NewPhytologist Commentary Forum 341

concept of stratification thermal time allowed the dormancyloss kinetics at different chilling temperatures to be con-veniently described on a single thermal time scale. By furthercharacterizing the change in light sensitivity with a secondthreshold distribution that can shift in response to accu-mulated stratification thermal time (Fig. 2), the responseof the entire seed population to any light level after anystratification temperature and duration might be readilymodeied using only a few parameters (Figs 1 and 3). Further,as has been argued previously (Bradford, 1995, 2002; Allen& Meyer, 1998), the ability of these models to closely matchactual seed behavior suggests that they have biological sig-nificance, rather than merely empirical utility. Understandingseed dormancy and its alleviation by environmental signalsis equivalent to understanding the physiological, biochemicaland molecular bases of sensitivity distributions and howthese are shifted in response to both external and internalsignals. By combining quantitative mathematical models thatcan characterize seed dormancy states with modern geneticand molecular techniques such as quantitative trait locusidentification (Alonso-Blanco etaL, 2003) and microarrayanalyses of gene expression responses to environmental signals(Vamauchi etaL, 2004), we can envision a path to decipheringhow seed populations make lite and death decisions aboutwhen or whether to germinate.

KentJ. BradfordDepartment of Vegetable Crops, One Shields Avenue,

University of California. Davis, CA 95616, USA(tel+1 530 752 6087; fax +1 530 754 7222;

email kjbradford@ucdavis.edu)

Bradford KJ. 1995. Water relations In seed germination. In: Kigel, J;Galili, G, eds. Seed Development and Germination. New York, USA;Marcel Dekker, 351-396.

Bratiford KJ. 1996. Population-based models describing seeddormancy behaviour: implications for experimental design andinterpretation. In: Lang, GA, ed. Plant Dormancy: PhysiologyBiochemistry, and Molecular Biology. Wallingford, UK: CABIPublishing, 313-339.

Bradford KJ. 2002. Applications of hydrothermal time to quantifyingand modeling seed germination and dormancy. Weed Science 50:248-260.

Christensen M, Meyer SE, Allen P. 1996. A hydrothermal timemodel of seed after-ripening in Bromus tectorum L, Seed ScienceResearchS: 155-163.

Finch-Savage WE. 2004. The use of population-based thresholdmodels to describe and predict the effects of seedbed environmenton germination and seedling emergence of crops. In: Benech-Arnold, RL, Sanchez, RA, eds. Handbook of Seed Physiology: Applica-tions to Agriculture. New York, USA: Haworth Press, 51 - 96.

Rowse HR, Finch-Savage WE. 2003. Hydrothermal thresholdmodels can describe the germination response of carrot (Dauctiscarota) and onion (Allium cepa) .seed populations across bothsub- and supra-optimal temperatures. New Phytologist 158: 101-108.

Steadman KJ, Pritchard HW. 2004. Germination o^ Aesculushippociistitnum seed.s following cold-induced dormancy loss can bedescribed in relation co a temperature-dependent reduction in basetemperature (7j ) and chermal time, Neiv Plrytotogist 161: 415—42').

VanDerWoude WJ. 1985. A dimeric mechanism tor the action of phy-tochrome: evidence from photothermal interactions in lettuce seedgermination. Photochemistry and PhotohioUigy 42: 655—661.

Yamauchi Y, Ogawa M, Kuwahara S, Hanada A, Kamiya Y,YamaguchJ S. 2004. Activation ofgibberellin biosynthe.sis andresponse pathways by low temperature during imbibition ofArahidopsis thaliana seeds. Plant CAl\6i .367-378.

Key words: seed germination, threshold models, Polygonum avicuiare,dormancy, germination ecology.

References

Allen PS, 2003. When and how many? Hydrothermal models andprediction of seed germination. New Phytologist 158: 1-9.

Allen PS, Meyer SE. 1998. Ecological aspects of seed dormancy loss.Seed Science Research 8:183-191.

Alonso-BIanco C, Bentsink L, Hanhart CJ, Blankestijn-de Vries H,Koornneef M. 2003. Analysis of natural allelic variation at seeddormancy loci of Arahidopsis thaliana. Genetics 164: 711-729.

Alvarado V, Bradford KJ. 2002, A hydrothermal time model explainsthe cardinal temperatures for seed germination. Plant. CellandEnvironment!'): 1061-1069.

Alvarado V, Bradford KJ. 2005. Hydrothermal time analysis of seeddormancy in irue (botanical) potato seeds. Seed Science Research.(In pre.ss).

Batlla D, Benech-Arnold RL. 2004. A predictive model for dormancyloss in Polygonum avicuiare L. seeds based on changes in populationhydrotime parameters. Seed Science Research 14: 277-286.

Batlla D, Benech-Arnold RL. 2005. Changes in the light sensitivityot Polygonum avicuiare buried seeds in relation to cold-induceddormancy loss: development ofa predictive model. New Phytologist165:445-452.

Benech-Arnold RL, Sindiez RA. Forcella F, Kruk BC, Ghersa CM.2000. Environmental control of dormancy in weed seed banks insoil, field Crops Research 67: 105-122.

Understanding a flammableplanet - climate, fire andglobal vegetation patterns

The extraordinary intelleaual achievement ofthe 19th cetituryGerman botanist Andreas Schimper was his book PLant-Geography upon a Physiobgical Basis (Schimper. 1903).Through sheer force of imagination and by drawing onnumerous written observations from around the world, hedescribed the correspondence between global climate andvegetation zones. Such 19th century global ecological syntheseswere superseded in the 20th century because attention wasdirected to specific questions using the hypothetico-deductiveapproach. However, growing concern over global environ-mental change and the advent of powerful space-age andcomputer technologies has seen the pendulum swing awayfrom narrowly focused analyses back towards global synthesis.

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r

Commentary

'A world without fire has fundamentally different

forest zones than occur on our real, highly fiammahle

planet'

Rather than being based on observation and induction, the21st century syntheses are powered by models that enablerhe mechanistic integration of data collected across spatialscales and disciplinary boundaries. The predictions possibleare sufficiently accurate to be testable against independentoKservarions and meta-analyses of existing datasets. Thepaper in this issue by Bond et al. (pp. 525-538) is anexetnplar of this intellectual moment. They have providedthe first evidence that global vegetation patterns are shapedby landscape fire. Their study is based on the disciplinedmarshalling of relevant field and satellite observationsand strategic application of existing mechanistic DynamicGlobal Vegetation models (DGVMs) based upon physiol-ogical processes. Their approach demonstrates a new wayof ecological thinking that provides profound insightsinto global ecological processes and the evolution of thebiosphere.

What would a world without fire be like?

Despite the feet that satellite sensors were not originallydesigned to map landscape fire, an unexpected spin-ofF ofglobal remote sensing was the demonstration of the ubiquityof landscape fire on every vegetated continent (Cochrane,2003; Justice et aL, 2003). The effect of landscape fire onglobal vegetation patterns is implicit in several DGVMsbecause they include 'fire modules' that introduced frequentdisturbances to modelled vegetation patterns and processes.Bond el al. (2005) asked a beguilingly simple question -what happens if these fire modules are switched off? Theyfound that a world without fire has fundamentally differenttore.st zones than occur on our real, highly flammableplanet. Without fire, the extent of forests with >80% tretcover doubled from 26.9% to 56.4% of the vegetated surfaceof the Earth. Further, more than half (52.3%) of the currentglobal distribution of C^ grasslands was transformed toangios perm-dominated forest. Of the 4 1 % of C, grasslandthat was replaced by forests, 53% were dominated bygymnosperms, 34% by angiosperms and 13% by a mixtureof both these taxa. The analysis of Bond et ai (2005) wasunable to capture postfire secondary successional sequenceswithin their broad v^ctation formations. If they had doneso, there is no doubt they would have provided even morestarding evidence of landscape fire upsetting the vegetation-

NewPhytoiogist

climate equilibrium. This would be particularly so forpyrophytic forests such as those dominated by Eucalyptus inAustralia and Pinus in the northern hemisphere.

Producing a global perspective

Landscape fire has not been a central concern in ecology.Indeed, only in the past decade have books been publishedoutlining the general principles of fite ecology (Whehui, 1995;Bond 8; van W i ^ n , 1996); most knowlec^e has been r^onallyfocused. Fire ecologists working in specific fiammable biotas,such as tropical savannas, mediterranean shrublands andpyrophytic forests, have long appreciated that landscape firedecouples the tight interrelationship between vegetation andclimate: the achievement of Bond et al. (2005) has been tounite these disparate finding into a single global perspective.

A common inference from regional landscape-scalestudies has been that the juxtaposition of patches of forestswithin a highly flammable matrix is the work of recurrentfires (Fig. 1). Bond et al. (2005) argue that such patternsrefiect the evolutionary divergence of fire-adapted and fire-tolcrant taxa, a process chat has occurred independently onall vegetated continents. Evidence for this evolutionary dichoto-misation is largely circumstantial, based mainly on fieldcorrelarion and fire exclusion. The recent study by Fenshametai (2003) is a notable exception. They demonstrated thatrecurrent fires caused the difTerential survival of evergreentree species characteristic of fire-prone savannas comparedwith evergreen tree species from 'rainforests' on fire-protectedsites (Fig. 2). However, the underlying mechanism that causesthis differential response remains unexplained.

Surviving fire

There are very few examples that demonstrate the evolutionoi specific features that enable plants to survive fire. Burrows(2002) showed that epicormic buds were situated on theinside rather than the outside of the cambium in some south-east Australian eucalypts and related taxa. Burrows (2002)interpreted this unique anatomical arrangement as anadaptation to recover vegetativeiy following fire damage.Research by Prior et al. (2003, 2004) has pointed to whole-plant differences between fire-tolerant and fite-sensitivc taxa.Eucalypts that dominate vast tracts of fire-prone savannawere found to have phorosynthetically less efficient leavesand slower stem growth rates than rainforest tree species chatare restricted to small fire-protected sites (Fig. 1). Such wholeplatit differences associated with fire tolerance may accountfor some of the variation between climate parameters andleaf functional attributes documented by Wright et al (2004).The physiological basis for fire tolerance, particularly whole-tree carbon allocation, is a fertile area for research.

WTiereas some recent studies have provided some micro-evolutionary insights into plant strategies to survive fire (e.g.

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NewPhytoiogist Commentary Forum 343

Fig. 1 Savanna fire burning around a topographically fire-protected patch of rainforest. Such a pattern of 'islands' of fire-sensitive vegetationin a 'sea' of fire-tolerant vegetation is evidence that landscape burning disturbs the tight interrelationship between vegetation type andclimate. The juxtaposition of floras with contrasting fire tolerances is also interpreted as representing the evolutionary dichotomisation drivenby landscape burning. However, there are few hard data about physiological and morphological bases of fire tolerance or how these traitsevolved. (Photographer: David Hancock).

Schwilk & Ackerly, 2001), the deeper question o f t h econvergent evolution of fire tolerance betvt'een continentalfloras remains open. Interrogation oi the fossil record todetermine when flammable vegetation evolved is stymiedby the ab.sencc of unambiguous morphological features tosurvive fire. An alternative approach to advance the questionofthe evolution of flatnmable floras may be sought by usingmolecular phytogenies to trace the evolution of unambigu-ously fire-adaptive traits such as transposed epicormic budstrands (Burrows, 2002).

Past climates and the impact of people

I'akeoccology has proved that landscape fire occurred formillions of years before the advent of fire-wielding hominids.Bond etaL (2005) suggest falling CO2 levels may havestimulated the development of fire-prone C^ grassland that,in turn, greatly increased the frequency of landscape fire.Keeley and Rundel (2003) argue that the development ofmonsoon climates may be as an important driver as lowatmospheric concentrations of CO2. This is because the dry

seasons characteristic of tnonsoon climates are concluded byintense convective storm activity that produce high densitiesof lightning strikes. The integration of global lightningactivity (Fig. 3) in DGVMs would provide far more realisticprobability distributions of ignitions than the unrealisticassumption that ignition is not limiting. It would alsobe instructive to discover the degree of congruence betweenpredicted 'hot spots' of natural fire activity and the diversityof fire adapted biotas. Such an anaiysis may help advance thetiming ofthe evolution of flammable biotas on Earth and togauge the evolutionary effect of anthropogenic burning.

Although it is accepted that indigenous people havemoulded landscapes through the use of fire, understandingthe extent of this impact is difficult given uncertainty aboutthe background rate of fire activity from lightning. Forexample, in North American forests it is widely regardedthat the impact of Native American burning was negligiblebecause stand-replacing fires are under the control of long-termdrought cydes (e.g. Grissino-Mayer etaL, 2004). Conversely,it is widely assumed that Aboriginal landscape burningcaused a continental-wide transformation of the Australian

© New Phytologist (2005) www.newphytologist.org New Phytologist (200S) 165: 341-345

344 Forum CommentaryNewPhytoiogist

I(0

ao

60

40

20

n

NS

•

' • • • *

" • • • • • • * ^

" • - • • • • • • • i

>

• • • • ^

Number of firesFig. 2 Declining mean percentage (± sf) of the survival ofresprouting species in response to five successive fires in apreviously fire-protected savanna fragment in north-eastQueensland. Closed circles: rainforest species; open circles; savannaspecies. The physiological and morphological base of the differentialsurvival betvi/een rain forest and savanna species to recurrent fireremains to be elucidated. Significance of Mann-Whitney t/-tests arewhere: NS. P > 0.05; •*P<0 .01 ; • • • P < 0.001. (Modified fromFensham et al. (2003) with additional data from R. J. Fensham,unpublished).

flora and fauna (Bowman, 1998; Miller etoL, 1999). Follow-ing the same logic as Bond etai (2005), a comparison ofacrual global vegetation patterns with those produced underlightning ignitions alone would help resolve the effect of

anthropogenic ignitions, both historically ajid prehistori-cally, on changing global vegetation patterns (Fig. 3). Thepositive feedback between smoke plumes and cloud-to-ground [ightning strikes (Lyons etaL^ 1998), however, mayconfound a simple causal relationship between the apparentconcordance of the spatial distribution of current observa-tions of high lightning aaivity and fire-tolerant floras.

There can be no escaping the Increasing global impactof contemporary anthropogenic landscape burning. Theincreased spatial scale of landscape burning in fire-proneenvironments reflects failed attempts to totally suppress fires(e.g. Grissino-Mayer etaL 2004) or the breakdown of skilfulindigenous fire management (e.g. Bowman etaL 2004).Fire is being used indiscriminately to clear tropical rainforests. An ensemble of positive feedbacks greatly increa.ses therisk of subsequent fires above the extremely low backgroundrate (Gxhrane etai, 1999; Cochrane, 2003). Recurrent burningcan therefore trigger a landscape-level transformation oftropical rainforests into flammable scrub and savanna.The transformation of tropical rain forest by fire providesinsights into die evolution and spread of flammable florasworldwide.

Perspectives

Clearly, much remains to be done to bring fire to the samefooting as climate variables as a factor driving biogeographicpatterns and biogeochemical processes. Discovering the

-150 -120 -90

• - . . ' • ••• -SO -:30 0 30 G O - • \ • :

Fig. 3 Global lightning activity (number of flashes per km^ per year). These data include both cloud-to-doud and cloud-to-ground strikes.There is a general concordance between high lightning activity in seasonally dry climates and those areas identified by Bond e( al- (2005) assusceptible to vegetation change when fire is 'switched off' in Dynamic Global Vegetation Models. Further, there appears to be associationbetween high lightning activity and regions with fire-adapted floras such as the Florida Peninsula, California coast, southern Africa andnorthern Australia. The v1,0 gridded satellite lightning data were produced by the NASA LiS/OTD Science Team (Principal Investigator, Dr H.J. Christian, NASA/Marshall Space Flight Center) and are available from the Global Hydrology Resource Center (http://ghrc.msfc.nasa.gov).

Neu'P/tyti>logist{200'j) 165:341-345 www.newphytologist.org © New Pl^ytologist {2005)

NewPhytoiogist Commentary Forum 345

causes of tlie evolution of flammable vegetation is of greatimportance in understanding and managing landscapefire, particularly given the accelerating rate of globalenvironmental change. Of prime interest are the effects ofclimatic variation, atmospheric C O , concentrations andprehistoric anthropogenic fire use relative to the backgroundrate of lightning ignitions. Bond et al. (2005) provide a vitaljolt in developing such global perspective and evolutionarythinking about landscape fire.

David Bowman

Key Centre for Tropical Wildlife Management,Charles Darwin University, Darwin NT 0909, Australia

(tel -f61 8 89467762; fax +61 8 89467088;email david.bowman@cdu.edu.au)

References

Bond WJ, van Wilgen BW. 1996. Fire and Plants. London, UK:Chapman & Hall.

Bond W], Woodward FI, Midgley GF. 2004. The global distributionof etosyNterns in a world without fire. New Phytoiogist 165: 525-538.

Bowman DMJS. 1998. The impact of Aboriginal landscape burningon [he Australian biota. New Phytoiogist 140: 385-410.

Bowman DMJS, Walsh A, Prior LD. 2004. landscape analysis ofAboriginal fire management in Central Arnhem Land, nortbAustralia, foumat of Biogeography 31: 207-223-

Burrows GE. 2002. Epicormic strand structure in Angophora,Eucalyptus, .ind Lophostemon (Myrtaceae) — implications forfire resistance and recovery. New Phytoiogist 153: 111-131.

Cochrane MA. 2003. Fire science for rainforests. Nature42\: 913-919.Cochrane MA, Afencar A, Schuize MD, Souza CM, Nepstad DC,

Lefebvre P, Davidson EA. 1999. Positive Feedbacks in the FireDynamic of Closed Canopy Tropical Forests. Science 2S4: 1832-1835.

Fensham RJ, Fairfax RJ, Buder DW, Bowman DMJS. 2003. Effectsof fire and drought in a tropical eucalypt savanna colonized by raintorests. Journal of Biogeography 30: 1405-1414.

Grissino-Mayer HD, Romme WH, Floyd ML, Hanna DD. 2004.Climatic and buman influences on fire regimes of the southern SanJuan Mountains, Colorado. USA. EcologyS5: 1708-1724.

Justice CO, Smith R, Gill AM, Csiszar L 2003. A review of currentspace-based fire monitoring in Australia and the GOFC/GOLDprogram for international coordination. International Journal ofmidland Eire \2: 247-258.

Keeley JE, Rundel PW. 2003. Evolution of CAM and C^ carbon-concentrating mechanisms. International Journal of Plant Sciences 164:555-577.

Lyons WA, Nelson TE, Williams ER, Cramer JA, Turner TR. 1998.Enhanced positive cloud-to-ground lightning in thunderstormsingesting smoke from fires. Science2'&2: 77-80.

Miller GH, Magee JW, Johnson BJ, Fogel ML, Spooner NA,McCuJIoch MX, Ayiiffe LK. 1999. Pleistocene extinaion ofGenyornis newtoni: Human impact on the Australian megafauna.5cw;fc283: 205-208.

Prior LD, Eamus D, Bowman DMJS. 2003. Leaf attributes in theseasonally dry tropics - a comparison of four habitats in northernAustralia. Functional Ecology \7: 504-515.

I'rior LD, Eamus D, Bowman DMJS. 2004. Tree growth rates innorth Australian savanna habitats: seasonal patterns and correlationswith leaf attributes. Australian Journal of Botany ^2: 303-314.

Schimper AFW. 1903. Plaiit-Geographyraphy Upon a Physiological Basis.Oxford, UK: Clarendon Press.

Schwilk DW, Ackerly DD. 2001. Flammability and serotiny asstrategies: correlated evolution in pines. Oileos9A: 326-336.

Whelan RJ. 1995. fAe &o&^ o/FrVr. Cambridge, UK: CambridgeUniversity Press.

Wright IJ, ReicK PB, Westoby M, Ackerty DD, Baruch Z, Bongers F,Cavender-Bares J, Cbapin FS, Corneiissen JHC, Diemer M.Hexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, l^mont BB,Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets t),Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI,Roumet C, Thomas SC, Tjoelker MG, Veneklaas E, Villar R.2004. The world-wide leaf economics spectrum. Nature A2S:821-827.

Keywords: biogeography, fire ecology, fire tolerance, evolution, globalecology, global vegetation patterns.

Are liverworts imitatingmycorrhizas?

Among the similarities between the liverworts and vascularplants (Tracheophyta; Fig. 1), the mycorrhizal symbiosis isperhaps the least expeaed. Vascular plants associate intimatelywith soil fungi: a limited colonization of roots by the fungusbtiilds a dual organ, che mycorrhiza, that allows nutrientexchanges. The fungus exploits plant photosynthates andprovides mineral resources for its host. However, nonvascularplants, such as liverworts, also form various associations withfungi, imitating the mycorrhizas: Russell & Bulman report onnew advances in our understanding of this symbiosis onpp. 567-579 in this issue.

Background

Liverworts (6000-8000 species) belong to the (presumably)paraphyletic Bryophyta (Fig. 1) and consist of a reducedsporophyte growmg on a frce-Hvmg gametophyte. Althoughsome debate still exists (Goffinet, 2000; Nishiyama etaL, 2004),most phylogenies place liverworts as the most basal extantland plants (Dombrovska & Qiu, 2004; Groth-Malonek etai,2004). Liverworts are classically divided into two subclades(Fig. 1 and Table 1) whose monophyly is now questioned(He-Nygren etai, 2004). Jungermanniopsida mostly havesmall shoots with leafy expansions, but some show a simplethalloid organization; Marchandopsida are thalloid, and somehave a complex structure, including a lower storage parenchyma,a green aerenchyma with stomata-like pores and sometimes ahydrophobic cuticle. In addition, some Jungermanniales havesubterranean axes bearing rhizoids, with positive gravitropismreminiscent of roots (DuclKtt etaL, 1991). Among the sitnilaritiesbetween liverworts and tracheophytes, the mycorrhizal symbitwisis certainly the least expected one.

© New Phytoiogist {2005) www.newphytologist.org New Phytoiogist i2005) 165: 343-349