Variation in plant demographic trajectories:

problems and opportunities

Owen R. Jones & Roberto Salguero-Gómezjones@demogr.mpg.de

Laboratory for Evolutionary Demography,Max Planck Institute for Demographic Research, Rostock, Germany

salguero@demogr.mpg.de

Evolution is a demographic process

“Evolution is driven by the propagation of genes, traits and individuals with and between populations. This propagation depends on the survival, fertility and dispersal at each age or stage during their life history.”

Metcalf & Pavard (2007) TREE

Mor

talit

y/fe

rtili

ty r

ate

Surv

ivor

ship

(lx

)

Classical theories of the evolution of senescence

Hamilton (1966)Williams (1957) Kirkwood (1977)Medawar (1952)

Older ages are less important to evolution than younger ages: - force of selection declines with age.

Classical theories of the evolution of senescence

“No life schedule ... could escape my spectrum of forces of senescence … in the farthest reaches of almost any bizarre universe” (Hamilton, 1966)

Mor

talit

y

AgeRe

prod

uctio

nAge

COMPADRE DatabaseCOMParative Plant & Algae Demographic REsearch

Trees

Palms

Succulents

Lianas

Shrubs

EpiphytesHerbsAlgae

Miguel Franco

Jonathan Silvertown

COMPADRE DatabaseCOMParative Plant & Algae Demographic REsearch

Trees

Palms

Succulents

Lianas

Shrubs

EpiphytesHerbsAlgae

Miguel Franco

Jonathan Silvertown

Roberto Salguero-Gómez

33"1 " " """""""44" " """""""""""""""""88 " " """""""""""""132"

COMPADRE DatabaseCOMParative Plant & Algae Demographic REsearch

Trees

Palms

Succulents

Lianas

Shrubs

EpiphytesHerbsAlgae

817 species

Number of species

From matrices to trajectories

lxmx

Age

Age

Caswell (2001); Cochran and Ellner (1992)

Mortality trajectories in plants

Acknowledgements

Discussion

Life and death in the garden: mortality and recruitment trajectories in plantsOwen R. Jones* & Roberto Salguero-Gómez*Laboratory of Evolutionary Biodemography, Max Planck Institute for Demographic Research, Rostock, Germany{jones/salguero}@demogr.mpg.de; *Authors contributed equally to this work

One group of 'classical' theories of senescence focuses on the existence of trade-offs between early and late life performance. This body of literature, initiated by Hamilton1 and later supplemented by Williams2, Medawar3 and Kirkwood4, was developed with unitary organisms in mind. These theories are usually interpreted to predict that, after the onset of sexual maturity, survival rate will decline alongside reproductive output. Using data derived from the COMPADRE database5, we examined age-specific mortality and per-capita recruitment trajectories for 329 vascular plant and algae species using population projection matrices6 to examine the validity of these theories for the age trajectories of modular organisms.We demonstrate the existence of an astonishing variety of demographic trajectories in modular organisms, the majority of which do not adhere to the 'classical' Hamiltonian predictions of inevitable senescence. We argue that environmental filtering and phylogenetic ancestry explains much of the observed variation, and that the classical theories of senescence are not sufficient to explain demographic trajectories in modular organisms like vascular plants, red and brown algae.

Summary

Methods

Legend

Force of mortality

Recruitment

Survivorship

Age

Stan

dard

ized

forc

e of

mor

tality

and

recr

uitm

ent

Surv

ivors

hip

We first obtained the average, control population projection matrices for 329 species of vascular plants and algae from the COMPADRE database5. Each of these matrices contains at least three years worth of stage-based information (stage-specific survival, changes in stage, and sexual reproduction) describing the species’ population dynamics. The average, control population projection matrix represents the element-by-element average of all temporally and spatially replicated matrices in each publication but only under “natural” conditions (i.e., experimental treatments such as fires, floods, and droughts were excluded).We employed methods described by Cochran & Ellner7 to obtain age-specific survorship (lx) and per-capita recruitment (mx), as well as mean age at sexual maturity (Lα)6 and lifespan (L)6. The estimates of lifespan excluded seedbank stasis and thus inform only on the performance of photosynthetically active individuals. We then calculated the force of mortality (μx) from lx, and standardized μx and mx by their respective mean values from age zero up to the age of 99% mortality. These standardized trajectories are informative about the distribution of mortality and per-capita recruitment events throughout the life course of each species8. We have sorted the panels from top-left to bottom-right by decreasing standardized force of mortality at old-age. We have color-coded the background of each plot according to the species' growth form (see legend).

Algae Epiphyte Herbaceousperennial Succulent Shrub Liana Palm tree Tree

References

Despite predictions based on Hamiltonian theories of aging, we found no species where there was a simultaneous increase in the force of mortality (μx) together with a decrease in per-capita recruitment (mx) after maturity. A small number of species did show either increasing μx [Plot #: 2, 4, 5, 6, 7, 8, 11, 13, 19, 24, 25, 26, 49, 177] or declining mx values with age [72, 118, 189, 313]. However, the vast majority of species displayed an increase in mx and flattened or decrease in μx with age.Contrary to expectation, the top part of the aging continuum depicted in our plots is not exclusively occupied by short-lived species, nor by species that invest relatively little in tissue construction and maintenance, such as herbaceous perennials. Instead, a number of long-lived trees, palm trees, succulents, and shrubs appear throughout the continuum. The center of the continuum is mostly dominated by species where μx and mx plateau very quickly after sexual maturity. Although a plateau is ultimately expected from the type of stage-to-age transformations shown here6,7, their initial trajectories prior to the plateau are biologically meaningful properties of their populations. For example, the μx of the desert shrub Cassia nemophila [260] appears to gently fluctuate before eventually stabilizing.These trajectories offer a fascinating glimpse into the demography and senescence of modular organisms, which until now have been neglected. The factors shaping these patterns of aging, as well as the conditions under which modular organisms may escape senescence remain to be explored.Note: species which are lacking mx trajectories are either (i) strictly clonally reproductive [10, 13, 65, 103, 161, 213, 229], (ii) did not report recruitment [2], or (iii) are species where <1% of surviving individuals reproduce [306].

1. Hamilton W. 1966. J. Theor. Biol. 12, 12-45. 2. Williams G. C. 1957. Evolution 11, 398-411. 3. Medawar P. B. 1952. An unsolved problem of biology. pp. 44-70. 4. Kirkwood T. B. 1977. Nature 270, 301-304. 5. Salguero-Gómez R. Unpubl. COMPADRE: COMparative Plant & Algae Demographic REsearch Database. MPIDR. 6. Caswell H. 2001. Matrix population models: Construction, analysis and interpretation. 7. Cochran M. E. & Ellner S. 1992. Ecol. Monogr. 62, 345-264. 8. Baudisch A. 2011. Methods in Ecol. & Evol. 2, 375-382.

This work was supported by the Laboratory of Evolutionary Biodemography, and the Max Planck Research Group: Modeling the Evolution of Aging, at the Max Planck Institute for Demographic Research, as well as two fellowships to R.S-G (Teece Family Foundation, University of Pennsylvania). We acknowledge help by the COMPADRE digitalization team: E. Briks, S. Zeh, C. Farack, G. Roemer, A. Henning & G. Hoppe.

Mean age at first reproduction

0.0

2.5

5.0

0 6Years

1Ceratozamia mirandae

(Cycadales)

0 5Years

2Prunus serotina

(Rosales)

0 37Years

3Pinus sylvestris

(Pinales)

0 109Years

4Escontria chiotilla

(Caryophyllales)

0 198Years

5Coccothrinax readii

(Arecales)

0 134Years

6Thrinax radiata

(Arecales)

0 52Years

7Fagus grandifolia

(Fagales)

0 6Years

8Pterygophora

californica(Laminariales)

0 62Years

9Podococcus berteri

(Arecales)

0 16Years

10Disporum smilacinum

(Liliales)

0 128Years

11Geonoma orbignyana

(Arecales)

0 14Years

12Rhododendron maximum

(Ericales)

0 27Years

13Clintonia borealis

(Liliales)

0 458Years

14Prioria copaifera

(Fabales)

0 309Years

15Pinus palustris

(Pinales)

0 40Years

16Callitris

intratropica(Pinales)

0 998Years

17Vouacapoua americana

(Fabales)

0 17Years

18Digitaria eriantha

(Lamiales)

0 8Years

19Carlina vulgaris

(Asterales)

0 672Years

20Dicorynia guianensis

(Fabales)

0 30Years

21Alnus indicata

(Liliales)

0 12Years0

0.5

122

Eriophorumangustifolium

(Poales)

0.0

2.5

5.0

0 15Years

23Anemone patens

(Ranunculales)

0 28Years

24Ulex gallii(Fabales)

0 86Years

25Pinus jeffreyi

(Pinales)

0 11Years

26Carex membranaceae

(Poales)

0 26Years

27Lonicera maackii

(Dipsacales)

0 18Years

28Carex aquatilis

(Poales)

0 37Years

29Aristida bipartita

(Poales)

0 16Years

30Ophrys sphegodes

(Asparagales)

0 8Years

31Centaurea jacea

(Asterales)

0 15Years

32Rosa multiflora

(Rosales)

0 998Years

33Balsamorhiza

sagittata(Asterales)

0 13Years

34Podophyllum peltatum

(Ranunculales)

0 57Years

35Iris germanica(Asparagales)

0 7Years

36Gaura neomexicana

(Myrtales)

0 24Years

37Achillea millefolium

(Asterales)

0 41Years

38Geonoma brevispatha

(Arecales)

0 14Years

39Neotinea ustulata

(Asparagales)

0 671Years

40Callycophyllum

spruceanum(Gentianales)

0 561Years

41Virola surinamensis

(Magnoliales)

0 482Years

42Carapa guianensis

(Sapindales)

0 396Years

43Pouteria sagotiana

(Ericales)

0 378Years0

0.5

144

Platymiscium filipes(Fabales)

0.0

2.5

5.0

0 355Years

45Mora paraensis

(Fabales)

0 136Years

46Arnica angustifolia

(Asterales)

0 271Years

47Licaria mahuba

(Laurales)

0 43Years

48Astragalus scaphoides

(Fabales)

0 14Years

49Cheirolophus

metlesicsii(Asterales)

0 50Years

50Abies sachalinensis

(Pinales)

0 92Years

51Dactylorhiza

lapponica(Asparagales)

0 140Years

52Hymenoxys herbacea

(Asterales)

0 68Years

53Trifolium pratense

(Fabales)

0 61Years

54Pinguicula ionantha

(Lamiales)

0 98Years

55Abies concolor

(Pinales)

0 35Years

56Himantoglossum

hircinum(Asparagales)

0 181Years

57Calochortustiburonensis

(Liliales)

0 706Years

58Taxus brevifolia

(Pinales)

0 475Years

59Heliconia acuminata

(Zingiberales)

0 82Years

60Laccospermasecundiflorum

(Arecales)

0 41Years

61Primula veris

(Ericales)

0 5Years

62Tillandsia

brachycaulos(Poales)

0 14Years

63Heteropogon contortus

(Poales)

0 15Years

64Bothriochloa

insculpta(Poales)

0 8Years

65Aechmea nudicaulis

(Poales)

0 10Years0

0.5

166

Braya fernaldii(Brassicales)

0.0

2.5

5.0

0 59Years

67Banksia ericifolia

(Proteales)

0 139Years

68Petrophile pulchella

(Proteales)

0 3016Years

69Prosopis glandulosa

(Fabales)

0 24Years

70Calochortus albus

(Liliales)

0 147Years

71Chamaedorea radicalis

(Arecales)

0 8Years

72Polemoniumvanbruntiae

(Ericales)

0 13Years

73Saussurea medusa

(Asterales)

0 32Years

74Fritillaria

camtschatcensis(Liliales)

0 25Years

75Actaea elata

(Ranunculales)

0 19Years

76Calluna vulgaris

(Ericales)

0 20Years

77Scabiosa columbaria

(Dipsacales)

0 6Years

78Pseudomisopatesrivas−martinezii

(Malpighiales)

0 32Years

79Fumana procumbens

(Malvales)

0 49Years

80Helianthusdivaricatus(Asterales)

0 27Years

81Viola fimbriatula

(Malpighiales)

0 33Years

82Tillandsia recurvata

(Poales)

0 34Years

83Cimicifuga elata(Ranunculales)

0 16Years

84Centaurea maculosa

(Asterales)

0 20Years

85Setaria incrassata

(Poales)

0 89Years

86Aquilaria crassna

(Malvales)

0 38Years

87Borderea pyrenaica

(Dioscoreales)

0 57Years0

0.5

188

Succisa pratensis(Dipsacales)

0.0

2.5

5.0

0 170Years

89Rosmarinus tomentosus

(Lamiales)

0 121Years

90Cirsium acaule

(Asterales)

0 401Years

91Scaphium borneense

(Malvales)

0 42Years

92Helianthemum juliae

(Malvales)

0 95Years

93Epilobium latifolium

(Myrtales)

0 44Years

94Primula farinosa

(Ericales)

0 34Years

95Calochortusmacrocarpus

(Liliales)

0 88Years

96Geum reptans

(Rosales)

0 125Years

97Eremophila maitlandii

(Lamiales)

0 375Years

98Borderea chouardii

(Dioscoreales)

0 62Years

99Nardostachys

grandiflora(Dipsacales)

0 26Years

100Geranium sylvaticum

(Arecales)

0 33Years

101Rubus saxitalis

(Rosales)

0 196Years

102Calochortusobisopensis

(Liliales)

0 16Years

103Cleistes varicata 1

(Asparagales)

0 84Years

104Periandra

mediterranea(Fabales)

0 99Years

105Guarianthe aurantiaca

(Asparagales)

0 35Years

106Calochortus lyallii

(Liliales)

0 9Years

107Arabis fecunda

(Brassicales)

0 85Years

108Lathyrus vernus

(Fabales)

0 25Years

109Clidemia hirta

(Myrtales)

0 39Years0

0.5

1110

Artemisia genipi(Asterales)

0.0

2.5

5.0

0 7Years

111Sarcocapnosenneaphylla

(Ranunculales)

0 34Years

112Acer saccharum

(Sapindales)

0 44Years

113Ipomoea leptophylla

(Solanales)

0 6Years

114Daucus carota

(Apiales)

0 37Years

115Aconitum

noveboracense(Ranunculales)

0 16Years

116Lomatium cookii

(Apiales)

0 16Years

117Manglietia fordiana

(Magnoliales)

0 7Years

118Hypericum cumulicola

(Malpighiales)

0 8Years

119Iridaea splendens

(Gigartinales)

0 14Years

120Asclepias meadii

(Gentianales)

0 237Years

121Ptychosperma

macarthurii(Arecales)

0 25Years

122Lespedeza cuneata

(Fabales)

0 24Years

123Hydrastis canadensis

(Ranunculales)

0 238Years

124Licania heteromorpha

(Brassicales)

0 5Years

125Cirsium vulgare

(Asterales)

0 9Years

126Atriplex acanthocarpa

(Caryophyllales)

0 399Years

127Eremophila forrestii

(Lamiales)

0 5Years

128Linum catharticum

(Malpighiales)

0 96Years

129Echinaceaangustifolia(Asterales)

0 24Years

130Themeda triandra

(Poales)

0 150Years

131Opuntia macrocentra

(Caryophyllales)

0 7Years0

0.5

1132

Gelidium sesquipedale(Gelidiales)

0.0

2.5

5.0

0 45Years

133Fritillaria meleagris

(Liliales)

0 37Years

134Coryphantarobbinsorum

(Caryophyllales)

0 419Years

135Lepanthes eltoroensis

(Asparagales)

0 45Years

136Aster amellus

(Asterales)

0 18Years

137Allium monanthum

(Liliales)

0 3Years

138Dipsacus sylvestris

(Dipsacales)

0 68Years

139Panax quinquefolium

(Apiales)

0 9Years

140Viola elatior(Malpighiales)

0 12Years

141Braya longii(Brassicales)

0 17Years

142Asarum canadense

(Piperales)

0 4Years

143Tragopogon dubius

(Asterales)

0 14Years

144Lupinus arboreus

(Fabales)

0 6Years

145Carnegiea gigantea

(Caryophyllales)

0 38Years

146Saxifraga cotyledon

(Saxifragales)

0 7Years

147Rumex rupestris(Caryophyllales)

0 6Years

148Taraxacum officinale

(Asterales)

0 21Years

149Chamaecrista keyensis

(Fabales)

0 20Years

150Tolumnia variegata

(Asparagales)

0 8Years

151Centaurea corymbosa

(Asterales)

0 11Years

152Zea diploperennis

(Poales)

0 11Years

153Aquilegia sp.(Ranunculales)

0 10Years0

0.5

1154

Tillandsia punctulata(Poales)

0.0

2.5

5.0

0 653Years

155Sarracenia alata

(Ericales)

0 5Years

156Cirsium dissectum

(Asterales)

0 10Years

157Lupinus tidestromii

(Fabales)

0 9Years

158Allium tricoccum

(Liliales)

0 27Years

159Anthyllis alpicola

(Fabales)

0 33Years

160Echeveria longissima

(Saxifragales)

0 5Years

161Cleistes varicata 2

(Asparagales)

0 16Years

162Viola stagnina(Malpighiales)

0 81Years

163Primula vulgaris

(Ericales)

0 272Years

164Duguetia neglecta

(Magnoliales)

0 11Years

165Cryptantha flava

(Lamiales)

0 32Years

166Aspasia principissa

(Asparagales)

0 9Years

167Bothriochloaischaemum

(Poales)

0 32Years

168Betula nana

(Fagales)

0 10Years

169Tillandsia deppeana

(Poales)

0 15Years

170Hydrangea paniculata

(Cornales)

0 36Years

171Pedicularisfurbishiae

(Malpighiales)

0 33Years

172Cytisus scoparius

(Fabales)

0 82Years

173Iriartea deltoidea

(Asparagales)

0 8Years

174Hypochaeris radicata

(Asterales)

0 15Years

175Lomatium bradshawii

(Apiales)

0 313Years0

0.5

1176

Garcinia lucida(Malpighiales)

0.0

2.5

5.0

0 72Years

177Pseudophoenix

sargentii(Arecales)

0 33Years

178Annamocarya sinensis

(Malvales)

0 77Years

179Swallenia alexandrae

(Poales)

0 26Years

180Manilkara zapota

(Ericales)

0 5Years

181Espeletia spicata

(Asterales)

0 641Years

182Molinia caerulea

(Poales)

0 9Years

183Viola pumila(Malpighiales)

0 311Years

184Paronychia pulvinata

(Caryophyllales)

0 20Years

185Lobularia maritima

(Brassicales)

0 43Years

186Atriplex canescens

(Caryophyllales)

0 6Years

187Dicerandra frutescens

(Lamiales)

0 3Years

188Ailanthus altissima

(Sapindales)

0 3Years

189Mimulus guttatus

(Lamiales)

0 158Years

190Araucaria hunsteinii

(Pinales)

0 142Years

191Atriplex vesicaria(Caryophyllales)

0 102Years

192Rourea induta

(Oxalidales)

0 11Years

193Pinguicula villosa

(Lamiales)

0 5Years

194Ambrosia deltoidea

(Asterales)

0 33Years

195Tillandsia

macdougallii(Poales)

0 758Years

196Encephalartos

villosus(Cycadales)

0 171Years

197Opuntia rastrera(Caryophyllales)

0 5Years0

0.5

1198

Oenothera deltoides(Myrtales)

0.0

2.5

5.0

0 1276Years

199Acacia bilimekii

(Fabales)

0 15Years

200Astragalus tyghensis

(Fabales)

0 106Years

201Agrimonia eupatoria

(Rosales)

0 29Years

202Andropogon semiberbis

(Poales)

0 43Years

203Trifolium montanum

(Fabales)

0 297Years

204Sclerocarya birrea

(Sapindales)

0 147Years

205Ardisia

escallonioides(Ericales)

0 6Years

206Disporum sessile

(Liliales)

0 6Years

207Festuca gracillima

(Poales)

0 39Years

208Silene regia

(Caryophyllales)

0 59Years

209Geum rivale

(Rosales)

0 16Years

210Syzygium jambos

(Myrtales)

0 5Years

211Eryngium cuneifolium

(Apiales)

0 20Years

212Werauhia

sanguinolenta(Poales)

0 41Years

213Aechmea magdalenae

(Poales)

0 28Years

214Lindera umbellata

(Laurales)

0 41Years

215Achnatherumcalamagrostis

(Poales)

0 12Years

216Haplopappus radiatus

(Asterales)

0 13Years

217Gentiana pneumonanthe

(Gentianales)

0 186Years

218Quercus rugosa

(Fagales)

0 35Years

219Ramonda myconi

(Lamiales)

0 5Years0

0.5

1220

Oxalis acetosella(Oxalidales)

0.0

2.5

5.0

0 28Years

221Scorzonera hispanica

(Asterales)

0 35Years

222Hudsonia montana

(Malvales)

0 3Years

223Aquilaria microcarpa

(Malvales)

0 595Years

224Euterpe edulis

(Arecales)

0 13Years

225Dodonaca angustifolia

(Sapindales)

0 6Years

226Catopsis sessiliflora

(Poales)

0 105Years

227Stryphnodendron

excelsum(Fabales)

0 22Years

228Calocedrus macrolepis

(Pinales)

0 5Years

229Carex humilis

(Poales)

0 6Years

230Neodypsis decaryi

(Arecales)

0 33Years

231Pterocarya rhoifolia

(Fagales)

0 51Years

232Abies magnifica

(Pinales)

0 186Years

233Borassus aethiopum

(Arecales)

0 30Years

234Machaerium cuspidatum

(Fabales)

0 302Years

235Juniperus procera

(Pinales)

0 24Years

236Lepidium davisii

(Brassicales)

0 6Years

237Aquilegia chrysantha

(Ranunculales)

0 11Years

238Hilaria mutica

(Poales)

0 998Years

239Myrsine guianensis

(Ericales)

0 78Years

240Chamaelirium luteum

(Liliales)

0 7Years

241Laminaria digitata

(Laminariales)

0 3Years0

0.5

1242

Limonium carolinianum(Caryophyllales)

0.0

2.5

5.0

0 209Years

243Kosteletzkyapentacarpos

(Malvales)

0 42Years

244Acer rurinerve

(Sapindales)

0 18Years

245Sanicula europaea

(Apiales)

0 499Years

246Roupala montana

(Proteales)

0 38Years

247Pinguicula alpina

(Lamiales)

0 4Years

248Austrostipaaristiglumis

(Poales)

0 59Years

249Pinus lambertiana

(Pinales)

0 38Years

250Miconia prasina

(Myrtales)

0 45Years

251Viburnum furcatum

(Dipsacales)

0 32Years

252Pinus kwangtungensis

(Pinales)

0 4Years

253Eupatoriumperfoliatum(Asterales)

0 65Years

254Magnolia salicifolia

(Magnoliales)

0 4Years

255Phyllanthus emblica

(Malpighiales)

0 61Years

256Geonoma macrostachys

(Arecales)

0 51Years

257Trillium grandiflorum

(Liliales)

0 22Years

258Actaea spicata(Ranunculales)

0 43Years

259Tachigali vasquezii

(Fabales)

0 33Years

260Cassia nemophila

(Fabales)

0 12Years

261Gardenia actinocarpa

(Gentianales)

0 25Years

262Ulex minor(Fabales)

0 158Years

263Sarcocapnos baetica

(Ranunculales)

0 40Years0

0.5

1264

Pentaclethramacroloba(Fabales)

0.0

2.5

5.0

0 40Years

265Parashorea chinensis

(Magnoliales)

0 150Years

266Sarracenia purpurea

(Ericales)

0 3Years

267Rhopalostylis sapida

(Arecales)

0 277Years

268Ardisia elliptica

(Ericales)

0 215Years

269Hyparrhenia diplandra

(Poales)

0 76Years

270Eremospathamacrocarpa

(Arecales)

0 40Years

271Calochortuspulchellus

(Liliales)

0 19Years

272Cleome droserifolia

(Brassicales)

0 12Years

273Arisaema serratum

(Alismatales)

0 13Years

274Arisaema triphyllum

(Alismatales)

0 21Years

275Pinus ponderosa

(Pinales)

0 12Years

276Tillandsiamulticaulis

(Poales)

0 92Years

277Rhododendron ponticum

(Ericales)

0 409Years

278Silene acaulis(Caryophyllales)

0 56Years

279Scorzonera humilis

(Asterales)

0 36Years

280Pinguicula vulgaris

(Lamiales)

0 17Years

281Acer mono(Sapindales)

0 4Years

282Chlorocardium rodiei

(Laurales)

0 198Years

283Minuartia obtusiloba

(Caryophyllales)

0 550Years

284Encephalartos

cycadifolius(Cycadales)

0 3Years

285Cirsium palustre

(Asterales)

0 81Years0

0.5

1286

Sarcocapnospulcherrima

(Ranunculales)

0.0

2.5

5.0

0 386Years

287Calocedrus decurrens

(Pinales)

0 18Years

288Armeria maritima

(Caryophyllales)

0 10Years

289Mimulus lewisii

(Lamiales)

0 4Years

290Mimulus cardinalis

(Lamiales)

0 30Years

291Harrisia fragrans(Caryophyllales)

0 31Years

292Mauritaria flexuosa

(Arecales)

0 70Years

293Tsuga canadensis

(Pinales)

0 239Years

294Dicymbe altsonii

(Fabales)

0 30Years

295Sabal yapa(Arecales)

0 69Years

296Pterocarpusangolensis(Fabales)

0 36Years

297Silene

douglasii(Caryophyllales)

0 45Years

298Primula elatior

(Ericales)

0 52Years

299Phytelephas seemannii

(Arecales)

0 9Years

300Styrax obassia

(Ericales)

0 16Years

301Acer amoenum

(Sapindales)

0 22Years

302Lepanthes rupestris

(Asparagales)

0 294Years

303Rumex obtusifolius

(Caryophyllales)

0 84Years

304Pinus nigra

(Pinales)

0 41Years

305Dacrydium elatum

(Pinales)

0 16Years

306Neobuxbaumiamacrocephala(Caryophyllales)

0 20Years

307Pterocereus gaumeri

(Caryophyllales)

0 3Years0

0.5

1308

Mammillariapectinifera

(Caryophyllales)

0.0

2.5

5.0

0 23Years

309Mammillaria

magnimamma(Caryophyllales)

0 48Years

310Avicennia germinans

(Lamiales)

0 5Years

311Cynoglossumvirginianum(Lamiales)

0 20Years

312Tillandsia juncea

(Poales)

0 3Years

313Eupatorium resinosum

(Asterales)

0 5Years

314Bouteloua rigidiseta

(Poales)

0 178Years0

0.5

1315

Miconia albicans(Myrtales)

0.0

2.5

5.0

0 6Years

316Zamia amblyphyllidia

(Cycadales)

0 101Years

317Avicennia marina

(Lamiales)

0 8Years

318Astrocaryum mexicanum

(Arecales)

0 137Years

319Bertholletia excelsa

(Ericales)

0 16Years

320Neobuxbaumia tetetzo

(Caryophyllales)

0 100Years

321Nothofagus fusca

(Fagales)

0 320Years0

0.5

1322

Aesculus turbinata(Sapindales)

0.0

2.5

5.0

0 9Years

323Araucaria

cunninghamii(Pinales)

0 6Years

324Lindera benzoin

(Laurales)

0 3Years

325Neobuxbaumiamezcalaensis(Caryophyllales)

0 4Years

326Calathea ovandensis

(Caryophyllales)

0 25Years

327Prunus africana

(Rosales)

0 4Years

328Plantago media

(Lamiales)

0 9Years0

0.5

1329

Trilliumcamschatcense

(Liliales)

Demographic trajectories in plantsM

orta

lity

(red

)R

ecru

itmen

t (b

lue)

Surv

ivor

ship

(gr

een)

Age (yrs)

Red fir (Abies magnifica)

Demographic trajectories in plants

Demographic senescence DOES occur in some species:

...but mostly only in mortality, not recruitment.

Demographic trajectories in plants

Most species are strongly negatively senescent... they get better with age.

Mortality trajectories in plants

Acknowledgements

Discussion

Life and death in the garden: mortality and recruitment trajectories in plantsOwen R. Jones* & Roberto Salguero-Gómez*Laboratory of Evolutionary Biodemography, Max Planck Institute for Demographic Research, Rostock, Germany{jones/salguero}@demogr.mpg.de; *Authors contributed equally to this work

One group of 'classical' theories of senescence focuses on the existence of trade-offs between early and late life performance. This body of literature, initiated by Hamilton1 and later supplemented by Williams2, Medawar3 and Kirkwood4, was developed with unitary organisms in mind. These theories are usually interpreted to predict that, after the onset of sexual maturity, survival rate will decline alongside reproductive output. Using data derived from the COMPADRE database5, we examined age-specific mortality and per-capita recruitment trajectories for 329 vascular plant and algae species using population projection matrices6 to examine the validity of these theories for the age trajectories of modular organisms.We demonstrate the existence of an astonishing variety of demographic trajectories in modular organisms, the majority of which do not adhere to the 'classical' Hamiltonian predictions of inevitable senescence. We argue that environmental filtering and phylogenetic ancestry explains much of the observed variation, and that the classical theories of senescence are not sufficient to explain demographic trajectories in modular organisms like vascular plants, red and brown algae.

Summary

Methods

Legend

Force of mortality

Recruitment

Survivorship

Age

Stan

dard

ized

forc

e of

mor

tality

and

recr

uitm

ent

Surv

ivors

hip

We first obtained the average, control population projection matrices for 329 species of vascular plants and algae from the COMPADRE database5. Each of these matrices contains at least three years worth of stage-based information (stage-specific survival, changes in stage, and sexual reproduction) describing the species’ population dynamics. The average, control population projection matrix represents the element-by-element average of all temporally and spatially replicated matrices in each publication but only under “natural” conditions (i.e., experimental treatments such as fires, floods, and droughts were excluded).We employed methods described by Cochran & Ellner7 to obtain age-specific survorship (lx) and per-capita recruitment (mx), as well as mean age at sexual maturity (Lα)6 and lifespan (L)6. The estimates of lifespan excluded seedbank stasis and thus inform only on the performance of photosynthetically active individuals. We then calculated the force of mortality (μx) from lx, and standardized μx and mx by their respective mean values from age zero up to the age of 99% mortality. These standardized trajectories are informative about the distribution of mortality and per-capita recruitment events throughout the life course of each species8. We have sorted the panels from top-left to bottom-right by decreasing standardized force of mortality at old-age. We have color-coded the background of each plot according to the species' growth form (see legend).

Algae Epiphyte Herbaceousperennial Succulent Shrub Liana Palm tree Tree

References

Despite predictions based on Hamiltonian theories of aging, we found no species where there was a simultaneous increase in the force of mortality (μx) together with a decrease in per-capita recruitment (mx) after maturity. A small number of species did show either increasing μx [Plot #: 2, 4, 5, 6, 7, 8, 11, 13, 19, 24, 25, 26, 49, 177] or declining mx values with age [72, 118, 189, 313]. However, the vast majority of species displayed an increase in mx and flattened or decrease in μx with age.Contrary to expectation, the top part of the aging continuum depicted in our plots is not exclusively occupied by short-lived species, nor by species that invest relatively little in tissue construction and maintenance, such as herbaceous perennials. Instead, a number of long-lived trees, palm trees, succulents, and shrubs appear throughout the continuum. The center of the continuum is mostly dominated by species where μx and mx plateau very quickly after sexual maturity. Although a plateau is ultimately expected from the type of stage-to-age transformations shown here6,7, their initial trajectories prior to the plateau are biologically meaningful properties of their populations. For example, the μx of the desert shrub Cassia nemophila [260] appears to gently fluctuate before eventually stabilizing.These trajectories offer a fascinating glimpse into the demography and senescence of modular organisms, which until now have been neglected. The factors shaping these patterns of aging, as well as the conditions under which modular organisms may escape senescence remain to be explored.Note: species which are lacking mx trajectories are either (i) strictly clonally reproductive [10, 13, 65, 103, 161, 213, 229], (ii) did not report recruitment [2], or (iii) are species where <1% of surviving individuals reproduce [306].

1. Hamilton W. 1966. J. Theor. Biol. 12, 12-45. 2. Williams G. C. 1957. Evolution 11, 398-411. 3. Medawar P. B. 1952. An unsolved problem of biology. pp. 44-70. 4. Kirkwood T. B. 1977. Nature 270, 301-304. 5. Salguero-Gómez R. Unpubl. COMPADRE: COMparative Plant & Algae Demographic REsearch Database. MPIDR. 6. Caswell H. 2001. Matrix population models: Construction, analysis and interpretation. 7. Cochran M. E. & Ellner S. 1992. Ecol. Monogr. 62, 345-264. 8. Baudisch A. 2011. Methods in Ecol. & Evol. 2, 375-382.

This work was supported by the Laboratory of Evolutionary Biodemography, and the Max Planck Research Group: Modeling the Evolution of Aging, at the Max Planck Institute for Demographic Research, as well as two fellowships to R.S-G (Teece Family Foundation, University of Pennsylvania). We acknowledge help by the COMPADRE digitalization team: E. Briks, S. Zeh, C. Farack, G. Roemer, A. Henning & G. Hoppe.

Mean age at first reproduction

0.0

2.5

5.0

0 6Years

1Ceratozamia mirandae

(Cycadales)

0 5Years

2Prunus serotina

(Rosales)

0 37Years

3Pinus sylvestris

(Pinales)

0 109Years

4Escontria chiotilla

(Caryophyllales)

0 198Years

5Coccothrinax readii

(Arecales)

0 134Years

6Thrinax radiata

(Arecales)

0 52Years

7Fagus grandifolia

(Fagales)

0 6Years

8Pterygophora

californica(Laminariales)

0 62Years

9Podococcus berteri

(Arecales)

0 16Years

10Disporum smilacinum

(Liliales)

0 128Years

11Geonoma orbignyana

(Arecales)

0 14Years

12Rhododendron maximum

(Ericales)

0 27Years

13Clintonia borealis

(Liliales)

0 458Years

14Prioria copaifera

(Fabales)

0 309Years

15Pinus palustris

(Pinales)

0 40Years

16Callitris

intratropica(Pinales)

0 998Years

17Vouacapoua americana

(Fabales)

0 17Years

18Digitaria eriantha

(Lamiales)

0 8Years

19Carlina vulgaris

(Asterales)

0 672Years

20Dicorynia guianensis

(Fabales)

0 30Years

21Alnus indicata

(Liliales)

0 12Years0

0.5

122

Eriophorumangustifolium

(Poales)

0.0

2.5

5.0

0 15Years

23Anemone patens

(Ranunculales)

0 28Years

24Ulex gallii(Fabales)

0 86Years

25Pinus jeffreyi

(Pinales)

0 11Years

26Carex membranaceae

(Poales)

0 26Years

27Lonicera maackii

(Dipsacales)

0 18Years

28Carex aquatilis

(Poales)

0 37Years

29Aristida bipartita

(Poales)

0 16Years

30Ophrys sphegodes

(Asparagales)

0 8Years

31Centaurea jacea

(Asterales)

0 15Years

32Rosa multiflora

(Rosales)

0 998Years

33Balsamorhiza

sagittata(Asterales)

0 13Years

34Podophyllum peltatum

(Ranunculales)

0 57Years

35Iris germanica(Asparagales)

0 7Years

36Gaura neomexicana

(Myrtales)

0 24Years

37Achillea millefolium

(Asterales)

0 41Years

38Geonoma brevispatha

(Arecales)

0 14Years

39Neotinea ustulata

(Asparagales)

0 671Years

40Callycophyllum

spruceanum(Gentianales)

0 561Years

41Virola surinamensis

(Magnoliales)

0 482Years

42Carapa guianensis

(Sapindales)

0 396Years

43Pouteria sagotiana

(Ericales)

0 378Years0

0.5

144

Platymiscium filipes(Fabales)

0.0

2.5

5.0

0 355Years

45Mora paraensis

(Fabales)

0 136Years

46Arnica angustifolia

(Asterales)

0 271Years

47Licaria mahuba

(Laurales)

0 43Years

48Astragalus scaphoides

(Fabales)

0 14Years

49Cheirolophus

metlesicsii(Asterales)

0 50Years

50Abies sachalinensis

(Pinales)

0 92Years

51Dactylorhiza

lapponica(Asparagales)

0 140Years

52Hymenoxys herbacea

(Asterales)

0 68Years

53Trifolium pratense

(Fabales)

0 61Years

54Pinguicula ionantha

(Lamiales)

0 98Years

55Abies concolor

(Pinales)

0 35Years

56Himantoglossum

hircinum(Asparagales)

0 181Years

57Calochortustiburonensis

(Liliales)

0 706Years

58Taxus brevifolia

(Pinales)

0 475Years

59Heliconia acuminata

(Zingiberales)

0 82Years

60Laccospermasecundiflorum

(Arecales)

0 41Years

61Primula veris

(Ericales)

0 5Years

62Tillandsia

brachycaulos(Poales)

0 14Years

63Heteropogon contortus

(Poales)

0 15Years

64Bothriochloa

insculpta(Poales)

0 8Years

65Aechmea nudicaulis

(Poales)

0 10Years0

0.5

166

Braya fernaldii(Brassicales)

0.0

2.5

5.0

0 59Years

67Banksia ericifolia

(Proteales)

0 139Years

68Petrophile pulchella

(Proteales)

0 3016Years

69Prosopis glandulosa

(Fabales)

0 24Years

70Calochortus albus

(Liliales)

0 147Years

71Chamaedorea radicalis

(Arecales)

0 8Years

72Polemoniumvanbruntiae

(Ericales)

0 13Years

73Saussurea medusa

(Asterales)

0 32Years

74Fritillaria

camtschatcensis(Liliales)

0 25Years

75Actaea elata

(Ranunculales)

0 19Years

76Calluna vulgaris

(Ericales)

0 20Years

77Scabiosa columbaria

(Dipsacales)

0 6Years

78Pseudomisopatesrivas−martinezii

(Malpighiales)

0 32Years

79Fumana procumbens

(Malvales)

0 49Years

80Helianthusdivaricatus(Asterales)

0 27Years

81Viola fimbriatula

(Malpighiales)

0 33Years

82Tillandsia recurvata

(Poales)

0 34Years

83Cimicifuga elata(Ranunculales)

0 16Years

84Centaurea maculosa

(Asterales)

0 20Years

85Setaria incrassata

(Poales)

0 89Years

86Aquilaria crassna

(Malvales)

0 38Years

87Borderea pyrenaica

(Dioscoreales)

0 57Years0

0.5

188

Succisa pratensis(Dipsacales)

0.0

2.5

5.0

0 170Years

89Rosmarinus tomentosus

(Lamiales)

0 121Years

90Cirsium acaule

(Asterales)

0 401Years

91Scaphium borneense

(Malvales)

0 42Years

92Helianthemum juliae

(Malvales)

0 95Years

93Epilobium latifolium

(Myrtales)

0 44Years

94Primula farinosa

(Ericales)

0 34Years

95Calochortusmacrocarpus

(Liliales)

0 88Years

96Geum reptans

(Rosales)

0 125Years

97Eremophila maitlandii

(Lamiales)

0 375Years

98Borderea chouardii

(Dioscoreales)

0 62Years

99Nardostachys

grandiflora(Dipsacales)

0 26Years

100Geranium sylvaticum

(Arecales)

0 33Years

101Rubus saxitalis

(Rosales)

0 196Years

102Calochortusobisopensis

(Liliales)

0 16Years

103Cleistes varicata 1

(Asparagales)

0 84Years

104Periandra

mediterranea(Fabales)

0 99Years

105Guarianthe aurantiaca

(Asparagales)

0 35Years

106Calochortus lyallii

(Liliales)

0 9Years

107Arabis fecunda

(Brassicales)

0 85Years

108Lathyrus vernus

(Fabales)

0 25Years

109Clidemia hirta

(Myrtales)

0 39Years0

0.5

1110

Artemisia genipi(Asterales)

0.0

2.5

5.0

0 7Years

111Sarcocapnosenneaphylla

(Ranunculales)

0 34Years

112Acer saccharum

(Sapindales)

0 44Years

113Ipomoea leptophylla

(Solanales)

0 6Years

114Daucus carota

(Apiales)

0 37Years

115Aconitum

noveboracense(Ranunculales)

0 16Years

116Lomatium cookii

(Apiales)

0 16Years

117Manglietia fordiana

(Magnoliales)

0 7Years

118Hypericum cumulicola

(Malpighiales)

0 8Years

119Iridaea splendens

(Gigartinales)

0 14Years

120Asclepias meadii

(Gentianales)

0 237Years

121Ptychosperma

macarthurii(Arecales)

0 25Years

122Lespedeza cuneata

(Fabales)

0 24Years

123Hydrastis canadensis

(Ranunculales)

0 238Years

124Licania heteromorpha

(Brassicales)

0 5Years

125Cirsium vulgare

(Asterales)

0 9Years

126Atriplex acanthocarpa

(Caryophyllales)

0 399Years

127Eremophila forrestii

(Lamiales)

0 5Years

128Linum catharticum

(Malpighiales)

0 96Years

129Echinaceaangustifolia(Asterales)

0 24Years

130Themeda triandra

(Poales)

0 150Years

131Opuntia macrocentra

(Caryophyllales)

0 7Years0

0.5

1132

Gelidium sesquipedale(Gelidiales)

0.0

2.5

5.0

0 45Years

133Fritillaria meleagris

(Liliales)

0 37Years

134Coryphantarobbinsorum

(Caryophyllales)

0 419Years

135Lepanthes eltoroensis

(Asparagales)

0 45Years

136Aster amellus

(Asterales)

0 18Years

137Allium monanthum

(Liliales)

0 3Years

138Dipsacus sylvestris

(Dipsacales)

0 68Years

139Panax quinquefolium

(Apiales)

0 9Years

140Viola elatior(Malpighiales)

0 12Years

141Braya longii(Brassicales)

0 17Years

142Asarum canadense

(Piperales)

0 4Years

143Tragopogon dubius

(Asterales)

0 14Years

144Lupinus arboreus

(Fabales)

0 6Years

145Carnegiea gigantea

(Caryophyllales)

0 38Years

146Saxifraga cotyledon

(Saxifragales)

0 7Years

147Rumex rupestris(Caryophyllales)

0 6Years

148Taraxacum officinale

(Asterales)

0 21Years

149Chamaecrista keyensis

(Fabales)

0 20Years

150Tolumnia variegata

(Asparagales)

0 8Years

151Centaurea corymbosa

(Asterales)

0 11Years

152Zea diploperennis

(Poales)

0 11Years

153Aquilegia sp.(Ranunculales)

0 10Years0

0.5

1154

Tillandsia punctulata(Poales)

0.0

2.5

5.0

0 653Years

155Sarracenia alata

(Ericales)

0 5Years

156Cirsium dissectum

(Asterales)

0 10Years

157Lupinus tidestromii

(Fabales)

0 9Years

158Allium tricoccum

(Liliales)

0 27Years

159Anthyllis alpicola

(Fabales)

0 33Years

160Echeveria longissima

(Saxifragales)

0 5Years

161Cleistes varicata 2

(Asparagales)

0 16Years

162Viola stagnina(Malpighiales)

0 81Years

163Primula vulgaris

(Ericales)

0 272Years

164Duguetia neglecta

(Magnoliales)

0 11Years

165Cryptantha flava

(Lamiales)

0 32Years

166Aspasia principissa

(Asparagales)

0 9Years

167Bothriochloaischaemum

(Poales)

0 32Years

168Betula nana

(Fagales)

0 10Years

169Tillandsia deppeana

(Poales)

0 15Years

170Hydrangea paniculata

(Cornales)

0 36Years

171Pedicularisfurbishiae

(Malpighiales)

0 33Years

172Cytisus scoparius

(Fabales)

0 82Years

173Iriartea deltoidea

(Asparagales)

0 8Years

174Hypochaeris radicata

(Asterales)

0 15Years

175Lomatium bradshawii

(Apiales)

0 313Years0

0.5

1176

Garcinia lucida(Malpighiales)

0.0

2.5

5.0

0 72Years

177Pseudophoenix

sargentii(Arecales)

0 33Years

178Annamocarya sinensis

(Malvales)

0 77Years

179Swallenia alexandrae

(Poales)

0 26Years

180Manilkara zapota

(Ericales)

0 5Years

181Espeletia spicata

(Asterales)

0 641Years

182Molinia caerulea

(Poales)

0 9Years

183Viola pumila(Malpighiales)

0 311Years

184Paronychia pulvinata

(Caryophyllales)

0 20Years

185Lobularia maritima

(Brassicales)

0 43Years

186Atriplex canescens

(Caryophyllales)

0 6Years

187Dicerandra frutescens

(Lamiales)

0 3Years

188Ailanthus altissima

(Sapindales)

0 3Years

189Mimulus guttatus

(Lamiales)

0 158Years

190Araucaria hunsteinii

(Pinales)

0 142Years

191Atriplex vesicaria(Caryophyllales)

0 102Years

192Rourea induta

(Oxalidales)

0 11Years

193Pinguicula villosa

(Lamiales)

0 5Years

194Ambrosia deltoidea

(Asterales)

0 33Years

195Tillandsia

macdougallii(Poales)

0 758Years

196Encephalartos

villosus(Cycadales)

0 171Years

197Opuntia rastrera(Caryophyllales)

0 5Years0

0.5

1198

Oenothera deltoides(Myrtales)

0.0

2.5

5.0

0 1276Years

199Acacia bilimekii

(Fabales)

0 15Years

200Astragalus tyghensis

(Fabales)

0 106Years

201Agrimonia eupatoria

(Rosales)

0 29Years

202Andropogon semiberbis

(Poales)

0 43Years

203Trifolium montanum

(Fabales)

0 297Years

204Sclerocarya birrea

(Sapindales)

0 147Years

205Ardisia

escallonioides(Ericales)

0 6Years

206Disporum sessile

(Liliales)

0 6Years

207Festuca gracillima

(Poales)

0 39Years

208Silene regia

(Caryophyllales)

0 59Years

209Geum rivale

(Rosales)

0 16Years

210Syzygium jambos

(Myrtales)

0 5Years

211Eryngium cuneifolium

(Apiales)

0 20Years

212Werauhia

sanguinolenta(Poales)

0 41Years

213Aechmea magdalenae

(Poales)

0 28Years

214Lindera umbellata

(Laurales)

0 41Years

215Achnatherumcalamagrostis

(Poales)

0 12Years

216Haplopappus radiatus

(Asterales)

0 13Years

217Gentiana pneumonanthe

(Gentianales)

0 186Years

218Quercus rugosa

(Fagales)

0 35Years

219Ramonda myconi

(Lamiales)

0 5Years0

0.5

1220

Oxalis acetosella(Oxalidales)

0.0

2.5

5.0

0 28Years

221Scorzonera hispanica

(Asterales)

0 35Years

222Hudsonia montana

(Malvales)

0 3Years

223Aquilaria microcarpa

(Malvales)

0 595Years

224Euterpe edulis

(Arecales)

0 13Years

225Dodonaca angustifolia

(Sapindales)

0 6Years

226Catopsis sessiliflora

(Poales)

0 105Years

227Stryphnodendron

excelsum(Fabales)

0 22Years

228Calocedrus macrolepis

(Pinales)

0 5Years

229Carex humilis

(Poales)

0 6Years

230Neodypsis decaryi

(Arecales)

0 33Years

231Pterocarya rhoifolia

(Fagales)

0 51Years

232Abies magnifica

(Pinales)

0 186Years

233Borassus aethiopum

(Arecales)

0 30Years

234Machaerium cuspidatum

(Fabales)

0 302Years

235Juniperus procera

(Pinales)

0 24Years

236Lepidium davisii

(Brassicales)

0 6Years

237Aquilegia chrysantha

(Ranunculales)

0 11Years

238Hilaria mutica

(Poales)

0 998Years

239Myrsine guianensis

(Ericales)

0 78Years

240Chamaelirium luteum

(Liliales)

0 7Years

241Laminaria digitata

(Laminariales)

0 3Years0

0.5

1242

Limonium carolinianum(Caryophyllales)

0.0

2.5

5.0

0 209Years

243Kosteletzkyapentacarpos

(Malvales)

0 42Years

244Acer rurinerve

(Sapindales)

0 18Years

245Sanicula europaea

(Apiales)

0 499Years

246Roupala montana

(Proteales)

0 38Years

247Pinguicula alpina

(Lamiales)

0 4Years

248Austrostipaaristiglumis

(Poales)

0 59Years

249Pinus lambertiana

(Pinales)

0 38Years

250Miconia prasina

(Myrtales)

0 45Years

251Viburnum furcatum

(Dipsacales)

0 32Years

252Pinus kwangtungensis

(Pinales)

0 4Years

253Eupatoriumperfoliatum(Asterales)

0 65Years

254Magnolia salicifolia

(Magnoliales)

0 4Years

255Phyllanthus emblica

(Malpighiales)

0 61Years

256Geonoma macrostachys

(Arecales)

0 51Years

257Trillium grandiflorum

(Liliales)

0 22Years

258Actaea spicata(Ranunculales)

0 43Years

259Tachigali vasquezii

(Fabales)

0 33Years

260Cassia nemophila

(Fabales)

0 12Years

261Gardenia actinocarpa

(Gentianales)

0 25Years

262Ulex minor(Fabales)

0 158Years

263Sarcocapnos baetica

(Ranunculales)

0 40Years0

0.5

1264

Pentaclethramacroloba(Fabales)

0.0

2.5

5.0

0 40Years

265Parashorea chinensis

(Magnoliales)

0 150Years

266Sarracenia purpurea

(Ericales)

0 3Years

267Rhopalostylis sapida

(Arecales)

0 277Years

268Ardisia elliptica

(Ericales)

0 215Years

269Hyparrhenia diplandra

(Poales)

0 76Years

270Eremospathamacrocarpa

(Arecales)

0 40Years

271Calochortuspulchellus

(Liliales)

0 19Years

272Cleome droserifolia

(Brassicales)

0 12Years

273Arisaema serratum

(Alismatales)

0 13Years

274Arisaema triphyllum

(Alismatales)

0 21Years

275Pinus ponderosa

(Pinales)

0 12Years

276Tillandsiamulticaulis

(Poales)

0 92Years

277Rhododendron ponticum

(Ericales)

0 409Years

278Silene acaulis(Caryophyllales)

0 56Years

279Scorzonera humilis

(Asterales)

0 36Years

280Pinguicula vulgaris

(Lamiales)

0 17Years

281Acer mono(Sapindales)

0 4Years

282Chlorocardium rodiei

(Laurales)

0 198Years

283Minuartia obtusiloba

(Caryophyllales)

0 550Years

284Encephalartos

cycadifolius(Cycadales)

0 3Years

285Cirsium palustre

(Asterales)

0 81Years0

0.5

1286

Sarcocapnospulcherrima

(Ranunculales)

0.0

2.5

5.0

0 386Years

287Calocedrus decurrens

(Pinales)

0 18Years

288Armeria maritima

(Caryophyllales)

0 10Years

289Mimulus lewisii

(Lamiales)

0 4Years

290Mimulus cardinalis

(Lamiales)

0 30Years

291Harrisia fragrans(Caryophyllales)

0 31Years

292Mauritaria flexuosa

(Arecales)

0 70Years

293Tsuga canadensis

(Pinales)

0 239Years

294Dicymbe altsonii

(Fabales)

0 30Years

295Sabal yapa(Arecales)

0 69Years

296Pterocarpusangolensis(Fabales)

0 36Years

297Silene

douglasii(Caryophyllales)

0 45Years

298Primula elatior

(Ericales)

0 52Years

299Phytelephas seemannii

(Arecales)

0 9Years

300Styrax obassia

(Ericales)

0 16Years

301Acer amoenum

(Sapindales)

0 22Years

302Lepanthes rupestris

(Asparagales)

0 294Years

303Rumex obtusifolius

(Caryophyllales)

0 84Years

304Pinus nigra

(Pinales)

0 41Years

305Dacrydium elatum

(Pinales)

0 16Years

306Neobuxbaumiamacrocephala(Caryophyllales)

0 20Years

307Pterocereus gaumeri

(Caryophyllales)

0 3Years0

0.5

1308

Mammillariapectinifera

(Caryophyllales)

0.0

2.5

5.0

0 23Years

309Mammillaria

magnimamma(Caryophyllales)

0 48Years

310Avicennia germinans

(Lamiales)

0 5Years

311Cynoglossumvirginianum(Lamiales)

0 20Years

312Tillandsia juncea

(Poales)

0 3Years

313Eupatorium resinosum

(Asterales)

0 5Years

314Bouteloua rigidiseta

(Poales)

0 178Years0

0.5

1315

Miconia albicans(Myrtales)

0.0

2.5

5.0

0 6Years

316Zamia amblyphyllidia

(Cycadales)

0 101Years

317Avicennia marina

(Lamiales)

0 8Years

318Astrocaryum mexicanum

(Arecales)

0 137Years

319Bertholletia excelsa

(Ericales)

0 16Years

320Neobuxbaumia tetetzo

(Caryophyllales)

0 100Years

321Nothofagus fusca

(Fagales)

0 320Years0

0.5

1322

Aesculus turbinata(Sapindales)

0.0

2.5

5.0

0 9Years

323Araucaria

cunninghamii(Pinales)

0 6Years

324Lindera benzoin

(Laurales)

0 3Years

325Neobuxbaumiamezcalaensis(Caryophyllales)

0 4Years

326Calathea ovandensis

(Caryophyllales)

0 25Years

327Prunus africana

(Rosales)

0 4Years

328Plantago media

(Lamiales)

0 9Years0

0.5

1329

Trilliumcamschatcense

(Liliales)

Weakly positive senescence

‘Negative’ senescence

• Great deal of variation among species.

• Huge majority incongruent with classical senescence theory.

• No pattern in relation to growth form, nor taxonomy.

Demographic trajectories in plants

Replication in plant demographySpatial replication in COMPADRE

Number of replicates

Freq

uenc

y

0 5 10 15 20 25 30 35

0

100

200

300

400

500

Temporal replication in COMPADRE

Length of study (yrs)

Freq

uenc

y

0 20 40 60

0

50

100

150

Spatial replication

Study length

• Most species are only known (demographically) from a single site.

• Most studies are about as long as a PhD.

• How representative are the data?

Demographic plasticity

• Response to ecological factors (population density, temperature, rainfall, nutrients, pH,...)

• Genetic differences.

• Will study-site selection affect life-history inferences?

• Will study-site selection affect estimates of phylogenetic signal?

• Can we do meaningful research with low replication?

How much does this variation really matter?

Within-species variation in senescence trajectories

Age (yrs)

Stan

dard

ised

mor

talit

y

0 5 10 15

01

23

45

Mortality

Age (yrs)

Stan

dard

ised

recr

uitm

ent

0 5 10 15

01

23

45

RecruitmentSt. Johns wort (Hypericum cumulicola)

Rock babyroot orchid (Lepanthes rupestris)

Age (yrs)

Stan

dard

ised

mor

talit

y

0 5 10 15 20

01

23

45

Mortality

Age (yrs)

Stan

dard

ised

recr

uitm

ent

0 5 10 15 20

01

23

45

Recruitment

Extract measures

• Mean age at first reproduction

• Mean life span

• Life expectancy at maturity

• Keyfitz’s entropy (survival)

• Demetrius’ entropy (degree of iteroparity)

• Phylogenetic signal

EntropyKeyfitz’s entropy

(survival)

Demetrius’ entropy(degree of iteroparity)

• High repeatability for age at maturity and Keyfitz entropy.

• Low repeatability for other traits.

Repeatability

Age atMaturity

Keyfitzentropy

Demetriusentropy

LifeExpectancy Lifespan

Trait

Rep

eata

bilit

y

0.0

0.2

0.4

0.6

0.8

1.0

Phylogenetic signalDemetrius

entropyKeyfitz’sentropy

Age atmaturity

Life expectancyat maturity

Life span

K

Frequency

0.0 0.2 0.4 0.6 0.8 1.0

050

100

150

200

p−value

Frequency

0.0 0.2 0.4 0.6 0.8 1.0

0200

400

600

800

K0.0 0.2 0.4 0.6 0.8 1.0

p−value0.0 0.2 0.4 0.6 0.8 1.0

K0.0 0.2 0.4 0.6 0.8 1.0

p−value0.0 0.2 0.4 0.6 0.8 1.0

K0.0 0.2 0.4 0.6 0.8 1.0

p−value0.0 0.2 0.4 0.6 0.8 1.0

K0.0 0.2 0.4 0.6 0.8 1.0

p−value0.0 0.2 0.4 0.6 0.8 1.0

Using methods from Ives et al. 2007

Conclusions

• Plant demography is incongruent with classical senescence theory.

• There’s plenty of data available to address plant comparative demography.

• ... but we lack replication.

• Trait selection may be critical.

• Opportunity for research into demographic plasticity.

Acknowledgements

✴ Jonathan Silvertown and Miguel Franco for starting COMPADRE.

✴ “Compadrinos” - for data entry.

✴ Max Planck Institute for Demographic Research

✴ Max Planck Institute Independent Research Group for Modeling the Evolution of Aging

Demographic trajectories in plantsArisaema triphillum

Cypripedium acaule

Pinus palustris

Silvertown et al. (2001)