ii F o r e s tF o r e s tBiogeosciences and ForestryBiogeosciences and Forestry

Sweetgum: a new look

Joshua P Adams (1), Jody M Lingbeck (2), Philip G Crandall (3), Elizabeth M Martin (4), Corliss A O’Bryan (3)

Sweetgum (Liquidambar styraciflua L.) is the only species of its genus in theWestern hemisphere. The species is a relatively early successional specieswith wide seed dispersal, fast growth and is considered one of the most adap-table tree species in North America, growing across a wide range of soil types,altitudes, and hydrologic conditions. This species has routinely been consi-dered a lesser desired species by many forest managers trying to grow treeplantations or even in natural stands because the species tends to rapidlyinvade and dominate a site. However, because of sweetgum’s adaptability,ease of propagation and field planting, and fast growth rate, the tending ofsweetgum as a potential crop for improved markets has been reinvigorated.Managing sweetgum also opens the possibility of development of new productsand markets that supplement the traditional markets and can produce furthervalue-added products. Increasingly, sweetgum is not viewed with as muchantipathy amongst foresters and its potential as valuable resources is beingrediscovered.

Keywords: Sweetgum, Liquidambar styraciflua L., Fast-growing species, Po-tential crop, Value-added products

Historical prospectiveThe North American species sweetgum

(Liquidambar styraciflua L.) is one of onlyfour species in the Liquidambar genus, alsoincluding species formosana, orientalis, andacalysina. The L. formosana, or Formosongum, inhabits southeastern Asia and is na-med for Formoson (Taiwan) Island; whilethe smaller statured species L. acalysinainhabits the mainland of Southeast Asia.Oriental sweetgum, L. orientalis, is nativeto the eastern Mediterranean region, in-cluding Turkey and the island of Rhodes.The genus first appears in the fossil recordwith many other flowering plants in thePaleocene epoch, ancestors to modern li-neages arose in the Oligocene epoch (Ku-prianova 1960). The genus reached its wi-dest distribution by the Miocene epoch(Uemura 1983) and is highly diverged fromother economically important fast-growingspecies that are currently common in thesoutheast United States (Fig. 1). There isextremely old evidence of L. styraciflua

inhabitation of North America, probablymoving into the continent during the exis-tence of an ancient North Atlantic landbridge that predates the more commonlyknown North Pacific land bridge (Hoey &Parks 1991). A relic of this ancient migrationis also evident in modern genetic divergen-ce data, in which sweetgum is actually acloser relative to the western Asia/Europespecies, L. orientalis, than the two eastAsian species, L. formosa and L. acalycina.The genetic identity based on a proportionof 22 loci similar between the two speciesis 0.51. While it potentially maintained con-tact with the east Asian species via theNorth Pacific land bridge, the North Ameri-can species had lower genetic identities of0.43 and 0.48 with L. formosa and L. aca-lycina, respectively (Hoey & Parks 1991,1994, Li et al. 1997). Interestingly, the low-est genetic similarities were between theEurope/west Asia species and the two eastAsia species (Hoey & Parks 1991).

Though the species have been isolated

for thousands of years, they are derivedfrom a common ancestor in the Mioceneera that favored sites of mesic, warm tem-perate areas (Hoey & Parks 1991). The endof the Miocene saw global cooling and thebeginning of glaciation in the Pleistoceneepoch. These climatic changes limited thegenetic exchange among the species pro-genitors and greatly limited each speciesgeographical range on the landscape (Wol-fe 1985). Though having a long period ofseparation, the species have similar mor-phologies thought to be due to evolutio-nary stasis and have similar ideal growingconditions (i.e., mesic and warm – Hoey &Parks 1991).

The North American sweetgum has mi-grated significantly since becoming iso-lated from the other Liquidambar speciesbut has maintained its preference for thesame prehistoric growing conditions. Inthe last 20 000 years of the late Quaternaryperiod comprising the Holocene epoch,sweetgum has migrated in iterations fromnorth to south with glacial movements(Williams et al. 2004). These glacial periodswere at their maximum between 21 000and 14 000 years ago pushing mesic, warmclimate species like sweetgum to the farsouth including the extreme gulf coast, Flo-rida, and Mesoamerica (Ruiz-Sanchez & Or-nelas 2014, Wright 1981). As glaciers beganto recede and the climate warmed andbecame wetter, the suite of present dayhardwood species began to move northagain. Only in the last 3000 years didsweetgum appear to begin to dominatethe southeast forests based on fossilizedpollen samples (Williams et al. 2004).

© SISEF http://www.sisef.it/iforest/ 719 iForest 8: 719-727

(1) School of Forestry, Louisiana Tech University, Ruston, Louisiana 71270 (USA); (2) Sea Star International LLC, Fayetteville, Arkansas 72701 (USA); (3) Departments of Food Science and Center for Food Safety, Fayetteville, Arkansas 72704 (USA); (4) Departments of Biologicaland Agricultural Engineering, University of Arkansas, Fayetteville, Arkansas 72704 (USA)

@@ Joshua P Adams (adamsj@latech.edu)

Received: Oct 02, 2014 - Accepted: Apr 21, 2015

Citation: Adams JP, Lingbeck JM, Crandall PG, Martin EM, O’Bryan CA (2015). Sweetgum: a new look. iForest 8: 719-727. – doi: 10.3832/ifor1462-008 [online 2015-06-23]

Communicated by: Gianfranco Minotta

Review ArticleReview Articledoi: doi: 10.3832/ifor1462-00810.3832/ifor1462-008

vol. 8, pp. 719-727vol. 8, pp. 719-727

Adams JP et al. - iForest 8: 719-727

Silvics, silviculture, and management overview

SilvicsPresently, sweetgum grows from central

Florida to eastern Texas. Its extreme north-ern range extends to Connecticut and sou-thern Illinois, south to the Gulf of Mexicocoast with scattered locations throughcentral America (Kormanik 1990). In thepast, the central American populationswere classified as their own species, Liqui-dambar macrophylla (Orsted 1863); how-ever, through the 20th century there emer-ged a consensus in literature that thegroup should be lumped into L. styraciflua.The species is regarded as one of the mostadaptable hardwood species in regards tosite conditions, growing best on moist allu-vial clays and loamy soils associated withriver floodplains (Kormanik 1990). The spe-cies is a major component of four forestcover types, a minor component of over 20others, and is commonly associated withother species such as maples (Acer rubrumand A. negundo), various hickories (Caryaglabra, C. laciniosa, C. ovate, and C. tomen-tosa), and shortleaf and loblolly pine (Pinusechinata and P. taeda, respectively).

Sweetgum enters into these site associa-tions via wind-blown seeds which are par-ticularly adapted to wind disseminationthrough the presence of small wingedstructures on the seed. The seeds emergeafter fruiting bodies mature by Septemberthrough November. The seeds are smalland prolific in which a kilogram of seedaverage 180 000 seeds compared to theassociated species P. taeda which may onlyaverage up to 40 000 seeds kg-1 (Bonner &

Karrfalt 2008). Germination of the seedscan occur quickly as they exhibit only ashallow dormancy (Nikolaeva 1969). In-deed with no cold stratification necessary,seeds may begin to germinate after anaverage of 7-8 days in a germinator andcan reach 90% germination after only 11days (Rink et al. 1979).

The initial growth traits can lead to rapidcolonization of a site, and within variousforest types, sweetgum is considered ashade intolerant species and grows veryrapidly to reach sunlight (Meadows & Stan-turf 1997). On a site cleared of overstory,sweetgum will tend to dominate the siteearly and continue to be a major compo-nent in the early to mid-successional stagesof a forest which can persist in southeast-ern U.S. forests for 200 years or longer(Hodges 1997). Cleared sites are also quick-ly re-colonized by sweetgum through pro-lific sprouting that produces vigorous andpersistent new trees (Wenger 1953). Onsites that are primarily regenerated withpine species, sweetgum is able to take theplace of pines as the pine cohort begins tosenesce as the stand goes through naturalsuccessional changes. Thus, sweetgum canbecome the dominant cover species untilthey are replaced by more shade-tolerantspecies (Hartnett & Krofta 1989).

Control of unwanted sweetgumSweetgum can be considered a weed or

nuisance tree in the context of some standmanagement objectives (Fig. 2). In a studyon the Yazoo National Wildlife Refuge,sweetgum was the most common speciesinto the area designated for cherrybark(Quercus pagoda), Nuttall (Q. nuttallii), Shu-

mard (Q. shumardii), water (Q. nigra), andwillow oak (Q. phellos) regeneration. Thisstudy led to the recommendation of plan-ting additional oak seedlings to ensurethese heavy-seeded species were presentfor wildlife management objectives (Allen1990). During initiation of southern pinestands that dominate timber production inthe southeast U.S., sweetgum is a definiteconcern. The presence of sweetgum canlead to greater competition for limitedresources such as water, reducing survivaland growth of the desired pine trees.Sweetgum can reduce soil moisture atdepths of 60-90 cm in the soil which candirectly adversely affect potential growthof the planted P. taeda stand (Mitchell et al.1993). Especially during times of limitedwater which is common from June to Sep-tember in much of the pine-sweetgum ran-ge, the effect of increased competition bysweetgum can lead to exacerbated waterstress and changes in stomatal conductan-ce, the exchange of carbon dioxide mole-cules through the leaf stomata, which af-fects photosynthesis (Perry et al. 1994).

Removal of sweetgum is often conductedduring the initial stages of stand develop-ment. This allows desired species to esta-blish and be more competitive with laterincursions by sweetgum. Control of juve-nile sweetgum can be conducted effecti-vely through use of various herbicides suchas glyphosate (e.g., Roundup™) which canbe applied via aerial, tractor, ATV, or ma-nual back pack sprayer depending on thesite, size of area, and affordability. Indeed,non-specific, broadcast spraying of a sitecan be very effective in control of sweet-gum. D’Anieri et al. (1990) reported thatsweetgum translocated 48% of appliedfoliar glyphosate to roots in comparison tocommon associates P. taeda and Acerrubrum L., 3% and 13%, respectively. Efficacyof glyphosate treatments is very good with1.68 kg m-2 glyphosate application effec-tively controlling 64-93% of sweetgum afterone year (Larsen et al. 1983, Wu et al.1983). Bacon & Zedaker (1987) found thatremoval of just two-thirds of woody com-petition (largely sweetgum) and herba-ceous control could result in a 53% increasein loblolly pine stem volume growth in thesecond year. With only total woody control(no herbaceous control), there was still a10% increase in pine volume production.Several other herbicides are notably effec-tive at controlling sweetgum, includingimazapyr, hexazinone, and triclopyr (Clat-terbuck & Armel 2011, Nelson et al. 2006).As for all herbicide treatments, the costs ofthe herbicides must then be carried for thelength of the stand rotation (e.g., 25-35years for an average managed loblolly pinestand), thus affecting decisions on sweet-gum removal.

Advances in propagation and growthWhile sweetgum may be regarded as of

marginal value, current and potential pro-duct markets may make sweetgum more

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Fig. 1 - A dendrogram created from the NCBI taxonomy browser (http://www.ncbi.nlm.nih.gov/Taxonomy/taxonomyhome.html/index.cgi) using other tree species thatare common to southeast United States’ forests. Species of the Liquidambar genusare in red.

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favorable in the future. Currently it is usedas a component in natural forest stands infloodplain areas and as an ornamental insome landscaping plans. To propel sweet-gum as a primary candidate for some ofthese uses, artificial propagation of sweet-gum will be necessary to ensure that supe-rior sweetgum trees are effectively andcheaply produced. Hare (1976) successfullypropagated cuttings that were taken frommature sweetgum (species formosa andstyraciflua) crowns. In early May, shootswere harvested and planted in a perlite-vermiculite mixture with temperature andwater control. After two months, up to 36%of cuttings rooted. Greater survival per-centages are achievable by taking a moretraditional approach and using cuttingsfrom sprouts. Vegetative shoots from se-verely pruned L. styraciflua plants resultedin 86% of cuttings rooted and 56% of cut-tings surviving and deemed plantable 25weeks after the cutting was rooted (Rieck-ermann et al. 1999). Rieckermann et al.(1999) also found that a weekly nitrogen(N) application of 25-50 mg l-1 was optimalfor promoting cutting development. Usingseverely pruned plants or hedging tech-niques, sweetgum can be quickly propaga-ted. These mini-cutting techniques involveinitial propagation of cuttings to producemini-stumps that are hedged and producesuccessive integrations of sprouts (avera-ging about 2.5 sprouts per 30 days) used asmicro-cuttings (Wendling et al. 2010). After10 intervals of harvesting mini-cuttings,only 6% of the mini-stumps had died. Thismethod was able to produce close to 3000mini-cuttings per square meter per yearand is a viable method to quickly expandgermplasm for field plantings (Wendling etal. 2010).

Sweetgum has also been successfullypropagated in vitro for many years. One ofthe earliest reports of an in vitro methodwas in 1980 using solid and liquid media(Sommer & Brown 1980). The researchersbased their initial work on established to-bacco protocols and found that bud diffe-rentiation would occur with cytokinin/au-xin ratios of (0.8-1.6 mg l-1 benzyadenine(BA) and 0.1-1.0 mg l-1 naphthaleneaceticacid (NAA), while root formation was con-ducted on media with a decreased ratio(0.2 mg l-1 BA and 1.0-4.0 mg l-1 NAA).Researchers germinated seedlings, excisedthe hypocotyl, and put sections of the tis-sue in the above cultures. Some cultureswere transferred to the same mediumswithout agar (i.e., liquid state) and main-tained in a shaker. In both solid and liquidform, successful somatic embryogenesiswas achieved.

This early success was followed bymature and juvenile plants successfullypropagated using excised shoot tips whichwere surface-sterilized with sodium hypo-chlorite (Sutter & Barker 1985). Both ma-ture and juvenile plants responded bestwhen first placed in a multiplication me-dia composed of Woody Plant Medium

(WPM), basal salt supplemented with 0.2mg l-1 BA and 0.05 mg l-1 NAA. Explants fromsuccessful multiplication were then rootedin WPM supplemented with 0.5-1.0 mg l-1

indole-3-butyric acid (IBA). While propaga-tion was successful, large differences inrooting percentages (33-100%) were evi-dent among parent stock (Sutter & Barker1985).

A protocol using the same hormones wasused by Brand & Lineberger (1988) on leaftissue. Woody Plant Medium (WPM) basalsalt supplemented with 2.5 mg l-1 BA and 0.1mg l-1 NAA was used to elicit shoot forma-tion from leaf tissue. Shoot formation wasincreased by damaging the leaf surface bycutting the lamina with razor. The authorsfound later in at least one variety, leavesused from intact plants produced over fourtimes the amount of adventitious shootsthan plants from in vitro use but was con-stant as the leaves aged (Brand & Line-berger 1991). In conjunction with develop-ment of in vitro techniques for propaga-tion, molecular transformation techniqueshave been developed which allow for thepotential of production of genetically mo-dified sweetgums. These could be engi-neered with advantageous traits such assuperior growth, regulation of seed pro-duction, and modified chemical synthesis.Sullivan & Lagrimini (1993) were able totransform sweetgum plantlets with threedifferent plasmids via Agrobacterium tume-faciens infection. Leaves were excised andtransversely cut at the midrib and incu-bated with the bacteria for three days inBA supplemented 2.5 mg l-1 BA WPM media.Afterwards, the bacterium was killed withcefotaxime and the leaf tissues were trans-ferred to fresh media. Callus tissue initiallyformed followed by shoots which were

excised and transferred to larger vessels.Plasmids have also been successfully trans-formed into sweetgum cultures via goldparticle bombardment. Using establishedbombardment protocols, Kim et al. (1999)were able to generate nodule cultureswhich were receptive to the gene transfertreatment. They found that sweetgum no-dules established from seedling hypocotylsshould be proliferated using a liquid me-dium and had desirable traits includingrapid growth of colonies, uniform cell size,and ability to produce regenerative tissue.

Sweetgum also appears to be easilytransferred from in vitro to greenhouseand subsequent field conditions. In vitroplants were noted to have physiologicalabnormalities including limited cytoplasmcontent, large leaf vacuoles, decreasedstarch content, and increased photosyn-thetic rates (Lee et al. 1985, Wetzstein &Sommer 1982). Plantlets must be accli-mated to field conditions and allowed timefor their morphology and cellular physio-logy to transform into normal field-grownconditions. Transferred to soil and harde-ning off is easily conducted by maintaininghigh-humidity by using a plastic bag cove-ring on the plant (Wetzstein & Sommer1982). Using such a technique allows foracclimation after about four weeks. Brand& Lineberger (1988) were also able to ea-sily root and acclimate shoots producedfrom leaf tissue culture.

Silviculture and managementThe next stage of sweetgum propagation

would be to plant the newly propagatedplants in nursery-like conditions for out-planting to true field conditions. Allowingthe propagules to acclimate and developroots is critical for eventual outplanting.

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Fig. 2 - Graduate student holding a desirable three-year-old loblolly pine that is underintense competition from fast growing sweetgum that naturally seeded into the areaafter the pine was planted. Sweetgum can be seen in both the foreground and back -ground and is already taller and crowding out the planted loblolly pine.

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Kormanik (1986) found that seedlings withmore than six lateral roots exceeding 1 mmin diameter outperformed lower gradeseedlings. These best seedlings only exhi-bited dieback in 41% of seedlings and had79% survival after the first year; whereas,the two lower grades had 67% and 89%dieback and 67% and 51% survival after oneyear. Larger seedlings, in regards to rootcollar diameter (RCD), are also good indica-tors of later growth. Increases of RCD from4-8 to 12-16 mm led to three-year increasein volume of 90% (Mc Nabb & Vander-Schaaf 2005).

During the seedling time ex vitro, theroots also have the added benefit of beingexposed to beneficial mycorrhizal. Thesefungal infections resulted in 80x greaterabove ground biomass after the seedlingwere grown for one year in nursery condi-tions (Bryan & Kormanik 1977). Indeed,without mycorrhizal presence, seedlingsare ill adapted to the competitive fieldenvironment and the plants will either dieor be severely stunted (Kormanik et al.1977). With mycorrhizal, sweetgum per-forms well with N fertilization (560 kg Nha-1) in nursery conditions. Additionally, afertilizer, such as ammonium nitrate, ispreferable over ammonium sulfate, as itdoes not acidify the soil as severely (Brownet al. 1981).

Once deployed in plantations, establi-shed sweetgum thrives with fertilization.Through most of sweetgum’s range, N isone of the most limiting factors to growthin forest ecosystems and N additions con-sistently result in increased stand net pri-mary production and increased fine rootproduction (Chang 2003, Norby & Iversen2006, Iversen & Norby 2008). In a young 4-

year-old study sweetgum plantation, Guoet al. (1998) applied N and phosphorous(P) treatments and found that a N+P (229.8kg ha-1 and 137.9 kg ha-1, respectively) com-bination treatment or N alone treatment at229.8 kg ha-1 generally performed the bestin regards to tree height, diameter andcrown length. These effects were very evi-dent after the first year-post treatment(i.e., ages 6 and above) and were maintai-ned through the course of the study whenthe stand was 15-years-old. In a 9-year-oldplantation, sweetgum produced the mostaboveground biomass at highest fertiliza-tion levels in the study that were equiva-lent of 400 kg N ha-1 (Nelson et al. 1995);however, annual incremental growth ismeasurable for only one to two years (Nel-son & Switzer 1990). Still, the need for fer-tilization is site specific and each siteshould be tested for its inherent nutrients.Scott et al. (2004) found that on a con-verted agriculture field rich in nutrients,there was no effect on sweetgum growthfrom the addition of N and P, while treeson a forest cut-over site responded with a60% increase in biomass.

Deployment of whole plantations ofsweetgum can generate rapid biomass pro-duction which can be used for many of theoutlined products. Volume production ran-ged from 8.4 m3 ha-1 year-1 to 18.62 m3 ha-1

year-1 with no fertilizer up to 399 kg ha-1 in aMississippi study after nine years (Nelson &Switzer 1992). In the same study, increasesin dimensional attributes after nine yearswere 9, 14, 28, 39, and 40% for height, DBH,basal area, stem volume, and woodybiomass, respectively (Nelson & Switzer1990). In South Carolina with irrigation andfertilization four-year growth rates of

sweetgum ranged from 2.4 to 5.1 Mg ha-1

year-1 (Coyle et al. 2008). On a marginalagriculture site in Georgia, sweetgumgrown without any amendments producedaverage of 12.3 Mg ha-1 after six years, whilemaximal amendments (irrigation+fertiliza-tion+pest control) resulted in 62.6 Mg ha-1.

While sweetgum is capable for producingrapid growth suitable for short rotationcrops, sweetgum is a valued hardwoodlumber species. As such, there is renewedinterest in sweetgum as a valuable compo-nent to predominantly oak stands by ex-ploiting its natural place in river floodplainecosystems. In an attempt to mimic naturalstand succession, Lockhart et al. (2006)planted cherrybark oak (Quercus pagoda)and sweetgum seedlings in mixtures. Inthese mixtures, cherrybark oak seedlingswere surrounded by two rows of sweet-gum (Fig. 3). Initially the stand was domi-nated by sweetgum as would be expectedbased on its early and aggressive growth.After 21 years, the sweetgum began to sta-gnate and the cherrybark oak ascendedinto the upper canopy. This planned spe-cies succession offers potential benefits ofa harvest of sweetgum timber before thecherrybark oaks are harvested which canbe 60-80 years in some cases. While cherry-bark oaks are competing with sweetgumfor light, the sweetgum serves as a “trai-ner” tree to increase the bole quality ofcherrybark oak. This echoes an earlier stu-dy by Clatterbuck & Hodges (1988) whichfound a lack of different species like sweet-gum around the desirable cherrybark oaktrees caused the cherrybark oak to havepoor form (e.g., many branches, straight-ness deficiencies) and to be commerciallyless desirable.

Mid-rotation removal of sweetgum iswarranted. Johnson & Krinard (1988)found that in a two mixed sweetgum-redoak stands (red oaks were composed of Q.pagoda, Q. phellos and Q. nigra), approxi-mately 25% of the sweetgum trees diedbetween ages 18 and 23. This was imme-diately following the maximum observeddensity (3879 trees per hectare) on the siteat which time light became a limiting fac-tor. This increased competition and declinein sweetgum led to the red oak trees gro-wing twice as fast in diameter and 60%faster in height between ages 23 and 29.The growth changes led to the predictionof oaks overtaking the sweetgum in totalheight by ages 30 to 35. Similar trendswere all observed by Clatterbuck et al.(1984), who found that oaks in their oldfield stand overtook sweetgum as early asage 15 to 25 years.

A final regeneration harvest necessitatesa system that lead to maximal light inter-ception for sweetgum. A clearcut methodis optimal for even-age regeneration of astand. This system will favor in the earlyyears of regeneration shade-intolerant andlight-seeded species such as sweetgum andriver birch (Meadows & Stanturf 1997). Aseed-tree method would also have the

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Fig. 3 - Sweetgum were planted and allowed to grow for 28 years around potentiallymore valuable cherrybark oaks. The crowns of sweetgum (narrow crowns in the cen-ter of the picture) are expected to help shear off limbs of the cherrybark oak, impro -ving their quality. The sweetgum also serve as a source of income before the cherry -bark oak is finally harvest which may be over 60 years.

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same effect, while leaving trees on sitemay be a waste as the species is so lightseeded that blown in seed from adjacentareas or regeneration from root sprouts isusually assured (Meadows & Stanturf1997). The shelterwood system as well asthe uneven-age system, single-tree selec-tion, are usually not favored for final har-vest if the goal is sweetgum regenerationas they favor more shade tolerant speciessuch as elms and maples (Johnson & Kri-nard 1983). Indeed, even the uneven-agesystem group selection usually does notproduce openings in the canopy largeenough to maintain a shade intolerant spe-cies such as sweetgum (Clatterbuck & Mea-dows 1993). Thus final harvest options,with the intent of sweetgum regeneration,are very limited.

Commercial products

Early usesSweetgum has chemical properties that

are beneficial for a large array of ailmentsas detailed by Lingbeck et al. (2015). Thesebenefits have been harnessed from earlytimes with several Native American tribesdocumented as using sweetgum for medi-cinal purposes. Hamel & Chiltoskey (1975)documented several uses among the Che-rokee tribe including using rosin and innerbark for diarrhea, flux, and dysentery, salvefrom leaves used for wounds, sores, andulcers, and infusions of bark were used as asedative and given to people with nervous-ness. The Choctaw and Houma tribes ofLouisiana both used a root mixture fordressing cuts and wounds (Bushnell 1909,Speck 1941). These tribes also used thesolidified sap as chewing gum. This prac-tice may even continue today and certainlywas prevalent during the early 20th centurybased on personal communications withseveral people from Louisiana born duringthe great depression.

Many of these same uses of sweetgumwere kept after European colonization.During the civil war, a field guide for medi-cal officers was commissioned for the Con-federate States and published after thewar. Sweetgum was mentioned many ti-mes in this book (Porcher 1869). In theguide, the author mentions many of thesame uses for patients including boilingequal amounts of red oak and sweetguminto syrup, adding spirits, and digesting theconcoction to alleviate diarrhea and dysen-tery. The manual also recommend mixingthe extract with tea or water. Ironically,water extraction is successfully used in cur-rent times to extract shikimic acid fromsweetgum bark as a precursor to Tamiflu®

(Martin et al. 2010). The leaves of thesweetgum were said to contain high tanninlevels to provide a powerful astringent.One interesting comment in the guide is areference to an acid obtained from sweet-gum. The author states that he disagreeswith the English assentation that benzoicacid is prevalent but rather cynamic acid.

This early reference to “cynamic acid” isprobably the same cinnamic acid that hassince been more recently “rediscovered”and studied across the Liquidambar speciesfor its antioxidant, antipathogenic, andantimicrobial properties (Karadeniz et al.2011, Ocsel et al. 2012, Sova 2012, Gurbuz etal. 2013).

TimberWhile much emphasis has dealt with the

removal of sweetgum from future timberstreams, sweetgum can be utilized forpulp, furniture grade lumber, pallets, ve-neer and panels. The heartwood of thesweetgum trees is reddish brown with in-terlocking grain and is often mistaken forcherry wood, given rise to the species alsobeing called redgum. The red heartwoodwas often used in furniture, millwork,doors and paneling, and was once a valua-ble resource as it was sold in Europeanmarkets as satin walnut (Cassens 2007).Dwindling supplies of the old-growth redheartwood, however, led to an increase insapwood use. Today, most sweetgum lum-ber is from the sapwood which is white incolor with a pinkish tint (Cassens 2007).Sapwood is used in making low end furni-ture and furniture frames. However, deve-lopment of composite wood for this pur-pose has reduced the demand for sweet-gum lumber. Due to its high shrinkagecoefficient and its tendency to warp due toits interlocked grain, sweetgum wood isone of the lowest valued hardwoods avai-lable (Cassens 2007). Still, sweetgum haswood properties that make it amenable tomodern wood processing techniques. Thespecies is easily peeled into veneers for usein plywood which can have at least equalstrength compared to similar processedsouthern pine plywood (Biblis & Lee 1984).

Recent lamination developments in struc-tural lumber have opened other uses forsweetgum which can be oriented to createbeams of considerable strength and lightweight for construction of bridges andground flotation mats on which heavyequipment is placed to prevent soil distur-bance (Shmulsky et al. 2008, Shmulsky &Shi 2008).

BiomassBiomass is a term for organic material

from plants and may be a key source ofrenewable energy, possibly replacing orreducing our demand for supplies of fossilfuels (Wang et al. 2012). The ability ofsweetgum to rapidly grow on a wide rangeof soils, as well as its ability to re-sproutprolifically, make sweetgum trees a suita-ble biomass source to be used for bioener-gy production including cellulosic ethanol,wood pellets and bio-oil (Wright & Cun-ningham 2008). This rapid proliferation ofproducts could be tied with recent ad-vances in development of specific varietiesproduced through tissue culture that arepromising for short-rotation biomass (Mer-kle & Cunningham 2011). The cultureswould be grown for just a few years andthen harvested and chipped before refinedinto a specific product (Fig. 4). However,hardwood plantations of sweetgum maynot be economically viable. In 2006, esti-mated costs for production of a sweetgumplantation throughout the first 12 yearsrange from 778 to 1742 US$ per hectareincluding costs associated with site prepa-ration, planting, herbicide and pesticidetreatments and fertilization. For a low pro-ducing plantation (5 Mg per hectare peryear) that could result in costs of 31 to 64US$ per Mg. Higher producing sweetgumplantations could expect costs of 13 to 27

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Fig. 4 - An industrial chipper is being used by a logging crew to produce chips fromsweetgum and other hardwoods in a pine plantation. Chips are able to be used as asource of biomass fuel.

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US$ per Mg compared to rival species eas-tern cottonwood and pine which couldcost 14-40 and 6-18 US$, respectively, inhighly productive plantations (Kline & Cole-man 2010). When costs of logging andtransportation are factored in, only highproducing plantations could expect to yielda profit given a target delivery price of 55US$ per Mg (DOE 2007, Kline & Coleman2010).

Cellulosic ethanolThe generation of ethanol from cellulosic

biomass offers many benefits. Ethanol iscleaner burning that traditional fuels, thusreducing pollution and greenhouse emis-sions which may lead to global warming(Wyman et al. 1992). Perhaps the biggestbenefit of cellulosic ethanol is the utiliza-tion of abundant, low-cost feedstockswhich may otherwise be considered waste.Cellulosic ethanol is generated from enzy-matic hydrolysis of cellulose to form glu-cose which is then fermented to produceethanol. However, due to the lignin con-tent, which protects much of the cellulosefrom enzymatic action, a pretreatmentstep before hydrolysis is usually necessaryto increases yields. Common pretreatmentsteps include treatment with dilute acid orbase, hot water, an organic solvent (orga-noslov) or by steam explosion (Yang & Wy-man 2008, Zhao et al. 2009).

Wyman et al. (1992) studied the efficiencyof simultaneous saccharification and fer-mentation (SSF) method in which biomass,hydrolysis enzymes and fermentation yeastare added together in one vessel. Greaterethanol yields are often seen with SSFbecause sugars, which are inhibitory to theconversion process, are rapidly convertedto ethanol. Four woody crops (aspen, twohybrids poplars and sweetgum), three her-baceous crops (switchgrass, weeping lovegrass and a legume Sericea lespedeza) andthree agricultural residues (corn cobs, cornstover and wheat straw) were studied. Thebiomass was pretreated in dilute acid andwoody crops were ground before theywere placed in the fermentation flask con-taining supplemented media along withcellulase, β-glucosidase (to reduce accumu-lation of the inhibitor cellobiose) and theyeast S. cerevisiae alone or in a mixed cul-ture with B. clausenii and incubated at 37 °Cfor 8 days. With S. cerevisiae alone, theagricultural residues, corn cobs, corn sto-ver and wheat straw produced the highestcellulose to ethanol conversion of 94, 92and 90%, respectively. The herbaceouscrops, weeping love grass and switchgrass, produced 89% and 84%, respectively,while Sericea lespedeza showed poor yieldsof 52%. The woody crops Populus maxi-mowiczii x nigra, Populus trichocarpa × del-toides, Populus tremuloides (aspen) andsweetgum produced 90, 82, 94, and 86%yields, respectively. Results were similarwith mixed yeast cultures at high enzymeand β-glucosidase concentrations. Using asimilar protocol of pentose fermentation,

the costs of hardwood produced ethanolwas estimated to be about 0.61 US$ L -1 withthe main costs attributable to raw mate-rials and capital (Sassner et al. 2008).

McConnell & Shi (2011) evaluated the par-tial hydrolysis of dilute sulfuric acid, dilutesodium hydroxide and deionized water onholocellulose content (total polysacchari-des fraction from wood) from sweetgum,red oak and yellow-poplar (Liriodendron tu-lipifera). All treatments reduced holocellu-lose levels in all species; however, sulfuricacid treatment showed the greatest reduc-tion in holocellulose levels in sweetgumand red oak, while sodium hydroxide sho-wed the greatest reduction of holocellu-lose levels in yellow-poplar. In addition,partial hydrolysis with dilute sulfuric acid ofsweetgum and red oak produced residualproperties in the wood which may makethem suitable for use in wood compositesadding additional value to the lignocellu-losic ethanol production process (McCon-nell & Shi 2011).

Sannigrahi et al. (2012) used a two-stepozone pretreatment to increase polysac-charide release and hence increase ethanolproduction from sweetgum and miscan-thus. In the first step, the biomass wastreated with ozone gas to generate acidiccomponents. The biomass was then equili-brated in water and subject to autohydro-lysis at high temperature and pressure toincrease solubilization of celluloses. Theresultant cellulose was converted glucoseat a conversion rate of 68% for both sweet-gum and miscanthus. The glucose was fi-nally fermented to produce ethanol withyields of 14.0 g ethanol per 100 g biomassfor sweetgum and miscanthus was 11.1 gethanol per 100 g biomass. In addition,ozone pretreatment is relatively inexpen-sive and generates an environmentallyfriendly waste stream and is thus a promi-sing pretreatment strategy (Sannigrahi etal. 2012).

Bio-oilBio-oil is generated from the fast pyroly-

sis of biomass and has the potential to beused as liquid fuel (Bridgwater et al. 2002).Sweetgum, switchgrass and corn stoverwere all evaluated for their ability to pro-duce bio-oil after various pretreatments.Sweetgum, with particle sizes from 0.68 to1.532 mm produced 52 wt% of bio-oil fromfast pyrolysis in which the biomass wasrapidly heated from 350-600 °C in the ab-sence of oxygen. In comparison, similarsized switchgrass produced 33 wt% whilecorn stover produced 35 wt%. Steam explo-sion pre-treatment lower bio-oil yield for allthree biomass compound pre-treatmentwith 1% sulfuric acid increase yields to 56%,46% and 51% for sweetgum, switchgrassand corn stover, respectively. The reducedyield seen with steam explosion wasthought to be due to the reduction ofhemicellulose content after treatment,whereas pre-treatment with 1% acid increa-se yield due to reduced ash content which

is thought to limit bio-oil production. Thehigh rate of bio-oil production, along withthe low cost of acid pretreatment andavailability of sweetgum trees, make it fea-sible that sweetgum can be a source ofbiomass for bio-oil production (Wang et al.2012).

Economic assessmentIn the current era, most timber is sold by

tonnage, segregated only by hardwoodand pine with the exception of trees tar-geted for very specific, high-value uses(e.g., black walnut for high quality furnitureand paneling or sycamore/cottonwoodplantations used for specialty paper). Inthis common scenario of timber sales,logged hardwoods are combined andweighed in mass as either sawtimber orpulpwood, depending on the size of thetree (≥30.5 and <30.5 cm diameter atbreast height, respectively). Over an 11state region stretching from Texas in thewest to the Atlantic and as north as Vir-ginia, the prices of mixed hardwood pulp-wood surpassed pine pulpwood in 2010 (inmany cases the highest stumpage pricesever received for such products) with anaverage 1st quarter 2010 price of 11.05 US$tonne-1. Hardwood sawtimber has histori-cally garnered higher prices with an ave-rage of 20.40 US$ tonne-1 (TMS 2010). Sincethen, prices fell slightly and have slowlyrebounded to near 2010 levels in early 2014with pulpwood averaging 9.15 US$ tonne-1

and sawtimber averaging 24.77 US$ tonne-1

(http://www.timbermart-south.com/ - TMS2014). As it is so often lumped togetherwith other hardwoods, sweetgum has gar-nered little specific study even from aneconomic prospective as prices have risen.For instance, the hardwood pricing publica-tion Harwood Review Global (http://www.hardwoodreview.com) has costs brokendown for a variety of species including cot-tonwood, cherry, hard maple, hickory, redoak, white oak, and walnut. However,sweetgum is noticeably lacking.

ConclusionSweetgum is a unique species in North

America and has been separated from itrelatives for many thousands of years. Inits current ecosystem spanning over muchof the eastern United States and into Cen-tral America, the species thrives. The spe-cies rapid growth rate and adaptability onmany sites poises both promise and pro-blems for forest management. When hard-wood markets were weak, the species wasconsidered by many a weed among thedesirable species. More recently with theincreased market for hardwood lumberand newer markets such as various bio-based energy products, renewed interest isupon sweetgum. Instead of spending capi-tal to rid sites of the native species, findingnew methods to potentially harness valuefrom the prolific species is now attractive.

The fast growth rate and developed cul-ture systems make this species a prime

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candidate for use alone or with speciesmixtures for plantations. Systems of propa-gation have been developed that allowgrowers to totally capture any genetic traitdeemed desirable and potentially mass-produce for planting. After planting,sweetgum competes well with other spe-cies and, with some treatment such as fer-tilization or irrigation, accumulates largequantities of biomass. Other exciting as-pects of this species are the medicinal pro-perties that have been recently outlined byLingbeck et al. (2015). Efficiently using thetree for both more traditional markets andintegrating into developing markets suchas biofuel and pharmaceuticals could pro-pel the species to a more desirable statusamong the forest managers.

ReferencesAllen JA (1990). Establishment of bottomland

oak plantations on the Yazoo National WildlifeRefuge Complex. Southern Journal of AppliedForestry 14 (4): 206-210. [online] URL: http://www.ingentaconnect.com/content/saf/sjaf/1990/00000014/00000004/art00013

Bacon CG, Zedaker SM (1987). Third-year growthresponse of loblolly pine to eight levels of com-petition control. Southern Journal of AppliedForestry 11 (2): 91-95. [online] URL: http://www.ingentaconnect.com/content/saf/sjaf/1987/00000011/00000002/art00008

Biblis EJ, Lee W-C (1984). Properties of sheath-ing-grade plywood made from sweetgum andsouthern pine. Wood and Fiber Science 16 (1):86-92.

Bonner FT, Karrfalt RP (2008). The woody plantseed manual. Agriculture Handbook 727, USDAForest Service, Washington, DC, USA, pp. 1223.[online] URL: http://books.google.com/books?id=ZnBRmdUU_3UC

Brand MH, Lineberger RD (1988). In vitro adven-titious shoot formation on mature-phase leavesand petioles of Liquidambar styraciflua L. PlantScience 57 (2): 173-179. - doi: 10.1016/0168-9452(88)90084-2

Brand MH, Lineberger RD (1991). The effect ofleaf source and developmental stage on shootorganogenic potential of sweetgum (Liquidam-bar styraciflua L.) leaf explants. Plant Cell, Tis-sue and Organ Culture 24 (1): 1-7. - doi: 10.1007/BF00044257

Bridgwater A, Toft A, Brammer J (2002). A tech-no-economic comparison of power productionby biomass fast pyrolysis with gasification andcombustion. Renewable and Sustainable Ener-gy Reviews 6 (3): 181-246. - doi: 10.1016/S1364-0321(01)00010-7

Brown R, Schultz R, Kormanik P (1981). Res-ponse of vesicular-arbuscular endomycorrhizalsweetgum seedlings to three nitrogen fertiliz-ers. Forest Science 27 (2): 413-420. [online]URL: http://www.ingentaconnect.com/content/saf/fs/1981/00000027/00000002/art00035

Bryan WC, Kormanik PP (1977). Mycorrhizae ben-efit survival and growth of sweetgum seedlingsin the nursery. Southern Journal of AppliedForestry 1 (1): 21-23. [online] URL: http://www.ingentaconnect.com/content/saf/sjaf/1977/00000001/00000001/art00009

Bushnell DI (1909). Choctaw of Bayou Lacomb,

St. Tammany Parish, Louisiana. WashingtonGovernment Printing Office, Washington, DC,USA, pp. 23.

Cassens DL (2007). Hardwood lumber and ve-neer series: sweetgum. Extension PublicationFNR-300-W, Purdue University, West Lafayette,IN, USA, pp. 4. [online] URL: http://www.extension.purdue.edu/extmedia/FNR/FNR-300-W.pdf

Chang SX (2003). Seedling sweetgum (Liquidam-bar styraciflua L.) half-sib family response to Nand P fertilization: growth, leaf area, net pho-tosynthesis and nutrient uptake. Forest Eco-logy and Management 173 (1-3): 281-291. - doi:10.1016/S0378-1127(02)00007-5

Clatterbuck WK, Hodges JD, Burkhardt EC(1984). Cherrybark oak development in naturalmixed oak-sweetgum stands - preliminary re-sults. In: Proceedings of the “3rd Biennial South-ern Silvicultural Research Conference” (Shoul-ders E ed). Southern Forest Experiment Sta-tion, USDA Forest Service, Atlanta, GA, USA,pp. 438-444.

Clatterbuck WK, Hodges JD (1988). Develop-ment of cherrybark oak and sweet gum in mi-xed, even-aged bottomland stands in centralMississippi, USA. Canadian Journal of ForestResearch 18 (1): 12-18. - doi: 10.1139/x88-003

Clatterbuck W, Meadows J (1993). Regeneratingoaks in the bottomlands. In: Proceedings of theSymposium “Oak Regeneration: Serious Pro-blems, Practical Recommendations” (Loftis DL,McGee CE eds). Knoxville (TX, USA) 8-10 Sep1992. General Technical Report SE-84, South-eastern Forest Experiment Station, USDA Fo-rest Service, Asheville, NC, pp. 184-195.

Clatterbuck WK, Armel GR (2011). PB1799 sitepreparation for natural regeneration of hard-woods. Publication no. PB1799, University ofTennessee Extension, Knoxville, TX, USA, pp. 11.[online] URL: http://trace.tennessee.edu/utk_agexfores/113

Coyle DR, Coleman MD, Aubrey DP (2008).Above-and below-ground biomass accumula-tion, production, and distribution of sweetgumand loblolly pine grown with irrigation and fer-tilization. Canadian Journal of Forest Research38 (6): 1335-1348. - doi: 10.1139/X07-231

D’Anieri P, Zedaker SM, Seiler JR, Kreh RE(1990). Glyphosate translocation and efficacyrelationships in red maple, sweetgum, andloblolly pine seedlings. Forest Science 36 (2):438-447. [online] URL: http://www.ingentaconnect.com/content/saf/fs/1990/00000036/00000002/art00021

DOE (2007). Biomass multi-year program plan.Office of the Biomass Program, Energy Efficien-cy and Renewable Energy, US Department ofEnergy, Washington, DC, USA.

Guo Y, Lockhart BR, Ka TT (1998). Effect of nitro-gen and phosphorus fertilization on growth ina sweetgum plantation in southeastern Arkan-sas. Southern Journal of Applied Forestry 22(3): 163-168. [online] URL: http://www.ingentaconnect.com/content/saf/sjaf/1998/00000022/00000003/art00008

Gurbuz I, Yesilada E, Demirci B, Sezik E, DemirciF, Baser KH (2013). Characterization of volatilesand anti-ulcerogenic effect of Turkish sweet-gum balsam (Styrax liquidus). Journal of Ethno-pharmacology 148 (1): 332-336. - doi: 10.1016/j.jep.2013.03.071

Hamel PB, Chiltoskey MU (1975). Cherokeeplants and their uses – a 400 year history. He-rald Publishing Co., Sylva, NC, USA, pp. 64.

Hare R (1976). Rooting of American and For-mosan sweetgum cuttings taken from girdledand nongirdled cuttings. Tree Planters’ Notes27 (4): 6-7.

Hartnett DC, Krofta DM (1989). Fifty-five years ofpost-fire succession in a southern mixed hard-wood forest. Bulletin of the Torrey BotanicalClub 116 (2): 107-113. - doi: 10.2307/2997194

Hodges JD (1997). Development and ecology ofbottomland hardwood sites. Forest Ecologyand Management 90 (2-3): 117-125. - doi:10.1016/S0378-1127(96)03906-0

Hoey MT, Parks CR (1991). Isozyme divergencebetween eastern Asian, North American, andTurkish species of Liquidambar (Hamamelida-ceae). American Journal of Botany 78 (7): 938-947. - doi: 10.2307/2445172

Hoey MT, Parks CR (1994). Genetic divergence inLiquidambar styraciflua, L. formosana, and L.acalycina (Hamamelidaceae). Systematic Bota-ny 19 (2): 308-316. - doi: 10.2307/2419604

Iversen CM, Norby RJ (2008). Nitrogen limitationin a sweetgum plantation: implications for car-bon allocation and storage. Canadian Journalof Forest Research 38 (5): 1021-1032. - doi:10.1139/X07-213

Johnson RL, Krinard R (1983). Regeneration insmall and large sawtimber sweetgum-red oakstands following selection and seed tree har-vest: 23-year results. Southern Journal ofApplied Forestry 7 (4): 176-184. [online] URL:http://www.ingentaconnect.com/content/saf/sjaf/1983/00000007/00000004/art00003

Johnson RL, Krinard RM (1988). Growth anddevelopment of two sweetgum-red oak standsfrom origin through 29 years. Southern Journalof Applied Forestry 12 (2): 73-78. [online] URL:http://www.ingentaconnect.com/content/saf/sjaf/1988/00000012/00000002/art00004

Karadeniz B, Ulker Z, Alpsoy L (2011). Genotoxicand cytotoxic effects of storax in vitro. Toxico-logy and Industrial Health 29 (2): 181-186. - doi:10.1177/0748233711428642

Kim M, Sommer H, Dean JD, Merkle S (1999).Transformation of sweetgum via microprojec-tile bombardment of nodule cultures. In VitroCellular and Developmental Biology - Plant 35(1): 37-42. - doi: 10.1007/s11627-999-0007-z

Kline KL, Coleman MD (2010). Woody energycrops in the southeastern United States: twocenturies of practitioner experience. Biomassand Bioenergy 34 (12): 1655-1666. - doi: 10.1016/j.biombioe.2010.05.005

Kormanik PP (1986). Lateral root morphology asan expression of sweetgum seedling quality.Forest Science 32 (3): 595-604. [online] URL:http://www.ingentaconnect.com/content/saf/fs/1986/00000032/00000003/art00008

Kormanik PP (1990). Liquidambar styraciflua L.sweetgum. In: “Silvics of North America - Vol. 2,Hardwoods” (Burns RM, Honkala BH eds). Agri-culture Handbook 654, USDA Forest Service,Washington, DC, USA, pp. 400-405. [online]URL: http://books.google.com/books?id=bMnRqCA3uzwC

Kormanik PP, Bryan WC, Schultz RC (1977). Influ-ence of endomycorrhizae on growth of sweet-gum seedlings from eight mother trees. Forest

iForest 8: 719-727 725

iFor

est

– B

ioge

osci

ence

s an

d Fo

rest

ry

Adams JP et al. - iForest 8: 719-727

Science 23 (4): 500-505. [online] URL: http://www.ingentaconnect.com/content/saf/fs/1977/00000023/00000004/art00021

Kuprianova LA (1960). Palynological data con-tributing to the history of Liquidambar. Pollenet Spores 2 (1): 71-88.

Larsen T, Gnegy J, Olinger H (1983). Glyphosatefor release of loblolly pine (Pinus taeda, hard-wood competition). Proceedings of the Sou-thern Weed Science Society 36: 235-238.

Lee N, Wetzstein HY, Sommer HE (1985). Effectsof quantum flux density on photosynthesis andchloroplast ultrastructure in tissue-culturedplantlets and seedlings of Liquidambar styraci-flua L. towards improved acclimatization andfield survival. Plant Physiology 78 (3): 637-641. -doi: 10.1104/pp.78.3.637

Li JH, Bogle AL, Klein AS (1997). Interspecificrelationships and genetic divergence of the dis-junct genus Liquidambar (Hamamelidaceae) in-ferred from DNA sequences of plastid genematK. Rhodora 99 (899): 229-240.

Lingbeck JM, O’Bryan CA, Martin EM, Adams JP,Crandall PG (2015). Sweetgum: an ancient sour-ce of beneficial compounds with modern bene-fits. Pharmcognosy Review 9 (17) 1-11. - doi:10.4103/0973-7847.156307

Lockhart BR, Ezell AW, Hodges JD, ClatterbuckWK (2006). Using natural stand developmentpatterns in artificial mixtures: a case study withcherrybark oak and sweetgum in east-centralMississippi, USA. Forest Ecology and Manage-ment 222 (1): 202-210. - doi: 10.1016/j.foreco.2005.09.029

Martin E, Duke J, Pelkki M, Clausen E, Carrier D(2010). Sweetgum (Liquidambar styraciflua L.):extraction of shikimic acid coupled to diluteacid pretreatment. Applied Biochemistry andBiotechnology 162 (6): 1660-1668. - doi: 10.1007/s12010-010-8947-7

Mc Nabb K, VanderSchaaf C (2005). Growth ofgraded sweetgum 3 years after root and shootpruning. New Forests 29 (3): 313-320. - doi:10.1007/s11056-004-5654-7

McConnell TE, Shi SQ (2011). Partially hydrolyzingsouthern hardwoods: possibilities for biofuelsand wood composite manufacturing. ForestProducts Journal 61 (3): 235-239. - doi: 10.13073/0015-7473-61.3.235

Meadows JS, Stanturf JA (1997). Silvicultural sys-tems for southern bottomland hardwood fo-rests. Forest Ecology and Management 90 (2-3): 127-140. - doi: 10.1016/S0378-1127(96)03898-4

Merkle S, Cunningham M (2011). Southern hard-wood varietal forestry: a new approach toshort-rotation woody crops for biomass ener-gy. Journal of Forestry 109 (1): 7-14. [online]URL: http://www.ingentaconnect.com/content/saf/jof/2011/00000109/00000001/art00004

Mitchell R, Zutter B, Green T, Perry M, Gjerstad D(1993). Spatial and temporal variation in com-petitive effects on soil moisture and pineresponse. Ecological Applications 3 (1): 167-174.- doi: 10.2307/1941799

Nelson LE, Switzer GL (1990). Sweetgum half-sibseed source response to nitrogen and phos-phorus fertilization in Mississippi. Soil ScienceSociety of America Journal 54 (3): 871-878. -doi: 10.2136/sssaj1990.03615995005400030043x

Nelson LE, Switzer GL (1992). Response of nine-

year-old plantation sweetgum to nitrogen fer-tilization in Mississippi. Southern Journal ofApplied Forestry 16 (3): 146-150. [online] URL:http://www.ingentaconnect.com/content/saf/sjaf/1992/00000016/00000003/art00010

Nelson LE, Switzer GL, Shelton MG (1995). Abo-veground net primary productivity and nutrientcontent of fertilized plantation sweetgum. SoilScience Society of America Journal 59 (3): 925-932. - doi: 10.2136/sssaj1995.03615995005900030043x

Nelson L, Ezell A, Yeiser J (2006). Imazapyr andtriclopyr tank mixtures for basal bark control ofwoody brush in the southeastern United Sta-tes. New Forests 31 (2): 173-183. - doi: 10.1007/s11056-005-0925-5

Nikolaeva MG (1969). Physiology of deep dor-mancy in seeds. Izdatel’stvo Nauka, Leningrad,Russia, pp. 220.

Norby RJ, Iversen CM (2006). Nitrogen uptake,distribution, turnover, and efficiency of use in aCO2-enriched sweetgum forest. Ecology 87 (1):5-14. - doi: 10.1890/04-1950

Ocsel H, Teke Z, Sacar M, Kabay B, Duzcan SE,Kara IG (2012). Effects of oriental sweet gumstorax on porcine wound healing. Journal ofInvestigative Surgery 25 (4): 262-270. - doi:10.3109/08941939.2011.639847

Orsted AS (1863). L’Amérique centrale: recher-ches sur sa flora et sa géographie physique.Résultats d’un voyage dans les états de CostaRica et de Nicaragua exécuté pendant les an-nées 1846-1848 [Central America: research onits flora and its physical geography. Resultsfrom a trip in the states of Costa Rica andNicaragua executed during the years 1846-1848]. B. Luno par FS Muhle, Copenhagen, Den-mark, pp. 18. [in French]

Perry M, Mitchell R, Zutter B, Glover G, GjerstadD (1994). Seasonal variation in competitive ef-fect on water stress and pine responses. Cana-dian Journal of Forest Research 24 (7): 1440-1449. - doi: 10.1139/x94-186

Porcher FP (1869). Resources of the southernfields and forests, medical, economical, andagricultural. Walker, Evans and Cogswell, Rich-mond, VA, USA, pp. 733.

Rieckermann H, Goldfarb B, Cunningham M, Kel-lison R (1999). Influence of nitrogen, photope-riod, cutting type, and clone on root and shootdevelopment of rooted stem cuttings of sweet-gum. New Forests 18 (3): 231-244. - doi: 10.1023/A:1006621330099

Rink G, Dell T, Switzer G, Bonner F (1979). Use ofthe Weibull function to quantify sweetgum ger-mination data. Silvae Genetica 28 (1): 9-12.[online] URL: http://silvaegenetica.com/fileadmin/content/dokument/archiv/silvaegenetica/28_1979/28-1-9.pdf

Ruiz-Sanchez E, Ornelas JF (2014). Phylogeogra-phy of Liquidambar styraciflua (Altingiaceae) inMesoamerica: survivors of a Neogene wide-spread temperate forest (or cloud forest) inNorth America? Ecology and Evolution 4 (4):311-328. - doi: 10.1002/ece3.938

Sannigrahi P, Hu F, Pu Y, Ragauskas A (2012). Anovel oxidative pretreatment of loblolly pine,sweetgum, and miscanthus by ozone. Journalof Wood Chemistry and Technology 32 (4): 361-375. - doi: 10.1080/02773813.2012.698691

Sassner P, Galbe M, Zacchi G (2008). Techno-eco-

nomic evaluation of bioethanol productionfrom three different lignocellulosic materials.Biomass and Bioenergy 32 (5): 422-430. - doi:10.1016/j.biombioe.2007.10.014

Scott DA, Burger JA, Kaczmarek DJ, Kane MB(2004). Growth and nutrition response ofyoung sweetgum plantations to repeated nitro-gen fertilization on two site types. Biomass andBioenergy 27 (4): 313-325. - doi: 10.1016/j.biombioe.2004.02.003

Shmulsky R, Saucier C, Howard I (2008). Com-posite effect of bolt-laminated sweetgum andmixed hardwood billets. Journal of Bridge Engi-neering 13 (5): 547-549. - doi: 10.1061/(ASCE)1084-0702(2008)13:5(547)

Shmulsky R, Shi S (2008). Development of novelindustrial laminated planks from sweetgumlumber. Journal of Bridge Engineering 13 (1):64-66. - doi: 10.1061/(ASCE)1084-0702(2008)13:1(64)

Sommer HE, Brown CL (1980). Notes: embryoge-nesis in tissue cultures of sweetgum. Forest Sci-ence 26 (2): 257-260. [online] URL: http://www.ingentaconnect.com/content/saf/fs/1980/00000026/00000002/art00014

Sova M (2012). Antioxidant and antimicrobialactivities of cinnamic acid derivatives. Mini Re-views in Medicinal Chemistry 12 (8): 749-767. -doi: 10.2174/138955712801264792

Speck FG (1941). A list of plant curatives obtai-ned from the Houma Indians of Louisiana. Pri-mitive Man 14 (4): 49-73. - doi: 10.2307/3316460

Sullivan J, Lagrimini LM (1993). Transformationof Liquidambar styraciflua using Agrobacteriumtumefaciens. Plant Cell Reports 12 (6): 303-306. -doi: 10.1007/BF00237423

Sutter E, Barker P (1985). In vitro propagation ofmature Liquidambar styraciflua. Plant Cell, Tis-sue and Organ Culture 5 (1): 13-21. - doi: 10.1007/BF00033565

TMS (2010). 1st quarter 2010. Timber Mart-SouthMarket News Quarterly, vol. 15, no. 1.

TMS (2014). 1st quarter 2014. Timber Mart-SouthMarket News Quarterly, vol. 19, no. 1, pp. 52.[online] URL: http://www.timbermart-south.com/pdf/1Q2014news.pdf

Uemura K (1983). Late Neogene Liquidambar(Hamamelidaceae) from the southern part ofnortheast Honshu, Japan. Memoirs of the Na-tional Science Museum 16: 25-36.

Wang H, Srinivasan R, Yu F, Steele P, Li Q,Mitchell B, Samala A (2012). Effect of acid,steam explosion, and size reduction pretreat-ments on bio-oil production from sweetgum,switchgrass, and corn stover. Applied Bioche-mistry and Biotechnology 167 (2): 285-297. - doi:10.1007/s12010-012-9678-8

Wendling I, Brondani G, Dutra L, Hansel F (2010).Mini-cuttings technique: a new ex vitro methodfor clonal propagation of sweetgum. New Fo-rests 39 (3): 343-353. - doi: 10.1007/s11056-009-9175-2

Wenger KF (1953). The sprouting of sweetgum inrelation to season of cutting and carbohydratecontent. Plant Physiology 28 (1): 35-48. - doi:10.1104/pp.28.1.35

Wetzstein HY, Sommer HE (1982). Leaf anatomyof tissue-cultured Liquidambar styraciflua (Ha-mamelidaceae) during acclimatization. Ameri-can Journal of Botany 69 (10): 1579-1586. - doi:10.2307/2442913

726 iForest 8: 719-727

iFor

est

– B

ioge

osci

ence

s an

d Fo

rest

ry

Sweetgum: a new look

Williams JW, Shuman BN, Webb T III, Bartlein PJ,Leduc PL (2004). Late-Quaternary vegetationdynamics in North America: scaling from taxato biomes. Ecological Monographs 74 (2): 309-334. - doi: 10.1890/02-4045

Wolfe JA (1985). Distribution of major vegeta-tional types during the Tertiary. GeophysicalMonograph Series 32: 357-375. [online] URL:http://onlinelibrary.wiley.com/doi/10.1029/GM032p0357/summary

Wright J, Cunningham M (2008). Sweetgumplantations for sawtimber, energy, pulp, and

other uses. Forest Landowners 67 (3): 26-28.Wright HJ (1981). Vegetation east of the Rocky

Mountains 18.000 years ago. Quaternary Re-search 15 (2): 113-125. - doi: 10.1016/0033-5894(81)90099-5

Wu C, Dixon G, Muench S, Sandberg C (1983).The use of glyphosate for pine release in theMidsouth. Proceedings of the Southern WeedScience Society 36: 230-234.

Wyman CE, Spindler DD, Grohmann K (1992).Simultaneous saccharification and fermenta-tion of several lignocellulosic feedstocks to fuel

ethanol. Biomass and Bioenergy 3 (5): 301-307. -doi: 10.1016/0961-9534(92)90001-7

Yang B, Wyman CE (2008). Pretreatment: thekey to unlocking low- cost cellulosic ethanol.Biofuels, Bioproducts and Biorefining 2 (1): 26-40. - doi: 10.1002/bbb.49

Zhao X, Cheng K, Liu D (2009). Organosolv pre-treatment of lignocellulosic biomass for enzy-matic hydrolysis. Applied Microbiology and Bio-technology 82 (5): 815-827. - doi: 10.1007/s00253-009-1883-1

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