-1600s to great expansion across the Midwest and Deep South during the 1700s and1800s before terminat-ing along the western margins of the Eastern Deciduous Forest and within the most rugged parts of the Appalachians (West Virginia Lewis 1998) in the early 1900s Catastrophic wildfires that burned through abundant down and dry slash also charac-terized this period especially during its later phase (1800sndashearly 1900s Guthrie 1936) Chestnut blight radiated outward from its origins in New York City in the early 1900s effectively wiping out this genus from eastern forests by the 1940s ( Anagnostakis 1987) Aggressive fire suppression throughout the eastern USA (Smokey Bear Era) started in the 1930s and continues to the present day ( Abrams 2010)

From the time of European settlement to the present the eastern USA experienced major compositional changes includ-ing (i) a large overall decline in conifers (Pinus Tsuga and Larix) Fagus and Castanea (ii) expansions of disturbance-oriented Populus and Quercus species in former conifer-northern hard-woods or subboreal forests and (iii) an ubiquitous increase in fire-sensitive shade-tolerant Acer across all regions (Table 2) When converted to and tracked by ecophysiological attributes forest systems with similar initial compositions and stand dynam-ics had a similar response to European alterations of disturbance regimes In oak-pine forests where the Quercus-to-Acer transi-tion was most prominent there was a distinct shift toward greater shade tolerance and less fire and drought tolerance (Table 2) In Northeast oak-pine forests cool-adapted Acer sac-charum Marsh was the principal benefactor whereas in the cen-tral oak-pine forests it was warm-adapted Acer rubrum L the latter representing a neutral temperature change from warm-adapted Quercus In rich mesic conifer-northern hardwood for-ests (Northeast and Great Lakes) the loss of Fagus and Tsuga had overwhelming effects on these systemsrsquo collective ecophys-iology with recorded losses of warm adaptation (Fagus) shade tolerance pyrophobicity and drought intolerance Here the replacement of warm-adapted genera by cold- and cool-adapted genera during a period of global warming is noteworthy The shift from cold shade-intolerant Pinus to warm shade-intermediate Quercus and shade-tolerant A rubrum in the drier systems of the Upper Midwest (Great Lakes pine-northern hardwoods and sub-boreal conifers) largely drove ecophysiological changes Here the replacement of long-lived Pinus by short-lived Populus pri-marily explains the reduction of tree longevity

It appears that change in anthropogenic disturbance regimes is a major driver of post-European forest dynamics in the study region For example significant increases in the cold-adapted disturbance-oriented clonal Populus species in conifer-northern hardwoods and subboreal forests runs counter to Anthropocene

warming but is highly consistent with the wholesale cutting and burning of northern hardwood forests ( Graham et al 1963 Cleland et al 2001) The loss of cold-adapted conifers in north-ern forests is consistent with the warming trend but we believe is better explained by their inability to sprout after clearcutting and burning The ubiquitous increase in Acer in all forest sys-tems whether cool-based (A saccharum) or warm-based (A rubrum) can be directly linked to changes in anthropogenic disturbance regimes that have produced inconsistencies when compared with the climate record In oak-pine systems the increase in Acer is generally attributed to fire suppression par-ticularly in the case of the widely distributed A rubrum ( Abrams 1992 1998 Nowacki and Abrams 2008) The increase in warm-adapted Quercus and A rubrum in the Great Lakes pine-northern hardwoods is consistent with warming but is more likely a response to the mass cutting of pines (prime timber tree) subsequent consumption of its fire-vulnerable regenera-tion and release of hardwood understoriesmdashphenomen a well documented in the historical literature ( Elliott 1953 Whitney 1987 Nowacki et al 1990) The loss of warm-adapted pyro-phobic Fagus in conifer-northern hardwood systems is also inconsistent with the warming trend being attributed to beech bark disease and its negative response to clearcutting and burn-ing of eastern forests ( Nowacki and Abrams 2015)

Across all oak-pine forest regions the overall reduction of drought- and fire-adapted trees and the corresponding increase in mesophytic species particularly Acer are consistent with the lessening of drought after the 1930s (increasing PDSI trends Figure 1 Table 2 McEwan et al 2011) However we believe that this is better explained by the lack of fire or other interven-ing anthropogenic factors For example the loss of mesophytic Tsuga is not consistent with the lessening of drought Moreover the twentieth-century increases in several important drought-tolerant or moderately drought-tolerant trees (eg Populus A rubrum Juniper (and Quercus in Great Lakes pine-northern hardwoods)) run counter to the PDSI trend The loss of Casta-nea early in the twentieth century is due to the chestnut blight and is unrelated to changes in climate The decreases in longev-ity for most eastern forest types are due to the loss of long-lived Quercus Pinus Fagus and Tsuga species collectively the major decreasers in eastern forests The increase in shade tolerance in most forest systems was due to the wide-ranging decrease in Quercus and Pinus and increase in Acer except for mesic conifer-northern hardwood forests that were previously dominated by Fagus and Tsuga It is important to note that most of these changes are unique to the clearcutting and catastrophic wildfire and fire suppression eras and did not occur during previous cen-turies with lessening drought events based on paleoecological studies (Figure 1 reviewed in Abrams 2002)

Converting forest compositional change to ecophysiological derivatives to better understand and interpret forest dynamics is in its infancy As with any embryonic field it may be met with




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skepticism which is part of any initial scientific endeavor Indeed the relative simplicity of our method to analyze and interpret complex arrays of ecological factors that affect eco-systems makes it particularly vulnerable to incertitude To wit our interpretation that land-use change specifically fire sup-pression principally drove succession to shade-tolerant fire-sensitive mesophytes in formerly pyrogenic oak-dominated ecosystems ( Nowacki and Abrams 2015) was questioned as this compositional conversion parallels increasing moisture over the last several centuries ( Pederson et al 2015) But we main-tain steadfast to our interpretation due to convergence of mul-tiple independent pointers especially the alignment of the historical record of European land disturbance (including post-1930s decline in fire occurrence and size) with tree distribu-tion-based trends in temperature (decreasing rather than increasing) shade tolerance (succession from fire-maintained sub-climax toward climatic climax conditions) and pyrogenicity (decrease in pyrophiles) ( Abrams and Nowacki 2015) Higher temperatures often negate increases in precipitation (through increased evapotranspiration) as expressed in Brzostek et al (2014) so the latter does not necessarily explain the shift toward shade-tolerant mesophytes per se Moreover the abruptness of the oak-to-maple transition is not consistent with ever-increasing moisture trend spanning centuries ( Pederson et al 2015) but is consistent with the universal and rather instantaneous removal of fire from the eastern landscape Now increased moisture deer herbivory etc may have facilitated some of this transition ( McEwan et al 2011) but were more ancillary in nature than primary drivers

The immediacy and extent by which European disturbances affected ecosystems (relative to slow climatic changes over time) cannot be underscored enough vastly overriding climatic changes that have occurred over the same period The fact that the rates of vegetation change assigned to European activities are roughly a magnitude above those of the past millennia is particularly telling In the Upper Great Lakes Region the average amount of vegetation change recorded in pollen was 24 times greater during the last 150 years than the preceding 850 years ( Cole et al 1998) Here post-European vegetation changes were best assigned to human disturbance as changes in climate were comparatively small ( Webb 1973) In the Central Hard-woods Region Cole and Taylor (1995) report that recent (last 150 years) rates of vegetation change are at least an order of magnitude higher than in the prior 4000 years This extreme rate of change is largely attributed to fire exclusion possibly enhanced by other factors including human-driven increases of nitrogen deposition ( Vitousek et al 1997) Only the rapid and profound changes in human land use (specifically fire suppres-sion) can explain the huge oak-to-maple compositional shift such as the 4000+ percent increase in maplendashbeech forests from 1962 to 1985 in Illinois ( Iverson et al 1989 Fralish 2004)

Disentangling disturbance versus climate change effects on vegetation and assigning importance is problematic for a num-ber of reasons including spatiotemporal differences (eg dis-turbance can have immediate dramatic and long-term impacts whereas climate changes play out more subtly over longer tim-escales due to ecological inertia and time lags Pielou 1991 Abrams and Nowacki 2015 Wu et al 2015) In any case we are encouraged by recent research that acknowledges the importance of disturbance regimes and other related factors on vegetation dynamics thus giving them fair and equatable treat-ment relative to climate (Danneyrolles et al 2016) For instance a mega-analysis of gt1600 plots from across western Canada found that internal stand dynamics and competition were the primary drivers of tree demographics compared with external climatic factors ( Zhang et al 2015) In the absence of distur-bance since the Great Cutover cold-adapted red spruce is moving downslope and reclaiming its former distribution in the face of global warming in New England ( Foster and DrsquoAmato 2015) This phenomenon has been found throughout the entirety of red sprucersquos range ( Nowacki et al 2010) and is consistent with human land use being the primary factor driving forest dynamics for this species Multiple peaks in mineral sediments suggestive of hydroclimate variability do not consistently correspond to shifts in Fagus grandifolia abundances in the Great Lakes Region during the Holocene ( Wang et al 2015) Flatley et al (2015) demon-strated that fire exclusion and not climate is driving changes within mixed oak stands in the southern Appalachian Mountains The conclusions of this site-specific study pair nicely with our broadscale research ( Nowacki and Abrams 2015) whereby dis-turbances (andor the absence of formerly important disturbance) may actually possess long-term lsquotrumping powerrsquo over climate-driven changes with regard to vegetation expression This does not discount the fact that climate is having some important impacts on forests and other vegetation types worldwide as stud-ies of drought- and heat-induced tree mortality indicate otherwise including the eastern USA ( Pederson et al 2014 Allen et al 2015) Whether this will have a profound effect on future forest dynamics remains to be seen and will greatly depend on forth-coming drought severity and duration and changes in temperature and disturbance regimes ( Gustafson and Sturtevant 2013 Peters et al 2015) However the results of this and other studies indi-cate that the loss of drought-tolerant Quercus Pinus and Carya and the increase in mesophytic trees in a process known as mesophication ( Nowacki and Abrams 2008) are increasing the drought vulnerability of eastern US forests ( Hart et al 2014 Frelich et al 2015) This vulnerability may exacerbate tree mortal-ity and water-stress declines in growth specifically for water-demanding mesophytic species ( Brzostek et al 2014)

The worldrsquos climate is warming in ways not seen for several thousand years ( Alley 2000) The post-1850 increases in greenhouse gases and abrupt global warming are clearly affect-ing tree physiology and many other ecosystem processes and

Global change impacts and drought vulnerability 425



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provide vast research opportunities for tree physiologists and other environmental scientists ( Norby et al 1999 Karnosky et al 2007 Way and Oren 2010) These topics are now the dominant focus worldwide but have the potential in our opinion to minimize the role of other important factors particularly among those who are intent on finding climate signals ( Pederson et al 2015) Human populations and their role as a disturbing agent in ecosystems have also changed dramatically along with the recent changes in climate ( Ellis 2015) Comprehending past and future impacts of climate change on vegetation requires a more complete understanding of the humanndashclimatendashvegetation dynamic Vegetation models should include changes in distur-bance regimes and not rely solely on climate change or bio-geochemical factors New research endeavors that combine multidisciplinary data as outlined in this article in other loca-tions and with other disciplines should greatly increase our understanding of global change impacts as we move further into the twenty-first century

Acknowledgments

We wish to thank Janet Ellsworth for help with data summary analysis and constructing figures and tables and CM Krause for an editorial review of the paper

References

Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America Tree Physiol 7227ndash238

Abrams MD (1992) Fire and the development of oak forests BioScience 42346ndash353

Abrams MD (1998) The red maple paradox BioScience 48355ndash364 Abrams MD (2002) The postglacial history of oak forests in eastern

North America In McShea WJ Healy WM (eds) The ecology and man-agement of oaks for wildlife John Hopkins University Press Baltimore MD pp 34ndash45

Abrams MD (2010) Native Americans Smoky Bear and the rise and fall of eastern oak forests Penn State Environ Law Rev 18141ndash154

Abrams MD Nowacki GJ (2015) Large-scale catastrophic disturbance regimes can mask climate change impacts on vegetationmdasha reply to Pederson et al (2014) Glob Change Biol doi101111gcb12828

Ali AA Xu C Rogers A et al (2015) Global-scale environmental control of plant photosynthetic capacity Ecol Appl 252349ndash2365

Allen CD Breshears DD McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene Ecosphere 61ndash55

Alley RB (2000) The two-mile time machine ice cores abrupt climate change and our future Princeton University Press Princeton NJ p 229

Alley W (1984) The Palmer Drought Severity Index limitations and assumptions J Clim Appl Meteorol 231100ndash1109

Anagnostakis SL (1987) Chestnut blight the classical problem of an introduced pathogen Mycologia 7923ndash37

Boden TA Krassovski M Yang B (2013) The AmeriFlux data activity and data system an evolving collection of data management techniques tools products and services Geosci Instrum Method Data Syst 2165ndash176

Brzostek ER Dragoni D Schmid HP Rahman AF Sims D Wayson CA Johnson DJ Phillips RP (2014) Chronic water stress reduces tree

growth and the carbon sink of deciduous hardwood forests Glob Change Biol 202531ndash2539

Burns RM Honkala BH (1990) Silvics of North America volumes 1 and 2 hardwoods and conifers Agriculture Handbook 654 Department of Agriculture Forest Service US Government Printing Office Wash-ington DC 877 p

Chung HH Muraoka M Nakamura N Han S Muller O Son Y (2013) Experimental warming studies on tree species and forest ecosystems a literature review J Plant Res 126447ndash460

Cleland DT Leefers LA Dickmann DI (2001) Ecology and management of aspen a Lake States perspective In Proceedings sustaining aspen in western landscapes RMRSP-18 US Department of Agriculture Forest Service Rocky Mountain Research Station Fort Collins CO pp 81ndash99

Cole KL Taylor RS (1995) Past and current trends of change in a dune prairieoak savanna reconstructed through a multiple-scale history J Veg Sci 6399ndash410

Cole KL Davis MB Stearns F Guntenspergen G Walker K (1998) His-torical landcover changes in the Great Lakes region In Sisk TD (ed) Perspectives on the land-use history of North America a context for understanding our changing environment Biological Science Report USGSBRDBSR-1998-0003 US Geological Survey Biological Resources Division Springfield VA pp 43ndash50 104 pp

Cramer W Bondeau A Woodward FI et al (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change results from six dynamic global vegetation models Glob Change Biol 7357ndash373

Danneyrolles V Arseneault D Bergeron Y (2016) Pre-industrial land-scape composition patterns and post-industrial changes at the tem-peratendashboreal forest interface in western Quebec Canada J Veg Sci doi101111jvs12373

Dietze MC Moorcroft PR (2011) Tree mortality in the eastern and cen-tral United States patterns and drivers Glob Change Biol 173312ndash3326

Elliott JC (1953) Composition of upland second growth hardwood stands in the tension zone of Michigan as affected by soils and man Ecol Monogr 23271ndash288

Ellis EC (2015) Ecology in an anthropogenic biosphere Ecol Monogr 85287ndash331

Flatley WT Lafon CW Grissino-Mayer HD LaForest LB (2015) Changing fire regimes and old-growth forest succession along a topographic gradient in the Great Smoky Mountains For Ecol Manag 35096ndash106

Foster JR DrsquoAmato AW (2015) Montane forest ecotones moved downslope in northeastern USA in spite of warming between 1984 and 2011 Glob Change Biol 214497ndash4507

Fralish JS (2004) The keystone role of oak and hickory in the Central Hardwood Forest In Spetich MA (ed) Upland oak ecology sympo-sium history current conditions and sustainability USDA Forest Ser-vice General Technical Report SRS-73 US Department of Agriculture Forest Service Southern Research Station Asheville NC pp 78ndash87

Frelich LE Reich PB Peterson DW (2015) Fire in upper Midwestern oak forest ecosystems an oak forest restoration and management hand-book USDA Forest Service General Technical Report PNW-GTR-914 US Department of Agriculture Forest Service Pacific Northwest Research Station Portland OR 64 p

Graham SA Harrison RP Jr Westell CE Jr (1963) Aspen Phoenix trees of the Great Lakes Region University of Michigan Press Ann Arbor MI pp 272

Gustafson EJ Sturtevant BR (2013) Modeling forest mortality caused by drought stress implications for climate change Ecosystems 1660ndash74

Guthrie JD (1936) Great forest fires of America USDA Forest Service Government Printing Office Washington DC 10 p

Hart JL Oswalt CM Turberville CM (2014) Population dynamics of sugar maple through the southern portion of its range implications for range migration Botany 92563ndash569




ownloaded from


Hoeppner SS Dukes JS (2012) Interactive responses of old-field plant growth and composition to warming and precipitation Glob Change Biol 181754ndash1768

Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments Ecol Monogr 54187ndash211

Iverson LR Oliver RL Tucker DP et al (1989) The forest resources of Illinois an atlas and analysis of spatial and temporal trends Erigenia 134ndash19

Iverson LR Prasad AM Matthews SN Peters M (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios For Ecol Manag 254390ndash406

Karnosky DF Skelly JM Percy KE Chappelka AH (2007) Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on US forests Environ Pollut 147489ndash506

Kattge J Knorr W Raddatz T Wirth C (2009) Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models Glob Change Biol 15976ndash991

Kattge J Diacuteaz S Lavorel S et al (2011) TRYmdasha global database of plant traits Glob Change Biol 172905ndash2935

Kramer PJ Kozlowski TT (1979) Physiology of woody plants Academic Press New York NY 811 p

Lewis RL (1998) Transforming the Appalachian countryside railroads deforestation and social change in West Virginia 1880ndash1920 The University of North Carolina Press Chapel Hill NC p 348

Linkov I Wood M Bates M (2014) Scientific convergence dealing with the elephant in the room Environ Sci Technol 4810539ndash10540

Loehle C (1988) Tree life history strategies the role of defenses Can J For Res 18209ndash222

Mann ME Zhang Z Rutherford S Bradley RS Hughes MK Shindell D Ammann C Faluvegi G Ni F (2009) Global signatures and dynamical origins of the Little Ice Age and Medieval Climate anomaly Science 3261256ndash1260

McEwan RW Dyer JM Pederson N (2011) Multiple interacting ecosystem drivers toward an encompassing hypothesis of oak forest dynamics across eastern North America Ecography 34244ndash256

Norby RJ Zak DR (2011) Ecological lessons from free-air CO2 enrich-ment (FACE) experiments Annu Rev Ecol Evol Syst 42181ndash203

Norby RJ Wullschleger SD Gunderson CA Johnson DW Ceulemans R (1999) Tree responses to rising CO2 in field experiments implications for the future forest Plant Cell Environ 22683ndash714

Nowacki GJ Abrams MD (2008) The demise of fire and ldquomesophicationrdquo of forests in the eastern United States BioScience 58123ndash138

Nowacki GJ Abrams MD (2015) Is climate an important driver of post-European vegetation change in the eastern United States Glob Change Biol 21314ndash334

Nowacki GJ Abrams MD Lorimer CG (1990) Composition structure and historical development of northern red oak stands along an edaphic gradient in north-central Wisconsin For Sci 36276ndash292

Nowacki G Carr R Van Dyck M (2010) The current status of red spruce in the eastern United States distribution population trends and environ-mental drivers In Proceedings of the conference on the ecology and management of high-elevation forests in the central and southern Appa-lachian Mountains USDA Forest Service General Technical Report NRS-P-64 Northern Research Station Newtown Square PA pp 140ndash162

Oliver CD Larson BC (1996) Forest stand dynamics update edition John Wiley amp Sons Inc New York NY 467 p

Pederson N Dyer JM McEwan RW Hessl AE Mock CJ Orwig DA Rieder HE Cook BI (2014) The legacy of episodic climatic events in shaping temperate broadleaf forests Ecol Monogr 84599ndash620

Pederson N DrsquoAmato AW Dyer JM et al (2015) Climate remains an important driver of post-European vegetation change in the eastern United States Glob Change Biol 212105ndash2110

Peters MP Iverson LR Matthews SN (2015) Long-term droughtiness and drought tolerance of eastern US forests over five decades For Ecol Manag 34556ndash64

Philippon-Berthier G Vavrus SJ Kutzbach JE Ruddiman WF (2010) Role of plant physiology and dynamic vegetation feedbacks in the climate response to low GHG concentrations typical of late stages of previous interglacials Geophys Res Lett 37L08705

Pielou EC (1991) After the last Ice Age the return of life to glaciated North America University of Chicago Press Chicago IL 366 p

Prasad AM Iverson LR Matthews S Peters M (2007ndashongoing) A Cli-mate Change Atlas for 134 forest tree species of the Eastern United States (database) Northern Research Station USDA Forest Service Delaware OH httpwwwnrsfsfedusatlastree (3 January 2014 date last accessed)

Ramenofsky A (2003) Native American disease history past present and future directions World Archaeol 35241ndash257

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Schulze E Kelliher FM Koumlrner C Lloyd J Leuning R (1994) Relation-ships among maximum stomatal conductance ecosystem surface con-ductance carbon assimilation rate and plant nitrogen nutrition a global ecology scaling exercise Annu Rev Ecol Syst 25629ndash662

Vitousek PM Aber JD Howarth RW Likens GE Matson PA Schindler DW Schlesinger WH Tilman DG (1997) Human alteration of the global nitrogen cycle sources and consequences Ecol Appl 7737ndash750

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Zhang J Huang S He F (2015) Half-century evidence from western Canada shows forest dynamics are primarily driven by competition followed by climate Proc Natl Acad Sci USA 1124009ndash4014




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Sturtevant 2013 Pederson et al 2014) However land-use alterations can mediate changes in forest composition that run counter to climate trends including the increase in some drought-tolerant trees during periods of increasing precipitation ( Abrams and Nowacki 2015) Indeed at present tree mortality trends across the eastern USA are more closely linked to stand characteristics (products of forest history and subsequent stand development sensu Oliver and Larson 1996) than climate vari-ables ( Dietze and Moorcroft 2011)

Our approach involves categorizing tree speciesgenera into temperature shade tolerance (intolerant intermediate and toler-ant) and pyrogenicity classes based on their known life history and physiological characteristics ( Nowacki and Abrams 2015) Temperature classes were established using actual temperature data from the Climate Change Tree Atlas ( Prasad et al 2007ndashongoing) Tree species were sorted by the average temperature within their ecological range (US distribution) and divided into four temperature classes (cold = 41ndash66 degC cool = 67ndash107 degC warm = 108ndash139 degC and hot = 140ndash198 degC) To assess level of disturbance tree genera were categorized by shade tolerance (intolerant intermediate and tolerant) and pyro-genicity (pyrophilic and pyrophobic Burns and Honkala 1990 Table 1) Tree survey data from pre-European settlement and present-day were tallied by temperature (cold cool warm and hot) shade tolerance (intolerant intermediate and tolerant) and pyrogenicity (pyrophilic and pyrophobic) and change per-centages were calculated for each class For the purpose of this article we expanded the ecophysiological classes to include drought tolerance and tree longevity (Table 1) Drought toler-ance classes were adapted from Peters et al (2015 Appendix

Supplemental Table S2) who used community assemblages of eastern US tree species and drought tolerance characteristics assessed from literature We chose three longevity classes short-lived (lt100 years) intermediate-lived (100ndash250 years) and long-lived (gt250 years) based on the range and distribution of the typical age of mortality for major eastern US tree species compiled by Loehle (1988) These classifications were applied to 190 tree-census datasets that compared pre-European settle-ment (original land survey data dating back to the 1600s) and current vegetation conditions in the eastern USA expressed as percent changes in the abundance (relative density or impor-tance value) of arboreal vegetation ( Nowacki and Abrams 2015) Importance value is typically calculated by combining or averaging speciesrsquo relative frequency density and dominance (basal area) Here we expanded this comparative analysis to five ecophysiological categories as a more robust set to relate compositional changes to known climate (temperature and drought) or disturbance (land-use) phenomena (Tables 1 and 2 Figure 1) The Palmer Drought Severity Index (PDSI Figure 1) a measurement of dryness based on precipitation and tempera-ture ( Alley 1984) was used to assess past drought conditions Zero depicts normal conditions whereas more negative num-bers indicate increasing drought and more positive numbers indicate increasing wetness (pluvials)

The Euro-American settlement period (asymp1500 onward) spans two major climatic periods the Little Ice Age (sim1400ndash1850) and the Anthropocene (after 1850) as well as two major anthro-pogenic disturbance periods the catastrophic disturbance era from 1600 through the 1930s (moving east to west across eastern North America) and the fire suppression era after 1940


Table 1 Common eastern North American tree genera classified by temperature shade tolerance pyrogenicity drought tolerance and longevity (adapted and expanded upon from Nowacki and Abrams 2015)

Major tree genera Common name Temperature preference Shade tolerance Pyrogenicity Drought tolerance Longevity

Abies Balsam fir Cold Tolerant Pyrophobic Intolerant ShortAcer Sugar maple Cool Tolerant Pyrophobic Intolerant LongAcer Red maple Warm Tolerant Pyrophobic Moderate IntermediateBetula Birch Cold Intolerant Pyrophobic Moderate IntermediateCarya Hickory Warm Intermediate Pyrophilic Tolerant IntermediateCastanea Chestnut Cool Intermediate Pyrophilic Moderate IntermediateFagus Beech Warm Tolerant Pyrophobic Moderate LongFraxinus Ash Cool Intermediate Pyrophobic Moderate IntermediateJuniperus Red cedar Warm Intolerant Pyrophobic Tolerant LongLarix Tamaracklarch Cold Intolerant Pyrophobic Moderate IntermediatePicea Spruce Cold Tolerant Pyrophobic Intolerant IntermediateNorthern Pinus Northern pine Cold Intolerant Pyrophilic Tolerant LongSouthern Pinus Southern pine Hot Intolerant Pyrophilic Tolerant LongPopulus Aspen Cold Intolerant Pyrophilic Moderate ShortPrunus Cherry Warm Intermediate Pyrophobic Moderate IntermediateQuercus Oak Warm Intermediate Pyrophilic Tolerant LongThuja Cedar Cold Tolerant Pyrophobic Intolerant LongTilia Basswood Cool Tolerant Pyrophobic Moderate IntermediateTsuga Hemlock Cool Tolerant Pyrophobic Intolerant LongUlmus Elm Warm Intermediate Pyrophobic Moderate Intermediate



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ture

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phile

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(minus6)

Fag

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17

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minus16

18

minus24

25

11

7minus1

83

minus2minus1

Cen

tral

oak

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e (3

3)

Acer

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7)

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(minus4)

Cas

tane

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minus23

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minus3minus1

08

minus22

18

minus19

minus20

minus15

31

Gre

at L

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oak

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8)

Ace

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Car

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3)

U

lmus

(3)

Que

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4)

1minus8

50

3minus1

51

0minus2

32

10

17

minus23

minus16

91

Nor

thea

st c

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r-no

rthe

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hard

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10)

Ace

r (19)

Pru

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Be

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suga

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Pic

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86

minus8minus1

36

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33

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Pop

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Fra

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uga

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Fag

us

(minus7

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etul

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21

minus60

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minus79

minus12

minus15

14

minus2minus1

3minus3

12

Gre

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pin

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rthe

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hard

woo

ds (

33)

Que

rcus

(13)

Pop

ulus

(

12)

Ace

r (12)

Pinu

s (minus

29

) T

suga

(minus

10

) F

agus

(minus4

)minus1

30

10

0minus1

69

4minus2

0minus6

19

minus16

minus16

minus11

5

Subb

orea

l con

ifers

(31)

Popu

lus

(15)

Fra

xinu

s (5

) A

cer (

5)

Pinu

s (minus

18

) L

arix

(minus

13

) B

etul

a (minus

3)

minus84

20

minus15

21

1minus1

minus15

9minus1

6minus1

0minus1

22

0




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ble

2

Rela

tive

chan

ges

(fro

m p

re-E

urop

ean

settl

emen

t to

pres

ent-da

y) in

the

abun

danc

e (d

ensi

ty o

r im

port

ance

val

ue in

par

enth

eses

) of

arb

orea

l veg

etat

ion

with

in s

even

maj

or fo

rest

regi

ons

(the

num

ber of

dat

aset

s an

alyz

ed in

par

enth

eses

) an

d th

e co

rres

pond

ing

chan

ges

in th

e ec

ophy

siol

ogic

al c

ateg

orie

s of

tem

pera

ture

sha

de to

lera

nce

pyr

ogen

icity

dro

ught

tole

ranc

e an

d lo

ngev

-ity

cla

sses

(ba

sed

on c

hang

es in

spe

cies

abu

ndan

ce)

in the

eas

tern

USA

(ad

apte

d fro

m a

nd e

xpan

ded

upon

Now

acki

and

Abr

ams

20

15

) T

he c

hang

es in

dro

ught

tol

eran

ce a

nd lo

ngev

ity w

ere

cond

ucte

d at

the

genu

s le

vel o

nly a

s lis

ted

in T

able

1

Regi

onVe

geta

tion Δ

Tem

pera

ture

ΔTo

lera

nce Δ

Fire

ΔD

roug

ht Δ

Long

evity

Δ

Maj

or in

crea

sers

Maj

or d

ecre

aser

sC

old

Coo

lW

arm

Hot

Into

lIn

ter

Tol

Pyro

phile

Pyro

phob

eIn

tol

Inte

rTo

lLo

ngIn

ter

Shor

t

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thea

st o

ak-p

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(10)

Ace

r (20)

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ula

(5)

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rcus

(minus1

5) C

asta

nea

(minus6)

Fag

us (minus3

)minus1

17

minus15

0minus1

minus16

18

minus24

25

11

7minus1

83

minus2minus1

Cen

tral

oak

-pin

e (3

3)

Acer

(7)

Juni

peru

s (3

)Q

uerc

us (minus1

7)

Pin

us

(minus4)

Cas

tane

a (minus

3)

minus23

minus1minus4

minus3minus1

08

minus22

18

minus19

minus20

minus15

31

Gre

at L

akes

oak

-pin

e (1

8)

Ace

r (9)

Car

ya (

3)

U

lmus

(3)

Que

rcus

(minus2

4)

1minus8

50

3minus1

51

0minus2

32

10

17

minus23

minus16

91

Nor

thea

st c

onife

r-no

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hard

woo

ds (

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Ace

r (19)

Pru

nus

(5)

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tula

Que

rcus

(4)

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s (minus

23

) T

suga

(minus

8)

Pic

ea (minus5

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9minus1

10

51

1minus1

86

minus8minus1

36

5minus8

33

Gre

at L

akes

con

ifer- n

orth

ern

hard

woo

ds (

29)

Ace

r (14)

Pop

ulus

(1

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Fra

xinu

s (3

)Ts

uga

(minus1

8)

Fag

us

(minus7

) B

etul

a (minus

6)

21

minus60

02

minus79

minus12

minus15

14

minus2minus1

3minus3

12

Gre

at L

akes

pin

e- no

rthe

rn

hard

woo

ds (

33)

Que

rcus

(13)

Pop

ulus

(

12)

Ace

r (12)

Pinu

s (minus

29

) T

suga

(minus

10

) F

agus

(minus4

)minus1

30

10

0minus1

69

4minus2

0minus6

19

minus16

minus16

minus11

5

Subb

orea

l con

ifers

(31)

Popu

lus

(15)

Fra

xinu

s (5

) A

cer (

5)

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s (minus

18

) L

arix

(minus

13

) B

etul

a (minus

3)

minus84

20

minus15

21

1minus1

minus15

9minus1

6minus1

0minus1

22

0




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