Global angiosperm family richness revisited: linking ecology and evolution to climate

14 Pages·2011·1.35 MB·English

JournalofBiogeography(J.Biogeogr.)(2011)38,1253–1266
Global angiosperm family richness
ORIGINAL
ARTICLE revisited: linking ecology and evolution
to climate
Bradford A. Hawkins1*, Miguel A´. Rodrı´guez2 and Stephen G. Weller1
1DepartmentofEcology&Evolutionary ABSTRACT
Biology,UniversityofCalifornia,Irvine,CA
Aim The global richness gradient of angiosperm families is correlated with
92697,USA,2DepartmentofEcology,
currentclimate,andithasbeenclaimedthathistoricalprocessesarenotnecessary
UniversityofAlcala´,Alcala´deHenares,28871
to understand patterns of plant family richness. This claim has drawn criticism,
Spain
and there have been doubts about the quality of the data used to quantify the
pattern. We revisit this issue using the Angiosperm Phylogeny Group (APG) III
classification and revised range maps, and we incorporate an evolutionary
variable, family age, to explore covariation between evolution and ecology and
their links to climate via the tropical conservatism hypothesis (TCH).
Location Global.
Methods The richness pattern for 408 families was derived from range maps,
andfamilyageswerederivedfromadatedangiospermphylogeny.Patternswere
generated for all families, 143 families composed of trees, and 149 families
composedofherbs.Wealsoexaminedfamilyrangesizepatternstotesttheextent
to which extratropical floras are nested subsets of tropical floras. Ordinary least
squares (OLS) multiple and partial regressions were used to generate climate
modelsforrichness,meanrangesizeandmeanageforeachplantdatasetandto
evaluatethecovariationbetweencontemporaryclimateandcladeageascorrelates
of family richness.
Results Weconfirmedthestrongassociationbetweencontemporaryclimateand
family richness. Age patterns predicted by TCH were also found for families
comprisingtrees.Therichnessofherbaceousfamilies,incontrast,wascorrelated
withclimatebuttheagepatternwasnotaspredictedbyTCH.Florasincoldand
dry areas are strongly nested within richer tropical floras.
Main conclusions Phylogenetic niche conservatism at the family level offers a
likelyexplanationfortheglobaldiversitygradientoftrees,butnotfornon-desert
herbs, probably because of the faster evolutionary rates for herbs and less
constrained evolutionary responses to climate change. Thus, it appears that
multiple processes account for the overall angiosperm family gradient. Our
analysis also demonstrates that even very strong associations of taxon richness
and climate do not preclude evolutionary processes, as has been widely argued,
and that climatic and evolutionary hypotheses for richness gradients are not
mutually exclusive.
Keywords
*Correspondence:BradfordA.Hawkins, Angiosperms, climate–richness relationships, diversity gradients, family rich-
DepartmentofEcology&EvolutionaryBiology,
ness, global diversity, niche conservatism, plant richness, range size, tropical
UniversityofCalifornia,Irvine,CA92697,USA.
E-mail:[email protected] conservatism hypothesis.
ª2011BlackwellPublishingLtd http://wileyonlinelibrary.com/journal/jbi 1253
doi:10.1111/j.1365-2699.2011.02490.x
B. A.Hawkins etal.
initially evolved, due to phylogenetic niche conservatism
INTRODUCTION
limiting the number of subclades that are able to break into
Broad-scale richness gradients are closely associated with novel environments as well as to longer residence times in
contemporary climate (Wright etal., 1993; Hawkins etal., ancestral climates (Ricklefs, 2006). If the clade (such as
2003; Field etal., 2009). As part of the evidence for climatic angiosperms) arose in tropical climates, not only will it be
control of taxonomic richness, Francis & Currie (2003) more species rich in the tropics, but tropical biotas will
generated models of angiosperm family richness including generally contain more older, ancestral subclades constrained
energyandwatervariablesthataccountedformorethan80% by niche conservatism, whereas non-tropical biotas will
oftheglobalspatialvariation,fromwhichtheyconcludedthat comprise members of more recent and evolutionarily derived
processesrelatedtotheevolutionaryhistorywerenotnecessary subclades that have undergone niche evolution (which has
to understandcurrent plantrichness patterns. then led to new radiations outside the tropics). Phylogenetic
Qian&Ricklefs(2004)thenrespondedtoFrancis&Currie patterns consistent with this prediction have recently been
(2003), criticizing them on numerous grounds including the documented for a number of animal groups (Hawkins etal.,
quality of the data and the interpretation of the statistical 2005, 2006, 2007a; Wiens etal., 2006, 2009; Hawkins &
models. First, they argued that family concepts in plants are DeVries, 2009; Hawkins, 2010). For plants, Donoghue (2008)
fluid and arbitrary, and the classification used by Francis & explicitly argued that the explanation offered by Latham &
Currie(2003)wasoutofdateaswellasmissingmanyfamilies Ricklefs (1993a) and Qian & Ricklefs (2004) can account for
[e.g. the analysis included 306 families, whereas APG II the spatial distribution of plant richness, driven by tropical
(Angiosperm Phylogeny Group, 2003) listed 397 families]. niche conservatism and the difficulty of evolving cold toler-
Further,theyclaimedthatthemapsusedbyFrancis&Currie ance.
(2003),takenfromHeywood(1993),containedenougherrors In this paper we revisit the debate concerning ecological
thattherichnesspatternsandenvironmentalassociationswere versus evolutionary explanations for angiosperm richness
subjecttodoubt.Theyalsoarguedthatcontrollingforclimate gradients, updating the family classification and range maps
before examining residual geographically based variation and using phylogenetically based information on the evolu-
minimized the observed differences between biogeographical tionaryhistoryofplantfamiliestoexaminehowclimatemight
regions, which in the opinion of Qian & Ricklefs (2004) driveplantdiversity.Weaddressfourspecificquestions.First,
obscured substantial historical effects. Finally, and most are the results of Francis & Currie (2003) robust to recent
importantly, Qian & Ricklefs (2004) argued that ecological taxonomicchangesinangiospermfamiliesandtheinclusionof
and evolutionary processes leading to correlations between allcurrentlyrecognizedfamilies?Second,doesclimateoperate
climate and richness are strongly collinear, since angiosperms on the angiosperm diversity gradient as a selective agent
probably have a tropical origin (Crane & Lidgard, 1989) and generating a replacement of plant families moving from the
havehadtoevolvefreezingtolerancetocolonizeareaswithlow tropics to the extra-tropics, or as a filter selectively excluding
temperatures,whichonlyasubsetofcladeshasmanagedtodo families moving from warm and wet climates to cold or dry
(Ricklefs, 2005). This evolutionary legacy of low family ones, as expected when tropical niche conservatism is oper-
richness in northern latitudes thus explains why richness is ating? Third, do the floras of warm, wet tropical climates
correlated withcontemporary climate. contain older families than those of regions that have
In a reply Currie & Francis (2004) defended their conclu- undergone cooling or drying since the early Tertiary, as
sions, arguing that it was unlikely that errors in the data expectedunderTCH?Fourth,areinfluencesofecologicaland
invalidated the patterns or the statistical models generated to evolutionary processes on the richness gradient strongly
explain them, and they admitted that their analysis did not collinear? We evaluate each of these questions for all angio-
preclude the existence of historical effects. They closed the spermfamiliesandforasubsetofarborescentandherbaceous
debate by agreeing that historical processes could becollinear families considered separately. The life-history traits of trees
with contemporary climate, but that predictions from histor- andherbsdiffersubstantially,andtheyhaveverydifferentrates
ically based hypotheses are difficult to generate and test, and of molecular and phenotypic evolution (Smith & Donoghue,
theevidence for historical processesiscontradictory. 2008; Smith & Beaulieu, 2010). It is likely that the processes
The proposition by Qian & Ricklefs (2004) that climate influencing their diversification rates also differ, and compar-
influences plant taxonomic richness through the tropical isons of patterns for the two groups may shed light on
origin of angiosperms and the evolution of freezing tolerance explanations for thediversityof angiospermsasawhole.
[seealsoLatham&Ricklefs(1993a)foranearlierpresentation
of this explanation] is now referred to as the tropical
MATERIALS AND METHODS
conservatism hypothesis (TCH; Wiens & Donoghue, 2004),
which is receiving attention because it generates testable
Plant richness data
predictions about the phylogenetic structure of diversity
gradients. A number of predictions are possible, depending The global family richness pattern was derived from the 413
on underlying assumptions, but generally, any clade will be families recognized by the APG III (Angiosperm Phylogeny
richerintheclimatesmostsimilartothoseinwhichthegroup Group, 2009) classification matched to the 506 family distri-
1254 JournalofBiogeography38,1253–1266
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Angiospermfamilyrichness
bution maps from Heywood etal. (2007). When family ceae], and Misodendraceae and its sister family Schoepfiaceae
designationsinHeywoodetal.differedfromthoserecognized wereassignedtheageprovidedbyAPwebfortheformer.Noage
byAPGIII,mapswerecombinedaccordingtothetaxonomic estimates were available for Cynomoriaceae or Apodanthaceae,
information provided by APG III (Angiosperm Phylogeny andtheywereassignedtheaverageageacrossallfamilies.
Group, 2009) and the Angiosperm Phylogeny Website (AP-
web;Stevens,2001onwards).APwebwasalsousedasthemap
Environmental data
source for 13 of the 16 families that were not mapped in
Heywood etal. (2007); the remaining three families with no Our environmental models used the same data sources as
maps (Guamatelaceae, Lophiocarpaceae and Talinaceae) and Francis & Currie (2003) and included: mean annual temper-
marine families (Cymodoceaceae, Posidoniaceae and Zoster- atureandannualprecipitation(Legates&Willmott,1992;data
aceae) were excluded. Finally, although APG III includes available at http://gcmd.nasa.gov/records/GCMD_gov.noaa.
Taccaceae within Dioscoreaceae, it acknowledged its distinct ngdc.G01976.html);Priestley–Taylor’sannualpotentialevapo-
morphologicalcharacteristicsandrecentphylogeneticanalyses transpiration (PET) and Thornthwaite’s annual actual evapo-
suggesting that Taccaceae is a separate clade. Our database transpiration (AET) (Ahn & Tateishi, 1994; data available at
included this separation and comprises 408 families (see http://www.grid.unep.ch/data/data.php); and annual water
TableS1inSupporting Information). deficit (WD), computed as the difference between PET and
Patternsfortreesandherbsweregeneratedbyclassifyingthe AET.
range of growth forms of species in each family using
information taken from APweb. Families that are exclusively
Analytical protocols
or primarily trees and with no herbaceous species were
classified as ‘arborescent’ (n=143), and families that are All variables were binned in a 9300km2 global grid in a
exclusively or primarily herbaceous and contain no tree or Behrman projection from which cells comprising Antarctica
liana species were classified as ‘herbaceous’ (n=149). The andsmallislandswereexcluded.Thisgeneratedamaximumof
remaining 116 families are either entirely shrubs or lianas or 17,281 cells, although cells with <50% of landmass and cells
contain both tree and herbaceous species and were not withnoangiospermswereexcludedfromtheanalysis.Sample
analysed separately. sizesvariedslightlyamonganalysesofthevariousplantgroups
TocompareourfamilyrichnessgradienttothatofFrancis& due totheexclusion ofempty cellsfor thegroup.
Currie (2003), we converted their gridded data (provided by FollowingtheanalyticalapproachofFrancis&Currie(2003),
D.J.Currie,UniversityofOttawa)tocentroidsandintersected we used simple and multiple ordinary least squares (OLS)
them with our grid (see ‘Analytical protocols’). Cells in our regression to explore relationships between plant family rich-
grid that contained acentroid from theirgrid wereextracted, ness,meanrangesizesandmeanageswithrespecttoclimate.In
andthetwosetsofrichnessvalueswerecorrelatedagainsteach generalwefoundthatthemodelsincludingvariouscombina-
other. tions of climatic predictors explained similar amounts of
The range maps were also used to calculate range sizes for variance(allR2valueswerewithin0.10ofeachother),aslong
each family. Mean range sizes were calculated in our global astheyincludedmeasuresofbothenergyandwaterinputs.We
gridtoevaluaterelationshipsbetweenfamilyrichnesspatterns alsofoundthatthebestmodelinFrancis&Currie(2003),which
andrangesizedistributionsandpartiallyaddressthequestion includedalineartermofWDandlinearandquadratictermsof
oftheextenttowhichclimateoperatesonrichnessasafilter. PET,alsoperformedaswellinourrichnessandmeanagedataas
anyothermodelcombiningtheotherclimaticvariables,andwe
focusedonthesevariablestoreduceredundancyandfacilitate
Plant agedata
comparisonwiththeirresults.Wealsousedpartialregression
Most family ages were obtained from a dated version of the (Legendre&Legendre,1998)toexplorepatternsofcovariation
megatree of Davies etal. (2004) (available at http://www. between current climate and evolutionary processes based on
phylodiversity.net/phylomatic/davies_dated.new; accessed April multiple regression models including both climatic variables
2010)whichincludesestimatesfor377familiesinourdatabase and mean family age. Separate models were generated for all
and24additionalfamiliesthatwereabsentbutregardedbyAPG response variables with all families, arborescent families only
III (Angiosperm Phylogeny Group, 2009) as being sister or andherbaceousfamiliesonly.
polytomoustofamiliesthatwereinDaviesetal.(2004).Forthe To explore the extent to which regression models success-
remainingsevenfamilies,Ripogonaceaewasassignedtheageof fully accounted for the spatial patterns of total, tree and herb
Smilacaceae,thefamilyfromwhichitwassegregatedbyAPGII family richness, we generated spatial correlograms using
(Angiosperm Phylogeny Group, 2003), Limeaceae and Peter- Moran’s I at 27 distance classes (see Diniz-Filho etal., 2003)
manniaceaewereassignedtheaveragesoftheagesoftheirclosest andcomparedtherawautocorrelation inthedataagainstthe
ancestral and daughter families in the APG III megatree residualautocorrelationinthemodelscontainingonlyclimatic
(availableathttp://www.phylodiversity.net/phylomatic/;accessed predictors,onlyage,orboth.Non-stationarityinrelationships
April 2010) [Stegnospermataceae and Molluginaceae for Lime- between richness and environment/age precluded spatially
aceae, and Melanthiaceae and Colchicaceae for Petermannia- explicit modeling.
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B. A.Hawkins etal.
Finally, we examined patterns of compositional nestedness ofarborescentfamiliesisalmosttwiceassteepasthegradient
to quantify the extent to which composition of extra-tropical for herbaceous families (0.853 vs. 0.488 families/degree), and
cells represents a subsample of tropical cells using three treefamilyrichnessishighestinthetropicsinallpartsofthe
transects five cells wide and of variable length (Fig. S1). The world(Fig. 1b).Incontrast,therichnessofherbaceousfamilies
transectswerelongandthintofocusinterpretationofpatterns remains high as far north as 45(cid:2), and parts of the northern
on the latitudinal axis. Because geographically extensive cold temperate zone, particularly in the Nearctic, are richer than
climatesaremostlyfoundintheNorthernHemisphere,andto many areas inthetropics (Fig.1c).
make all cells comparable, the nestedness analysis used only Francis & Currie’s (2003) strongest regression model
cells in continental landmasses north of the equator. To contained potential evapotranspiration (PET )PET2) and
examine possible variation among regions arising from water deficit (WD) and explained 83.7% of the variance in
historical contingencies, separate transects were generated in family richness. The same model based on our richness data
theNew World, thewesternOldWorld, andeastern Asia. has equally strong explanatory power (Table1a). We also
Three nestedness metrics were calculated: (1) NODF found that actual evapotranspiration by itself generated a
(nestedness metric based on overlap and decreasing fill; strong model that did not require a polynomial term
Almeida-Netoetal.,2008);(2)matrixtemperature,T(Atmar (r2=0.763). Irrespective, the relationships between water,
& Patterson, 1993), reported as 100)T, and (3) a novel energy and richness identified by Francis & Currie (2003) are
metric,subsamplenestedness(SSN),calculatedasthepropor- extremely robust tothedifferences intheplant data.
tionoffamiliesfoundinalessrichcellalsofoundinapaired Climatic models for arborescent and herbaceous families
richercell.Asourfocuswasonthelatitudinalpatternoffamily differ from the overall angiosperm model, although not
replacement,cellswithineachtransectwereassignedidentical substantially (Table 1a1,2). The relatively high herb richness
longitudes. We used a spatially explicit approach, generating of the temperate zone generates a stronger negative PET2
metricsforallpossiblepairsofcellsandthenaveragingvalues coefficient and a model with somewhat weaker explanatory
within10distanceclasses.Thisallowedustoquantifylevelsof power,butbothgroupshavestrong(forherbs)toverystrong
nestedness with respect to the distance between pairs of cells (for trees)statistical relationships withenergy and water.
on a north–south axis. The first two indexes were computed Residual spatial autocorrelation in the richness gradient
with aninhado (Guimara˜es & Guimara˜es, 2006; available at after fitting the climatic models (Fig. S1) indicates that the
http://www.guimaraes.bio.br), and the third with a BASIC modelsexplainmostofthespatialpatterninthedata,butnot
programwrittenbyus(availableuponrequest).Forstatistical all. Substantial unexplained pattern remains in the smallest
evaluation the observed values for the first two indices were distance class in all three data sets, which is typical of broad-
compared against values obtained when the observed family scale analyses based on range maps due to a combination of
occurrences in cells within each transect were distributed usingfilled-inrangesandmacroclimatic predictors.However,
randomly;itwasnotpossibletogeneratenullmodelsforSSN, residual Moran’s I values >0.1 or <)0.1 are found in a
so we generated 95% confidence intervals. In this paper we numberofdistancesclassesinallthreeplantgroups,indicating
explorepatternsofcompositionalnestedness,butphylogenetic that the climate models do not explain all spatial structure
nestednessofextra-tropicalfloraswithintropicalflorasisalso across all scales, and that additional spatially structured
predictedundersomescenariosoftropicalnicheconservatism. variables are needed to account completely for the global
We willexamine this elsewhere. richness gradient.
RESULTS The globalrange sizegradient
Average family range sizes are smallest in the tropics and
The angiosperm familyrichness gradient
largest in northern latitudes and in major deserts (Fig.2a).
The pattern of family richness we obtained is as would be Further, the range size pattern is strikingly similar to the
expectedbasedonthemapofFrancis&Currie(2003)(Fig. 1), richness gradient (cf. Fig.1a), and they are tightly correlated
andthespatialrichnesspatternsarevirtuallyidentical(paired- (r=)0.978).Thus,familyrichnesscanbeconsideredalinear
cellcorrelation =0.977).Becauseourdatacomprise102more transformationofrangesizepatterns,andtheclimate–richness
families than Francis & Currie (2003), our absolute per-cell relationshipcanbeinterpreteddirectlyviatherangedynamics
estimatesareslightlyhigher(e.g.amaximumof219vs.201), ofangiospermfamilies.Becausemeanrangesizeissostrongly
despite our smaller grain (c.9300km2 vs. 35,000km2). But correlatedwithrichness,aclimate-basedregressionmodelfor
despite differences in the data sets, the shape of the global range size also has very strong explanatory power (Table1b).
gradientdocumentedbyFrancis&Currie(2003)hasremained Separate models for trees and herbs are also strong
extremely robust. (Table 1b1,2).
Although there are far fewer arborescent and herbaceous Extra-tropical floras are largely nested subsets of tropical
families in the polar and sub-polar zones than in the wet florasinallthreeregionsoftheworld,andthethreenestedness
tropics,theirgradientsinthesub-tropicalandtemperatezones metrics generated equivalent results (Fig.3). In all cases
are substantially different (Fig. 1b,c). The latitudinal gradient nestedness is much higher than expected under a random
1256 JournalofBiogeography38,1253–1266
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Angiospermfamilyrichness
(a) All families
Tropic of Cancer
Equator
Tropic of Capricorn
1 55 110 165 219
(b) Arborescent families
1 20 39 58 78
(c) Herbaceous families
1 20 39 58 78
Figure1 Globalpatternofangiospermfamilyrichnessina9300km2grid.(a)All408families,excludingmarineandsmall-island
endemics,(b)143arborescentfamiliescomprisingexclusivelyorprimarilytreesbutnoherbaceousspecies,and(c)149herbaceousfamilies
comprisingexclusivelyorprimarilyherbsbutnotreesorlianas.Notedifferenceinscalesof(a)and(b,c).
modelorhasnarrowerrors(TableS2).IntheNewWorldand south, but SSN at the longest distance class is similar to the
easternAsia,cells>6000kmapartremainnestedat>79.5% other regions (Fig.3). The nestedness analysis indicates that
and reflect smooth reductions in richness moving north. In low-richnessareascontainlarge-rangedfamiliesalsofoundin
Africa, Asia Minor and Europe the richness gradient is more high-richness areas, whereas smaller-ranged families drop out
complexandslightlylessnestedatintermediatedistancesdue as richness decreases (also visually apparent when cells are
tothepresenceofMediterraneanfamiliesnotoccurringfarther rankedfromhighesttolowestrichness,Fig.3g–i).Thatis,the
JournalofBiogeography38,1253–1266 1257
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B. A.Hawkins etal.
Table1 Globalordinaryleastsquares(OLS)
Predictor(standardizedcoefficients)
regressionmodelsof(a,d)familyrichness,
Model
PET PET2 WD Age R2 (b)meanrangesizeand(c)meanfamilyage
forall408angiospermfamiliesstudied.Note
(a)Familyrichness(climate) 1.85 )0.77 )0.71 – 0.844 thatageismodelledasaresponsevariablein
(1)Treefamilies 1.28 )0.15 )0.71 – 0.873 (c)andasapredictorin(d).Modelsforherb
(2)Herbfamilies 1.87 )0.93 )0.75 – 0.696 (n=149)andtree(n=143)familiesarealso
(b)Meanrangesize(climate) )1.74 0.64 0.70 – 0.850 providedforcomparison.Predictorvariables
(1)Treefamilies )1.53 0.46 0.58 – 0.804 arePET=potentialevapotranspiration,WD
(2)Herbfamilies )1.50 0.47 0.67 – 0.741 [waterdeficit]=PET)AET[actualevapo-
(c)Meanage(climate) 0.93 )0.22 )0.90 – 0.596 transpiration],andAge=meanageof
(1)Treefamilies 1.76 )0.81 )0.23 – 0.778 families.
(2)Herbfamilies 0.16 )0.09 )0.67 – 0.389
(d)Familyrichness(climate+age) 1.46 )0.68 )0.34 0.41 0.913
(1)Treefamilies 0.89 0.02 )0.66 0.23 0.885
(2)Herbfamilies 1.82 )0.91 )0.45 0.47 0.829
tropics contain families varying from being narrowly distrib-
The agesof tropical andextra-tropical floras
uted endemics to cosmopolitan, but only the most widely
distributed families occur inthefarnorth and majordeserts. Thegeographicdistributionofmeanfamilyageisnotentirely
The ranges of arborescent and herbaceous families largely consistent with the version of the tropical conservatism
follow those of all families, with some differences (Fig.2b,c). hypothesis developed in the Introduction (Fig.4a). Tropical
Tree family ranges are smaller than herb family ranges florasaresubstantiallyolderthanthoseofdesertsandnorthern
(mean=22,063,915km2, SE=2,400,333 vs. mean= tundra,aspredicted,butmeanfamilyageisalsoolderinparts
39,605,515km2, SE=3,367,965), and the geographic pattern of the extra-tropics, including the south-eastern USA, and
of mean tree range size is very similar to that found for all across a broad band across the boreal zone of Eurasia. This
families, except in Australia (Fig.2b) due to 13 Australasian complexpatternresultsinaclimatemodelformeanagewith
endemictreefamilies.Thenestednessoftreefamilyrichnessin moderate explanatory power (Table1c). It also arises from
thelongest distanceclassesisalsoverystrongasmeasuredby mixing essentially opposite age patterns for trees and herbs;
SSN: 100 in the western Old World, 83.0 in the New World arborescent families are oldest in the tropics/sub-tropics and
and78.6ineasternAsia(Fig.3a–c).Meanrangesizesofherbs the Southern Hemisphere, and youngest on average in the
also tend to be relatively small in the tropics, although the northern temperate, boreal and sub-polar zones (Fig.4b),
eastern USA and northern California also support relatively whereas herbaceous families are oldest across much of North
narrowly ranged families on average (Fig. 2c). Even so, America and the forest belt of Eurasia (Fig.4c). Herbaceous
nestedness levels are high in all regions, with SSNs in the familiesareyoungestonaverageintheSaharaandAustralian
longest distance classes ranging from 69.1 in the western Old deserts,TierradelFuegoandthenortherntundrazone,butare
World, 80.6 in eastern Asia and 83.5 in the New World not especially old in the tropics. Fundamentally different
(Fig.3a–c). Thus, although herb families are more widely relationships between climate and age for trees and herbs are
distributed than arborescent families, their richness pattern alsoreflectedbyverydifferentmultipleregressionmodels.Tree
stillreflectsprimarilyafilteringoutofsmaller-rangedfamilies ages are strongly associated with climate, being oldest on
moving from the topics towards the pole, with a limited average in warm climates (Table 1c1), whereas herb ages are
replacement bytemperate-zone families. somewhat weakly associated with climate but are youngest in
The nested nature of the richness gradient in the Northern dry regions (Table1c2). Thus, a strong TCH signal is found
Hemisphereisfurtherreflectedbythefactthatfewfamiliesare amongthosefamiliescomprisingonlytrees,buttheprediction
strictlyextra-tropicalintheHolarctic:only2%(3/149)oftree that tropical herb families are older than temperate-zone
families occur exclusively north of the Tropic of Cancer, and families isrejected.
only7%(10/143)ofherbaceousfamiliesdoso.Amongthe116
remainingfamiliescomprisingshrubs,lianasoramixofgrowth
Covariance between current climate and familyage
forms,onlytwo(1.7%)areexclusivelynorthernextra-tropical.
The strong link between family richness and ranges sizes Mean family age and richness are moderately positively
togetherwiththehighlevelsofnestednessindicatethatclimate correlated across all families (r=0.740) and tree families
primarily drives angiosperm family richness as a filter; (r=0.770) but more weakly for herb families (r =0.449).
selectively excluding families moving into colder and drier Thus, for all groups richness is more strongly associated with
climates to a much greater extent than it selects for the currentclimatethanwithevolutionaryhistoryasmeasuredby
replacement of tropical families by non-tropical families in familyages.Age-basedmodelsalsocontainmoreunexplained
cold,dry regions. spatial structure than the climate models, especially for all
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Angiospermfamilyrichness
(a) All families
51 68 85 103 120
6 2
x10 km
(b) Arborescent families
31 49 67 85 104
6 2
x10 km
(c) Herbaceous families
31 49 67 85 104
6 2
x10 km
Figure2 Globalpatternofmeanrangesizeofangiospermfamilies.(a)Allfamilies(n=408),(b)arborescentfamiliesonly(n=143),and
(c)herbaceousfamiliesonly(n=149).Notedifferenceinscalesof(a)and(b,c).
families and herbaceous families (Fig.S2). Adding age to the for almost all of the spatial structure in the global gradient
climatic models increased their explanatory power for all except at thesmallestdistance class(Fig.S2).
familiesaswellasherbs,butnotfortrees(Table1d),andthe Partitioning the independent and covarying associations of
models combining both age and climate successfully account family richness with climate and age indicates substantial
JournalofBiogeography38,1253–1266 1259
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B. A.Hawkins etal.
(a) New World (b) Western Old World (c) East Asia
100
90
80
)
% 70
( 60
N 50
S 40
S 30 All families
20 Arborescent families
10 Herbaceous families
0
e (d) (e) (f)
cn 0
e -20
re -40
ffid --8600
s-100
s-120
e
n-140
h-160
c
iR 0 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 0 1 2 3 4 5 6
Northwarddistance(x 1000 km)
(g) (h) (i)
s
s
e
n
h
c
iR
SSN=90.8% SSN=83.5% SSN=90.6%
NODF= 87.8% NODF=80.8% NODF=87.9%
100–T=86.5% 100–T=78.8% 100–T=87.5%
Figure3 Nestednesspatternsoftotal,arborescentandherbaceousfamilyrichnessinthreeregions(seeFig.S1fortransectlocations).(a–c)
Spatialpatternsofmeansubsamplenestedness(SSN)forcellsgroupedin10distanceclasses,(d–f)spatialpatternsofchangesoffamily
richnessmovingfromtheequatornorthwardswithineachtransect,and(g–i)maximallypackedpresence–absencematricesforallcellsin
eachtransect,withthreenestednessmetrics(SSN,NODFand100)T,seetext).Pointsin(a–c)alsoinclude95%confidenceintervals,
whichinallcasesarenarrowerthantheheightsofthesymbols.
covarianceofcurrentconditionsanddeepevolution(Fig. 5a), controlofherbfamilyrichnessisindependentofhowlongthe
andthatmostoftheage-relatedsignalintherichnesspattern familieshaveexisted,andsimultaneouslythattheevolutionary
covarieswiththeclimaticgradient.Buttherelationshipsacross signalislargelyindependentofcurrentclimaticgradients.
all families conceal substantial differences between herbs and Basedontheevolutionarymetricatourdisposal,familyage,
trees. High overlap between climate and age for tree families thepropositionthatclimateandfamilyrichnessarecorrelated
(Fig.5b) is consistent with the proposition that covariation at least in part due to an evolutionary legacy of angiosperm
betweentreerichnessandclimateisalegacyoftheevolutionary evolution that is itself associated with climate is supported
developmentoftheflora.Indeed,virtuallyalloftheevolutionary across all families and particularly strongly for arborescent
signalmeasuredbyfamilyagecanbeexplainedbyclimate.In families. Herbs, on the other hand, seem to be responding
contrast,herbfamilyrichnessisstronglyassociatedwithcurrent much more strongly to current climate per se, and although
climate,butthereisalsoamoderateindependentrelationship theirgradientcontainsclearagestructure(seeFig. 4c)mostof
with age (Fig.5c). Surprisingly, there is minimal overlap thisstructurehasarisenindependentlyoftheclimaticgradient
between climateand age, suggestingthat most of theclimatic described bycontemporary variables.
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Angiospermfamilyrichness
(a) All families
71.1 68.8 66.6 63.8 34.9
x 10 6 yr
(b) Arborescent families
80.5 73.9 69.0 61.5 33.2
x 10 6 yr
(c) Herbaceous families
80.7 69.9 67.6 65.0 34.8
x 10 6 yr
Figure4 Globalpatternofmeanmaximumageofangiospermfamilies.(a)Allfamilies(n=408),(b)arborescentfamiliesonly(n=143),
and(c)herbaceousfamiliesonly(n=149).Colourscalesarebasedon32quantiles.
richness gradient. One unambiguous result is that the global
DISCUSSION
pattern identified by Francis & Currie (2003) is reproducible
Most of our analyses generated clear answers to the four despite being based on only 75% of the families currently
questions on which we focused, but they also identified some recognized. As an emergent property, the pattern of taxon
of the complexity that must underlie the angiosperm family richnessderivedfromrangemapsisrelativelyinsensitivetothe
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B. A.Hawkins etal.
(a) All families herbaceousfamiliesisnotapoorfittingmodel.Thatis,wefind
associationsindicativeofclimaticcontroloftaxonrichnessfor
36.6 47.8 6.9 8.7 herbs at the global extent, even when using a simple model
including only twoofmany potential climatic predictors.
PET - PET 2 + WD Overlap Ageunexpl.
How climate drives angiosperm family richness seems
unambiguous, givenboththeverystrongassociation between
(b) Arborescent families
1.2 range sizes and richness and the high levels of compositional
nestedness of floras moving from high-richness floras of the
29.2 58.1 11.1
wet tropics to low richness floras of deserts and tundra. Our
PET - PET 2 + WD Overlap Age unexpl. findingsareconsistentwiththehypothesisforthediversityof
northern temperate trees developed by Latham & Ricklefs
(c) Herbaceous families (1993b),basedonpresumeddifficultiesfortreecladestoadapt
to the widespread cold climates that appeared in the Oligo-
62.7 6.9 13.3 17.1 cene. It is further consistent with a version of the tropical
conservatismhypothesisthatproposesthatnicheconservatism
PET - PET 2 + WD Overlap Age unexpl.
atthefamilylevelhasremainedstrongamongplantsrelativeto
Figure5 Partialregressionsoffamilyrichnessagainstclimate nicheevolution.Wealsofindverysimilarnestednesspatterns
andmeanfamilyagefor(a)allangiospermfamilies(n=408),(b) forbothherbsandtrees,indicatingthatdespitedifferencesin
arborescentfamiliesonly(n=143),and(c)herbaceousfamilies their richness gradients, associations with climate, range size
only(n=149).Numberswithinbarsarepercentagesofvariation distributions and age patterns, the same underlying process
inrichnessexplainedbyeachcomponent.Theoverlapregion applies to both. Climate primarily drives higher level angio-
representsvariationinrichnessthatcannotbeunambiguously sperm diversity via a filtering process irrespective of the
assignedtoeitherclimateorageduetocollinearitybetweenthem.
families’ growth form.
Thevariationnotexplainedbythemodelisalsoprovided.
Therange size pattern also suggests a simple interpretation
forawidelystudiedecogeographicalrule,Rapoport’srule,asit
applies to angiosperm families. Range sizes are larger in the
detailsofhowtaxaaredistinguishedandmapped,andevento north and in deserts than in the wet tropics, but not because
the taxonomic completeness of the data. It also follows that the families that have colonized these regions differ from
statistical evaluations of richness patterns with respect to tropicalgroupsbyhavingbroaderclimatictolerances(Stevens,
environmentalgradientsarerobust,andcurrentlyknownlinks 1989).Mostfamiliesintheextra-tropicsarealsotropical;they
between plant family richness and climate are unlikely to justdifferfromothertropicalfamiliesbyincludingspeciesthat
change even if future phylogenetic work redefines the plant have evolvedtraits thathave permitted rangeexpansions into
clades currently considered to be families. The stability of coldordryclimates.Thisisasubtlebutimportantdifference
climatic models for woody plant richness across multiple in the usual explanation of this ecogeographical pattern that
taxonomic levels of resolution (Field etal., 2005; O’Brien, may arise from considering range sizes of higher level clades
2006) further indicates that plant diversity and climate are so ratherthanspecies.Ourfocusonfamiliesmayalsoexplainthe
closely linked that associations between plants and water/ verystrongcorrelationbetweenmeanrangesizeandrichness,
energy cannot be decoupled by vagaries in how plants are not typical of analyses at the species level (e.g. Graves &
classifiedor howdetailed theirdistributions are mapped. Rahbek, 2005; Orme etal., 2006; Kraft etal., 2010). On the
Analyses of taxon richness gradients focused on woody otherhand,rangesizepatternsanalogoustothosedescribedby
groups invariably find strong associations between richness Rapoport’srulegeneratedbynestedrangestructureshavebeen
andwater/energygradients(e.g.Currie&Paquin,1987;Adams foundatthespeciesleveloversmallerspatialextents(Beketov,
&Woodward,1989;O’Brien,1993;Fieldetal.,2005;Hawkins 2009, and references therein).
etal., 2007b; Montoya etal., 2007), and disagreement about Although rangesizepatterns representoneline ofevidence
the link between tree diversity and climate is not about thatangiospermfamilydiversitymaybeinfluencedbytropical
whetheritexistsbutwhy(Latham&Ricklefs,1993b;McGlone, niche conservatism, patterns of family age generate a more
1996; Francis & Currie, 1998; Svenning & Skov, 2007). The complexpicture.Overall,tropicalangiospermassemblagesare
associationbetweenclimateandherbrichnessismoretenuous olderinthetropicsthaninmostpartsoftheextra-tropics,but
and in some situations cannot be found even when matching given the very different mean age patterns of tree and herbs
woodyplantrichnessdoescorrelatewithclimate(Bhattarai& (they are weakly negatively correlated, r=)0.223), interpre-
Vetaas, 2003). And in cases when broad-scale herb taxon tationofthegeneralagegradientmaynotbeinformative.On
richnessandclimatearecorrelated,theassociationsareweaker theotherhand,thepatternofmeanagesoftreefamiliesisas
thanforwoodyplants(Oberleetal.,2009;Wangetal.,2009). predicted by tropical niche conservatism (see Fig.4b), if we
We similarly found a statistically weaker association between assume significant niche conservatism (i.e. intolerance to
climateandherbfamilyrichnessthanforwoodyfamilies,buta freezing)atthefamilylevel.Thetropicscontaintheoldesttree
model that explains 70% of the variance in global richness of families, and mean family age decreases with decreasing
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