Ecological consequences and ontogeny of seed ... - Accueil du site

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Ecological consequences and ontogeny of seed heteromorphism 

Eric Imbert 

Institut des Sciences de l’Evolution, Université Montpellier II, France 

Received: 9 October 2001 · Revised version accepted: 22 February 2002 

Introduction 

Abstract 

Seed heteromorphism represents the production of different kinds of seeds by a single individual. 

The morphological differentiation affects either the fruit – heterocarpy – or the seed sensu stricto 

– heterospermy. In this study the phylogenetic distribution of seed heteromorphism among different 

families and habitats is investigated for 218 plant species based on existing literature. The 

ecological consequences of seed heteromorphism are explored as well. Seed heteromorphism is 

most common in the Asteraceae and Chenopodiaceae, suggesting that these families have morphological 

characteristics favouring the appearance of seed heteromorphism and ecological features 

that maintain it. Using the distribution of seed heteromorphism within the genus Crepis, 

the relationship between seed heteromorphism and life cycle and habitats is examined. From this 

analysis it appears that heterocarpic species are often monocarpic. In contrast, the relationship 

between heterocarpy and habitats is not obvious. Finally, a synthesis is presented about the ontogeny 

of heteromorphism and some guidelines are proposed for future research on this topic. 

Key words: bet-hedging, dispersal, germination, plasticity, seed morphology 

Seeds are defined as units of sexual reproduction developed 

from a fertilised ovule containing an embryo, 

usually a supply of stored nutrients and a protective 

coat (Hickey & King 2000). However, in a wider sense 

the term is often used including diaspores that are actually 

fruits, i.e. seeds plus maternal tissue from the 

ovary. In the present review the term seed is used in a 

broad sense, i.e. a unit of dispersal resulting from sexual 

reproduction, but seed sensu stricto and fruit are 

distinguished when necessary. 

Perspectives 

in Plant Ecology, 

Evolution and 

Systematics 

While early theoretical models suggested that stabilizing 

selection on seed size and seed morphology 

should be intense (Smith & Fretwell 1974; McGinley 

et al. 1987), most plant species show a continuous 

intra-individual variation for seed mass and/or seed 

morphology (Harper et al. 1970; Fenner 1985). For 

instance, in many Asteraceae, the achene size decreases 

in a continuous pattern from the periphery towards 

the centre of the capitulum, while the pappus size increases 

(Zohary 1950; McGinley 1989). In some 

species, the intra-individual variation, often occurring 

within the same infrutescence, is tremendous and differ- 

Corresponding author: Eric Imbert, Institut des Sciences de l’Evolution, CC065, Université Montpellier II, 34095 Montpellier Cedex 5, France; 

Phone: +33-4 67 14 49 10, Fax: +33-4 67 14 26 22, e-mail: imbert@isem.univ-montp2.fr 

1433-8319/02/5/01-13 $ 15.00/0

14 E. Imbert 

ent types (or morphs) of seeds or fruits can be defined. 

This variation is associated with heteromorphism, 

which is an example of phenotypic variation as it 

refers to within-individual variation. Therefore, seed 

heteromorphism can be defined as the production of 

different types of seeds by a single individual. 

Plant ecologists have neglected intra-specific variation 

in seed size for a long time, because such variation 

was considered negligible compared to that occurring at 

the interspecific level (Harper et al. 1970; Fenner 1985). 

Conversely, early botanists recognised this feature as 

an important character for species diagnosis, and 

intra-individual variation in seed morphology has even 

been used to name some genera and species. Dimorphotheca 

in the Asteraceae, (named by C. Moench 

1744–1805; biographic data of botanical authors are 

from Mabberley 1997) and Heterotheca (named by 

A.H.G. Cassini 1781–1832) for example, include in 

their names the Greek word theke, meaning seed and 

clearly refer to different forms of seeds. M.C. Durieu 

de Maisonneuve (1796–1878) used the production of 

different fruits to name the species Ceratocapnos heterocarpa 

(Fumariaceae), carpos meaning fruit. 

Several words or expressions can be found in the literature 

to describe this character. In his Population Biology 

of Plants, Harper (1977) used the expression 

“somatic polymorphism” to signify that the phenotypic 

differentiation among seeds is “not a genetic segregation 

but a somatic differentiation” (Harper 1977, 

p. 69). However, the term polymorphism commonly 

refers to a differentiation among individuals, in particular 

“genetic polymorphism”, thus Venable (1985a) 

suggested the use of the term “heteromorphism”. 

Hannan (1980) suggested “heterospermy” for differentiation 

among seeds and “heterocarpy” for differentiation 

among fruits. Mandák (1997) proposed a more 

complete classification of seed heteromorphism based 

on diaspore morphology and other features. In the 

present study, seed heteromorphism is used in its 

broad sense, and heterospermy and heterocarpy are 

distinguished when necessary. 

The review deals with both the ecological consequences 

of differentiation among seed morphs and the 

ontogeny of seed heteromorphism in angiosperms. 

However, before considering these topics in detail, it is 

important to describe the nature of the differentiation 

among morphs, and in particular to distinguish continuous 

variation and heteromorphism. For most species 

classified as seed heteromorphic, the differentiation 

among morphs is obvious. For instance, the variation 

of achene shape in Calendula sp. is a well-known example 

of heterocarpy, and in many Calendula species 

(C. arvensis, C. stellata for instance), three or four achene 

morphs are present (Heyn et al. 1974). However, 

plant species commonly show intra-individual varia- 

Perspectives in Plant Ecology, Evolution and Systematics (2002) 5, 13–36 

tion in seed size, either mass or length. This variation 

can also be observed for other structures as pappus or 

wing. Therefore, the distinction between continuous 

variation and heteromorphism can be difficult. In such 

cases, I propose to associate heteromorphism to a clear 

bimodal (for dimorphism) or multimodal distribution. 

Venable (1985a) defined seed heteromorphism as 

“the production by single individuals of seeds of different 

form or behavior”. Behaviour means ecological 

behaviour, i.e. mainly dispersal ability and germination 

requirements. There are several examples of differentiation 

in ecological behaviour without any morphological 

difference. For instance, in the Cistaceae, 

seeds are protected by a very hard seed coat, and seeds 

can only germinate when high temperatures, provoked 

by fire, destroy this seed coat. However, some seeds 

are morphologically identical to the previous ones but 

lack a hard seed (Vuillemin & Bulard 1981). This 

leads to “germination heterochrony”, a character that 

is probably be very common in plant species (Harper 

1977; Westoby 1981; Silvertown 1984; Fenner 1985). 

Burke (1995) also described a case of seed heteromorphism 

sensu Venable in the Asteraceae Geigeria alata. 

In this species from the Namib desert, plants produce 

seed heads at the base and along the main stem, but 

there are no morphological differences between the 

achenes according to the position of the seed head 

(Burke 1995). The only difference is in relation to dispersal 

ability, since basal achenes are less dispersed 

than aerial ones (Burke 1995). These two examples of 

ecological differentiation in absence of apparent morphological 

differences illustrate the idea of “cryptic 

heteromorphism”. This character is supposed to be 

very common in angiosperms (Silvertown 1984; Venable 

1985a) although underestimated. In the present 

review, some cases of well-described cryptic heteromorphism 

are included. 

The taxonomic distribution of seed 

heteromorphism and its nature 

The collection of data is based on an extensive literature 

survey. To avoid synonymous species names, I checked 

each species using the Global Provisional Checklist created 

by the International Organization for Plant Information 

(www.bgbm.fu-berlin.de/IOPI/GPC/default.htm; last 

updated 27 November 2000). This checklist includes 

information from Flora Europaea, the USDA Plants 

Database and the Med-Checklist. I included 218 species 

with either heterocarpy or heterospermy (Appendix; 

note that only 170 are referenced in the Global Provisional 

Checklist); the number of species is similar to 

the one proposed by Flint & Palmblad (1978). Because 

it is not feasible to check the seeds of the ca.

250,000 angiosperm species, the present list is of 

course not exhaustive. However, the present list may 

serve for a comparison among angiosperm families. 

Seed heteromorphism has been described in 18 families 

of angiosperms (Table 1), but the dominance of 

Asteraceae and Chenopodiaceae is obvious, as 63% of 

the recorded species belonged to Asteraceae (52% of 

the genera) and 8% belonged to Chenopodiaceae 

(10% genera). Seven families are represented by only 

one species and ten with only one genus (Table 1). This 

distribution does not reflect species diversity within 

each family, as Asteraceae account for less than 10% 

of the angiosperm species and 12% of the genera. For 

the Chenopodiaceae, the corresponding values are 

0.5% and 0.8%, respectively. Furthermore, some families 

have a species diversity of the same magnitude as 

the Asteraceae (e.g. Fabaceae, Table 1), but seed heteromorphism 

is infrequent in these families (Table 1). 

Therefore, it can be tentatively concluded that, 

within the angiosperms, the character occurs more frequently 

in Asteraceae and Chenopodiaceae. This dominance 

of Asteraceae has also been observed for the 

Flora of Israel (Ellner & Shmida 1981). 

Asteraceae 

Differentiation in this family mainly occurs among the 

achenes (single-seeded fruits, i.e. heterocarpy) in the periphery 

of the capitulum (peripheral achenes) and those 

in the centre of the capitulum (central achenes). Actually, 

seed dimorphism is common, but for several species, 

Table 1. Systematic repartition of heterocarpic or heterospermic species 

(see complete list in Appendix). Data for number of species and genera per 

family are from Mabberley (1997). 

Family Seed heteromorphic species Total diversity 

No. species No. genera No. species No. genera 

Apiaceae 3 3 3540 446 

Asteraceae 138 52 22750 1528 

Brassicaceae 12 8 2350 365 

Caryophyllaceae 11 2 2300 87 

Chenopodiaceae 18 10 1300 103 

Cistaceae 4 1 175 8 

Commelinaceae 1 1 640 39 

Euphorbiaceae 1 1 8100 313 

Fabaceae 5 5 18000 642 

Fumariaceae 1 1 530 17 

Nyctaginaceae 9 1 390 30 

Papaveraceae 2 2 230 23 

Plantaginaceae 1 1 275 3 

Poaceae 7 7 9500 668 

Polygonaceae 1 1 1100 46 

Rubiaceae 1 1 10220 630 

Thymelaceae 1 1 750 53 

Valerianaceae 2 1 300 10 

TOTAL 218 99 – – 

Consequences and ontogeny of seed heteromorphism 15 

intermediate achenes can be found. Such achenes have a 

similar morphology to both the peripheral type and 

central one, and are in an intermediate position within 

the seed head (Zohary 1950; Pomplitz 1956; Bachmann 

1983). Peripheral and central achenes differ in size, 

presence/absence of dispersal structures (e.g. pappus, 

trichomes), colour and shape. Peripheral achenes are 

typically heavier than central ones, e.g. in Bidens sp., 

Crepis sancta, Hedypnois cretica and Picris sp. For instance 

the weight of peripheral achenes is four times 

greater than that of central ones in Picris amalecitana 

(Ellner & Shmida 1984). For a few species, central achenes 

are heavier than peripheral ones (Carduus pycnocephalus 

and C. tenuiflorus, Olivieri & Berger 1985; Picris 

radicata, Ellner & Shmida 1984). The mass difference 

is mainly due to differences in embryo size, but in 

few species the difference is also due to the structure 

and thickness of the pericarp (Crepis sancta, Imbert et 

al. 1999; Dimorphotheca sinuata, Beneke et al. 1992a; 

Heterotheca subaxillaris, Venable & Levin 1985a). 

In addition to a difference in size, there is variation in 

dispersal structures within a seed head. For example, 

peripheral achenes do not have a pappus in Carthamus 

lanatus, Centaurea solstitialis, Charieis heterophylla, 

Crepis sancta, Hedypnois cretica, Hemizonia increscens, 

Heterotheca sp., Picris galilea, Grindelia papposa and 

Senecio jacobea, but they bear a residual pappus in Laya 

platyglossa and Picris echioides (references in Appendix). 

In Bidens tripartita, peripheral and central achenes differ 

in the number and size of awns (Montégut 1970). In 

Anthemis chia, peripheral achenes have a large wing 

whereas central achenes do not have any wing (Feinbrun-Dothan 

& Zohary 1978). Finally, the size of the 

beak bearing the pappus varies in several species (Crepis 

foetida, E. Imbert, pers. observ.; Hypochoeris glabra, 

Baker & O’Dowd 1982). In Crepis leontodontoides, 

Hedypnois cretica, Picris echioides and Picris galilea, 

peripheral achenes remain enclosed in the involucral 

bracts, while in Anacyclus arenaria, Calendula stellata, 

Carduus tenuiflorus, Hedypnois arenaria and Leontodon 

taraxacoides they remain enclosed in the whole seed 

head (Appendix). In both cases, the dispersal unit is not 

only the achene but the achene combined with another 

structure, whereas central achenes disperse normally. 

Achene morphs can also differ in colour (e.g. Crepis 

sancta), the ornament on the pericarp (Chrysanthenum 

sp.) or shape (Calendula sp.). 

However, not all differentiation involves the position 

of the achene. In the annual Heterosperma pinnatum, 

achenes also vary within a head but there is no relation 

between position and morphology (Venable et al. 1987). 

Gardocki et al. (2000) reported that all different seed 

morphs are produced by peripheral florets in a Calendula 

species. In Gymnarhena micrantha, heterocarpy is associated 

with amphicarpy, i.e. the production of both 

Perspectives in Plant Ecology Evolution and Systematics (2002) 5, 13–36

16 E. Imbert 

aerial and subterranean flowers, and subterranean seeds 

are heavier than aerial ones and both morphs also differ 

in morphology (Koller & Roth 1964). Catananche lutea 

also produces subterranean achenes that differ from 

aerial ones, but in addition there is differentiation between 

peripheral and central achenes in the aerial capitula 

(Ruiz de Clavijo 1995). Finally, heterospermy can be 

found in the genus Xanthium. In Xanthium species, the 

fruit contains two seeds, and the upper seed is heavier 

than the lower one (see references in Appendix). 

Chenopodiaceae and Nyctaginaceae 

In the genus Atriplex and the species Halogeton glomeratus, 

the unit of dispersal (the anthocarp; Wilson 1974) is 

composed of a fruit and bracts surrounding it, that result 

from the development of the sepals. In some Atriplex 

species (Appendix), the shape and colour of bracts vary 

according to their position around the axis, whereas in 

Halogeton glomeratus the different seed morphs are produced 

at different stages during the life cycle (Williams 

1960). In Chenopodium album the pericarp is either 

reticulate or smooth, and either black or brown, leading 

to four seed morphs (Williams & Harper 1965). Therefore, 

this differentiation is related to heterocarpy. 

In Salicornia sp. the inflorescence consists of a central 

flower and usually two lateral flowers, and each 

flower has only one ovule. In most species central seed 

mass is greater than lateral ones (Davy et al. 2001), 

but seed dimorphism is really important only in Salicornia 

europaea (Ungar 1979; Davy et al. 2001). Furthermore, 

the perianth of central flowers remains 

closed after seed maturation, which reduces seed dispersal, 

whereas lateral seeds disperse normally. Heterospermy 

can also be found in two Chenopodiaceae 

species, Aellinia autrani and Salsola volkensii, where 

individuals produce single-seeded fruits, containing 

either a green embryo or a yellow embryo without 

chlorophyll (Negbi & Tamari 1963). In Salsola komarovii 

the differentiation affects both the fruit (long- or 

short-winged) and the seed (green or yellow embryo; 

Takeno & Yamaguchi 1991). 

In the Abronia genus (Nyctaginaceae, a family close to 

Caryophyllaceae; Mabberley 1997) the unit of dispersal 

is also an anthocarp, resulting from the development of 

the lower part of the perianth that forms lobes or wings 

around the seed (Wilson 1974; Wiggins 1980). Morphological 

changes of the anthocarp within an inflorescence 

include the existence, number and size of the lobes. 

Caryophyllaceae 

In the genus Spergularia, heterospermy has been described 

in some species, in particular in the two closely 

related species Spergularia maritima and S. marina. In S. 


maritima seeds are usually winged, but some individuals 

produce capsules containing both numerous winged 

seeds and a few wingless ones. In S. marina the relation is 

reverse: winged seeds are fewer than wingless seeds. For 

both species individuals with homomorphic seeds are the 

most frequent in natural populations (Telenius 1992). 

Several arguments demonstrate that heteromorphic individuals 

are not hybrids between the two species (Sterk 

1969). In particular, heterospermic individuals can be 

found in monospecific populations (Salisbury 1958). 

Brassicaceae 

In Cakile sp. fruits consist of two segments, each containing 

one seed. The seed in the upper position is larger 

than the one in lower position. Furthermore, at maturity 

only the upper seed is dispersed (see references in 

Appendix). The fruit type of many species within this 

family, the silique, is a two-valved vessel that is normally 

dehiscent. Three species, Aethionema carneum, 

A. heterocarpum and A. saxatile, are heterocarpic since 

individuals produce both many-seeded dehiscent siliques 

and one-seeded indehiscent siliques (Zohary 1966; Andersson 

et al. 1983). In Sinapsis alba, Erucaria boveana, 

Fezia pterocarpa and Hirschfeldia incana the silique is 

not completely dehiscent, and seeds in the distal part 

do not disperse (see Appendix). Finally, in Cardamine 

chenopodifolia plants produce both aerial fruits containing 

many light seeds and subterranean siliques containing 

few (even one) but heavy seeds (Battandier 

1883; Cheplick 1983). 

Fabaceae and Poaceae 

In the Fabaceae heteromorphism is associated with amphicarpy, 

and subterranean pods have heavier seeds 

than aerial ones (e.g. 3 vs. 1.5 g in Vicia sativa; Plitmann 

1973). In Amphicarpaea bracteata plants produce 

both aerial flowers, that are either chasmogamous 

or cleistogamous, and subterranean cleistogamous 

flowers. Pods and seeds from aerial flowers are identical, 

but pods from subterranean flowers contain a single 

seed much larger than aerial ones, and are surrounded 

by a thinner seed coat (see references in Appendix). 

In the Poaceae heteromorphism is also associated with 

amphicarpy in Amphicarpum purshii and others (see 

Campbell et al. 1983). In Agrostis hiemalis, Amphibromus 

scabrivalvis, Danthonia spicata, Nasella leucotricha 

and Triplasis purpurea seeds from cleistogamous flowers 

are heavier than those from chasmogamous flowers. 

Various examples 

Subterranean fruits are six times heavier than aerial 

ones (mean 18.3 vs. 2.7 mg) in the amphicarpic Com-

melina benghalensis (Commelinaceae; Budd et al. 1979), 

and four times heavier in Emex spinosa (Polygonaceae) 

(60 vs. 15 mg; Weiss 1980). Variation in pericarp 

morphology occurs in Asperula arvensis (Rubiaceae), 

Torilis nodosa (Apiaceae) and Eremocarpus 

setigerus (Euphorbiaceae). In the last species there is 

an important polymorphism among individuals for the 

colour of the pericarp (black or white) and its ornament 

(mottled or uniform). Few individuals produce 

an intermediate colour, i.e. grey seed, during their 

senescent phase (Cook et al. 1971). 

Other particular, and sometimes complex, examples of 

seed heteromorphism can be found in Ceratocapnos heterocarpus 

(Fumariaceae), Plantago coronopus (Plantaginaceae), 

Platystenom californicus (Papaveraceae), and 

Fedia spp. (Valerianaceae; see references in Appendix). 

Ecological consequences of seed 

heteromorphism 

Dispersal ability 

For most seed-heteromorphic and especially amphicarpic 

species, seed morphs differ in their dispersal ability. Typically 

in Asteraceae, peripheral achenes achieve lower dispersal 

than central achenes (Burtt 1977; Ellner & Shmida 

1984; McEvoy 1984; Venable & Levin 1985a; McEvoy 

& Cox 1987; Venable et al. 1987; Tanowitz et al. 1987; 

Imbert 1999). Telenius & Torstensson (1989) and Redbo- 

Torstensson & Telenius (1995) reported that winged 

seeds of Spergularia sp. are better dispersed by water than 

wingless seeds. In Cakile edentula, the upper segment of 

the silique is probably more efficiently water-dispersed 

than the lower part (Payne & Maun 1981). The development 

of bracts in Chenopodiaceae or the lobes of anthocarp 

in Abronia also affect dispersal ability (Wilson 1974; 

Mandák & Pysˇek 2001b). For some species, morphs differ 

in their dispersal agents. For instance, in Picris 

echioides (Asteraceae) peripheral achenes, that remain enclosed 

within the involucral bract, may experience exozoochorous 

dispersal by mammals, whereas central achenes 

are wind-dispersed (Sorensen 1978). Such differentiation 

for dispersal agents has been reported also for 

Hypochoeris glabra (Baker & O’Dowd 1982), and for 

Senecio jacobea (McEvoy 1984). Heterocarpy also occurs 

in zoochorous species: for instance Thymelea velutina 

produce both fleshy fruits dispersed by animals and dry 

barochorous fruits (Tébar & Llorens 1993). 

Dormancy and germination requirements 

Thickness and structure of the pericarp play a major 

role in germination, in particular for water absorption 

of the embryo tissue and for gas exchange (Taylorson 


& Hendricks 1977; Mohamed-Yasseen et al. 1994). In 

some Asteraceae of desert habitats the achenes remain 

enclosed within the involucral bracts, which form an 

important barrier against water absorption (Gutterman 

1993). Consequently, germination can only occur 

when rainfall is considerable, increasing the survival 

likelihood for seedlings. A similar strategy is found in 

some species with heteromorphic seed, such as the 

Chenopodiaceae in which the bracts enclosing the fruit 

are more or less permeable. Dormancy is influenced by 

differences in bract morphology among morphs (Beadle 

1952; Williams 1960; Williams & Harper 1965; 

Ungar 1971, 1979, 1987; Takeno & Yamaguchi 1991). 

Similarly, in the Brassicaceae seeds that remain enclosed 

within the silique show delayed germination 

compared those dispersed (Zohary 1962). A mixed 

strategy of germination has also been described for 

Platystemon californicus (Hannan 1980). McDonough 

(1975) compared water absorption between peripheral 

and central achenes in Grindelia squarrosa, and showed 

that water uptake was more rapid for central achenes. 

Actually, in many species with heteromorphic seed, the 

difference in seed size results from the structure of the 

pericarp or the mass ratio embryo/pericarp (Maurya 

& Ambasht 1973; Baskin & Baskin 1976; Burtt 1977; 

Flint & Palmblad 1978; Weiss 1980; Schat 1981; Clay 

1983; Ellner & Shmida 1984; McEvoy 1984; Venable 

& Levin 1985a; Ellner 1986; Tanowitz et al. 1987; Venable 

et al. 1987; Beneke et al. 1992a, b, 1993a; Rocha 

1996). This leads to a particular pattern of variation in 

germination dynamics: one morph (usually central achenes 

in the Asteraceae) germinates immediately when 

favourable conditions occur, while the second morph 

(peripheral achenes) shows delayed germination. 

Dormancy can also result from the chemical components 

of the seed coat (Mohamed-Yasseen et al. 1994). 

Experiments performed on Carduus (Bendall 1973) 

and Dimorphotheca species (Beneke et al. 1992a, 

1993a) suggest that the pericarp of each achene morph 

differ in their respective concentration of water-soluble 

germination inhibitors. In Salsola komarovii, shortwinged 

fruits contain more abscisic acid than longwinged 

ones, a difference that is associated with differences 

in germination rate (Takeno & Yamaguchi 1991). 

Finally, germination requirements (photoperiod, temperature, 

etc) can vary among morphs (Becker 1913; 

Koller 1957; Evenari 1963; Williams & Harper 1965; 

Cavers & Harper 1966; Brown & Mitchell 1984; Ruiz 

de Clavijo 1994). For instance, in the salt-tolerant species 

Salicornia europaea lateral and central seeds do not respond 

equally to salinity concentration (Grouzis et al. 

1976; Ungar 1979; Philipupillai & Ungar 1984; Berger 

1985). In contrast, for Arthrocnemum macrostachyum, 

salinity concentration greatly affects the final percentage 

of germination, but both seed morphs respond 


18 E. Imbert 

nearly equally to changes in salinity (Khan et al. 1998; 

Khan & Gul 1998). The absence of chlorophyll in yellow 

seeds of Salsola volkensii also affects dormancy 

(Negbi & Tamari 1963). 

Differences in pericarp morphology do not always influence 

germination. Arctotis fastuosa, Arthrocnemum 

macrostachyum, Centaurea soltistialis, Charieis heterophylla, 

Crepis sancta, Dimorphotheca pluvialis, Galinsoga 

parviflora and Hypochoeris glabra are all heteromorphic 

but the different morphs do not have different 

germination requirements (references in Appendix). Furthermore, 

heterochrony of germination can vary among 

populations (Venable et al. 1987; Kigel 1992). For instance, 

in Bidens bipinnata heterochrony between peripheral 

and central achenes is important in Asian populations 

(Dakshini & Aggarwal 1974), but reduced in 

South African populations (Brown & Mitchell 1984). 

The last point related to dormancy is the conservation 

of seed viability, i.e. the ability to remain viable 

when embryos cannot germinate. This character is poorly 

documented in species with heteromorphic seed, but 

is observed in heterocarpic Asteraceae (Imbert 1999). 

Yet, the delayed germination could be successful only 

if ungerminated seeds remain viable in the seed bank 

(Cohen 1966). Interspecific comparisons showed that 

large seeds, which contain more storage material and a 

thicker seed coat, could remain viable longer than 

small seeds (Priestley 1986). However, Thompson et 

al. (1993) suggested that there is a negative correlation 

between seed size and longevity. This pattern has been 

observed in Bidens pilosa (Rocha 1996), whereas in 

Crepis sancta the peripheral achenes are heavier and 

remain viable longer than central ones (Imbert 1999). 

Actually, it seems that seed viability is mainly determined 

by the hardness of the seed coat, which acts as a 

physical defence against humidity and fungal infection 

(Mohamed-Yasseen et al. 1994). For instance, in 

Atriplex semibaccata and Blackiella inflata hard and 

dark coloured seeds remain viable longer than soft and 

light ones (Beadle 1952). 

Seedling emergence, seedling survival and growth 

Differences among morphs are often associated with differences 

in embryo size; therefore, a difference in seedling 

success is expected. A positive relationship between seed 

size and seedling survival has been documented for a few 

species with heteromorphic seed (Koller & Roth 1964; 

Budd et al. 1979; Venable & Levin 1985a; Rai & Tripathi 

1987; Venable et al. 1987). Initial seedling size also 

influences reproductive output for some heteromorphic 

species (Weiss 1980; Cheplick & Quinn 1982; Venable 

& Levin 1985b; Schnee & Waller 1986; Ellison 1987; 

Beneke et al. 1993b). Plants germinating from the largest 

seeds often have a competitive advantage (Weiss 1980; 


Cheplick & Quinn 1982; Venable & Levin 1985b; Rai 

& Tripathi 1987; Imbert et al. 1997). 

For some species, plants from one seed morph appear 

to be more resistant to water stress (Koller & 

Roth 1964; Bendall 1973; Cheplick & Quinn 1982; 

Venable 1985b) or to nutrient deficiency (Galinsoga 

parviflora; Rai & Tripathi 1987). Such a difference 

suggests that the root/shoot ratio differs between plants 

from different seed morphs. Indeed, interspecific comparisons 

tend to show that larger embryos have a 

greater root/shoot ratio (Gleeson & Tilman 1994; but 

see Marañon & Grubb 1993). This difference has been 

also observed in intraspecific comparisons (Wulff 1986b), 

but in species with heteromorphic seed comparisons 

between morphs failed to show such difference (Baker 

& O’Dowd 1982; Beneke et al. 1993b). For instance, 

in the Asteraceae Crepis sancta peripheral achenes are 

three times heavier than central ones (0.27 vs. 0.10 mg; 

Imbert et al. 1996). Consistently, seedlings from peripheral 

achenes are larger than those from central 

ones (Table 2), and have greater above– and belowground 

parts, but the root/shoot ratio does not differ 

between the morphs (Table 2). Further experiments 

have shown that both morphs are equally affected by 

nutrient depletion (Imbert et al. 1997). Zhang (1995) 

reports similar results for Cakile maritima. 

Seed heteromorphism as 

a bet-hedging strategy 

It therefore appears that ecological differences between 

morphs can be important. This confirms the assertion 

of Harper (1977) who associated seed heteromorphism 

with a strategy combining “seeds for different 

ends or function ...”. The mixed strategy for germination, 

which has been established for at least thirty 

species, is presented as the major ecological conse- 

Table 2. Comparisons of seedling size between achene morphs in Crepis 

sancta (Asteraceae). For each achene morph one thousand achenes were 

germinated in Petri dishes, each dish containing one disk of Whatmann 

paper which was regularly supplied with distilled water. Measurements were 

made on the first hundred seedlings of each achene morph. Maximal diameter 

of the two cotyledons was measured immediately after emergence. 

Length of the radicle was measured when the seedling was totally separated 

from its seed coat. Once measured, seedlings were removed from the Petri 

dish. Seedlings were visited every 12 hours (means ± SE). 

Achene morph Cotyledon Radicle Root/shoot 

length (mm) length (mm) ratio 

Peripheral 5.40 ± 0.19 6.49 ± 0.22 1.41 ± 0.05 

Central 3.96 ± 0.05 4.67 ± 0.06 1.37 ± 0.04 

F 1,198 74.54 13.91 0.28 

P-value

quence of seed heteromorphism (Harper 1977; Lloyd 

1984; Silvertown 1984; Venable 1985a). Spreading 

offspring in time, resulting from variation in germination 

time, could be efficient to reduce sib competition 

(Cheplick 1996a). The efficiency of spreading individuals 

in time also represents a bet-hedging strategy, reducing 

temporal variance in fitness, which is advantageous 

in highly variable and unpredictable habitats 

(Slatkin 1974; Gillespie 1977; Kaplan & Cooper 

1984). This major consequence of seed heteromorphism 

has been clearly formalised with the High 

Risk/Low Risk strategy by Venable (1985a). 

Identically, intra-individual variation in seed morphology 

could optimise the respective seed shadows by 

maximising the spread of seeds in space (Augspurger 

& Franson 1993). For instance, in wind-dispersed 

seeds the dispersal distance depends on the terminal 

velocity that in turns depends on seed morphology 

(Sheldon & Burrows 1973). Therefore, any morphological 

variation contributes to variation in dispersal 

distance (Greene & Johnson 1989). Such variation is 

important to reduce density-dependent effects, and 

thus sib-competition, and to increase colonisation 

ability of new habitats. As presented above, in several 

species with heteromorphic seed, one morph has 

greater dispersal ability than the other one. This difference 

in dispersal is of interest, because the proportion 

of seeds that are potentially dispersed produced by a 

single individual can be related to the dispersal rate of 

its progeny. A number of theoretical models exist for 

evolution of dispersal rate, although these are typically 

used for animals (e.g. Johnson & Gaines 1990; Ronce 

et al. 2001). Thus, species with heteromorphic seed are 

appropriate to empirically test theoretical predictions 

about the dispersal rate in plant species (Olivieri & 

Gouyon 1985; Imbert 2001; Imbert & Ronce 2001). 

Furthermore, there is an obvious trend that associates 

low dispersal ability with high seed dormancy, while 

seed morphs with high dispersal show reduced dormancy 

(see also Olivieri & Berger 1985). This pattern 

fits with theoretical expectations about trade-offs between 

dispersal in space and in time (Venable & 

Lawlor 1980; Olivieri 2001). 

All these ecological differences represent ultimate 

factors assuring the evolutionary success of mixed 

strategy in seed morphology. Indeed, seed heteromorphism 

is adaptive when seed morphs differ in their ecological 

behaviour (Lloyd 1984; Venable 1985a). However, 

the maintenance of seed heteromorphism can also 

be explained by the positive effect of seed size on competitive 

ability, and the trade-off between seed size and 

the number of seeds produced by a single individual. 

Geritz (1995) showed that, considering these two selective 

forces, intra-individual variation in seed size represents 

an evolutionarily stable strategy (ESS) provided 


there is spatial variation in seedling density. Indeed, in 

safe sites where seed density is high, the heaviest seeds 

are advantageous, while in low-density conditions, a 

small seed size is not disadvantaged. As small seeds are 

more numerous, they have a greater probability to join 

sites where the density is low. This has to be related to 

the relation between seed size and dispersal ability 

(Venable & Brown 1988). It can also be shown that 

intra-individual variation for seed size represents an 

ESS in situations where seed predation is positively 

related to seed size (Geritz 1998). Recently, Fenner et 

al. (2002) demonstrated a positive relationship between 

capitulum size and pre-dispersal seed predation in 

some Asteraceae species. Therefore, considering the 

theoretical predictions obtained by Geritz (1998) and 

these observations, it can be suggested that seed size 

variation should be positively correlated to capitulum 

size. As a corollary, seed heteromorphism is supposed 

to occur more often in species with large capitula than 

in species with small capitula. More data concerning 

the predation rate in species with heteromorphic seed, 

and in particular data concerning differences in predation 

rate among seed morphs, are thus needed. 

Seed heteromorphism in the genus Crepis 

Because seed heteromorphism represents a mixed strategy 

reducing temporal variance in fitness, species with 

heteromorphic seed should mainly occur in unpredictable 

habitats such as the desert (Zohary 1962) and disturbed 

environments (Harper 1965). For instance, using the 

Flora of Israel, Ellner & Shmida (1981) observed that 

heteromorphism was more frequent in desert habitats 

(13.2% of 604 species) than in Mediterranean habitats 

(0.7 % of 1560 species). Telenius & Torstensson (1991) 

showed that Spergularia species with heteromorphic 

seeds mainly occurred in saltmarshes which can be considered 

as a frequently disturbed. 

It is also often stated that seed heteromorphism 

mainly occurs in monocarpic species, in particular because 

polycarpy allows spreading the risk of reproduction 

over several years, and thus it is also a bet-hedging 

strategy (Venable & Brown 1988). Consistently, 

Plitmann (1986) reported a significant association between 

annual life cycle and heterocarpy in Turkish 

Asteraceae. In contrast, this relation was not observed 

in the genus Spergularia (Telenius & Torstensson 

1991; see also Ellner & Shmida 1981). 

It is not possible to test directly both statements 

with the species surveyed in the present review, because 

ecological and phenological information about 

non-heteromorphic sister species is missing in most 

cases. To deal with this topic, I focused on the genus 

Crepis which is well represented within the Appendix. 


20 E. Imbert 

Fig. 1. Phylogenetic relationship among the 27 sections of the genus Crepis according to Babcock (1947). For section 15, the relations are numerous, and 

thus are not represented. For each section, the number of species is given; “H” symbolizes the presence of at least one heterocarpic species within the section. 

Babcock (1947) produced a monograph of this genus 

describing 196 species. Based on this study, 30 species 

can be considered as heterocarpic. In the Appendix, 

however, 28 Crepis species only are listed because two 

species described by Babcock are no longer recognised 

(C. cretica and C. corymbosa, see the Global Provisional 

Checklist). Because this review is based on the 

phylogenetic structure with 27 sections within the genus 

proposed by Babcock (1947, Fig. 1), it uses also the respective 

taxonomy. Although the phylogeny suggested 

by Babcock (1947) may change with time, it can still 


be used to test a phylogenetic pattern in seed heteromorphism. 

To test for association between annual life 

cycle and seed heteromorphism, species were arranged 

in two classes: monocarpic (annual and biennial 

species) and polycarpic (perennial species). For the relationship 

between habitats and seed heteromorphism, 

habitats were first classified in dry habitats (including 

desert, sclerophyllous communities, rocky and sandy 

places) and wet habitats (river verges, grassland, deciduous 

and tropical forests). In a second step, to test 

for an association between predictability of habitats

and presence/absence of seed heteromorphism, species 

were arranged in five classical biogeographical areas 

(mediterranean, desert, tropical, continental, and temperate) 

assuming a greater unpredictability in mediterranean 

and desert areas than in other biomes, which is 

commonly stated in particular for annual precipitations 

(Ellner & Shmida 1981; Petit 1990). Mountains 

were added as a sixth biogeographical unit, and species 

were included in this category when their distribution 

were limited to mountainous habitats; this biome was 


Fig. 2. The relationship between presence/absence of heterocarpy and life cycle (monocarpic or polycarpic) in Crepis according to the phylogenetic relationship 

among the 27 sections (from Babcock 1947). “H” symbolizes the presence of at least one heterocarpic species in the section. Box with full lines, all 

species polycarpic; box with bold lines, all species monocarpic; and box with broken lines, the section contains both monocarpic (M) and polycarpic (P) species. 

Numbers represent section numbers (cf. Fig. 1). 

considered as predictable. Crepis species were sorted 

according to the description given by Babcock (1947). 

No statistical test was used since the data cannot be 

considered as independent. 

The heterocarpic species belong to 12 different sections, 

and it can be suggested that seed heteromorphism has 

evolved independently several times within the genus 

(Fig. 1). However, heterocarpy and monocarpy seem to be 

associated (Fig. 2). For instance, in section 20 (9 spp.) and 

section 26 (7 spp.) all species are monocarpic and these 


22 E. Imbert 

Fig. 3. The relationship between presence/absence of heterocarpy and habitat characteristics (wet vs dry) in Crepis according to the phylogenetic relationship 

among the 27 sections (from Babcock 1947). “H” symbolizes the presence of at least one heterocarpic species in the section. Box with full lines, all species 

occur in wet habitats; box with bold lines, all species occur in dry habitats; and box with broken lines, the section contains species from dry (D) and wet (W) 

habitats. Numbers represent section numbers (cf. Fig. 1). 

species, except one in each section, are heterocarpic. Furthermore, 

most heterocarpic species are monocarpic, and 24 

monocarpic species (out of 43, i.e. 55%) are heterocarpic 

(Table 3a). In the sections containing both monocarpic and 

polycarpic species and heterocarpic species (9, 19, 23, 25 

and 27, Fig. 2), heterocarpic species are more frequently 

monocarpic than polycarpic (Table 3a), and monocarpic 

species tend to be more often heterocarpic (6 out of 14, 

43%) than polycarpic species (3 out 19, 16%; Table 3a). 


Heterocarpic species occur more often either in dry 

habitats or in mediterranean-desert habitats (Table 3b). 

Considering only the sections where heterocarpic species 

occur or species that occupy either dry or wet habitats 

(Fig. 3), the association is less obvious as 13 heterocarpic 

species (out of 20) occupy dry habitats, while 

22 non-heterocarpic species (of 43) occupy the same 

habitats. Carrying out the same analysis with the biogeographical 

area (Fig. 4), heterocarpy appears as

Table 3. Number of heterocarpic and non-heterocarpic species in the 

genus Crepis according to (a) life cycle and (b) habitat. Data from Babcock 

(1947) but see text for details. Sections refer to phylogenetic relationship according 

to Babcock (1947, cf. Fig. 1). 

(a) Global data Sections 9, 19, 23, 25 and 27 

Mono- Poly- Total Mono- Poly- Total 

carpic carpic carpic carpic 

Heterocarpic 24 6 30 6 3 9 

Non-heterocarpic 19 147 166 8 16 24 

TOTAL 43 153 196 14 19 33 

(b) Habitat Biogeographical area 

Dry Wet Total Mediterranean Others Total 

+ desert 

Heterocarpic 21 9 30 25 5 30 

Non-heterocarpic 46 120 166 86 80 166 

TOTAL 67 129 196 111 85 196 

equally frequent in species present in mediterranean 

and desert areas (20 of 44) as in species occurring in 

other biogeographical area (5 of 11). 

Of course, an improved phylogeny of the genus Crepis 

– which is to be expected for the next years – and a phylogenetically 

corrected approach would further improve 

knowledge about the relationship between heterocarpy, 

life cycle and habitats. Furthermore, a similar analysis on 

other genera would be desirable. However, the present 

analysis suggests that heterocarpic species are more often 

monocarpic than polycarpic species, while the relationship 

between heterocarpy and habitats is less obvious. 

Ontogenetic constraints as proximate factors 

Environmental factors may produce morphological 

variation among repeated organs within the same individual, 

since plants have a modular architecture. For 

instance, ambient light conditions and osmotic pressure 

affect leaf size and shape in hydrophytes (Bachmann 

1983; Niklas 1997), and foliar morphology 

varies between immersed leaves and aerial ones (the socalled 

“heterophylly”, see Wells & Pigliucci 2000). 

This morphological differentiation corresponds to 

plasticity, i.e. the modification of the expression of a 

given genotype according to environmental conditions. 

Such a mechanism can explain heterocarpy observed in 

Halogeton glomeratus (Chenopodiaceae), as black and 

brown fruits are produced at different stages of the life 

cycle of a single plant, depending on light intensity and 


photoperiod (Williams 1960). Heterophylly can also 

result from changes in the state of the meristem due either 

to its position or to ageing (Bongard-Pierce et al. 

1996; Briggs & Walter 1997). A famous example is 

Hedera helix where leaves on vegetative stems are morphologically 

different from leaves on reproductive 

stems. Senescent plants of the Euphorbiaceae Croton 

setigerus produce seeds that differ in colour and chemical 

composition from those produced earlier in the reproductive 

stage (Cook et al. 1971). Some studies on 

the causes of heterophylly provide possible mechanisms 

for the ontogeny of seed heteromorphism, but 

the analogy may work only for some species. Indeed, a 

major feature of seed heteromorphism is its independence 

from environmental conditions (Lloyd 1984). It 

thus appears necessary to develop a specific model for 

the ontogeny of heterospermy and heterocarpy. 

The spike represents the primary organisation of 

most inflorescences in angiosperms. Spikes are characterised 

by apical growth and developing axillary buds. 

This development leads to a sequential maturation of 

flowers, and flowers near the bottom of the axis mature 

first, i.e. the order of flowering and seed maturation is 

acropetal. Seeds in the bottom of the axis receive resources 

earlier than those at the tip of the axis. Proximity 

to vascular tissues can also affect fruit and seed size 

(Diggle 1995; Susko & Lovett-Doust 2000). Considering 

the different levels of hierarchy (position of the infrutescence 

within the individual, position of the fruit 

within the infrutescence, position of the seed within the 

fruit), this development leads to an intra-individual 

variation in seed size. Such variation has been observed 

for various species (Cavers & Harper 1966; Harper et 

al. 1970; Schaal 1980; Hendrix 1984; Wulff 1986a; 

Roach 1987; Mehlman 1993; Senseman & Oliver 1993; 

Crochemore et al. 1994; Lokker & Cavers 1995; Simons 

& Johnston 2000; Susko & Lovett-Doust 2000). Such 

processes are often used to explain positional effects on 

seed maturation, abortion (Diggle 1995; Gutiérrez et al. 

1996; Susko & Lovett-Doust 1998) and germination requirements 

(Baskin & Baskin 1998), and may influence 

developmental stability (Simons & Johnston 1997). Accordingly, 

most examples of seed size variation are related 

to developmental constraints due to the hierarchy 

of development. In other words, intra-individual variation 

might be the result of architectural or physiological 

constraints (McGinley et al. 1987; Diggle 1995). While 

a continuous variation is not sufficient to define heteromorphism 

(see Introduction), this model can explain 

seed heteromorphism in species that present a variation 

in seed morphology between two extremes, like in 

Atriplex species (Chenopodiaceae) and Abronia sp. 

(Nyctaginaceae). However, developmental contraints 

has also to take the apical dominance into account. Indeed, 

in Cakile sp. (Brassicaceae) and Xanthium stru- 


24 E. Imbert 

Fig. 4. The relationship between presence/absence of heterocarpy and biogeographical origin (mediterranean and deserts vs. others) in Crepis according to 

the phylogenetic relationship among the 27 sections (from Babcock 1947). “H” symbolizes the presence of at least one heterocarpic species in the section. Box 

with bold lines, all species occur in either mediterranean or desert areas; box with full lines: all species occur in other areas; box with broken lines: the section 

contains species from mediterranean or desert areas (M) and from other areas (O). Numbers represent section numbers (cf. Fig. 1). 

marium (Asteraceae) fruits are dispermic and seeds in 

the upper position are the heaviest (Shull 1911; Thornton 

1935; Maun & Payne 1989; Zhang 1993). 

The capitulum of Asteraceae is supposed to directly 

derive from a spike, resulting from condensation of the 

axis (Harris 1995), and flower development is thus 

centripetally. Following the ontogenic arguments presented 

above, we expect peripheral achenes to be heavier 

than central ones. Several authors have reported 


that in Tragopogon dubius, where seed size decreases 

linearly from the periphery towards the centre (McGinley 

1989; Maxwell et al. 1994; see also Zohary 1950), 

and consistently in most heterocarpic Asteraceae, morphological 

differentiation between achene morphs is 

related to position within the capitulum, peripheral 

achenes being heavier than central ones. However, in 

Carduus pycnocephalus, C. tenuiflorus, Centaurea solstitialis 

(Olivieri & Berger 1985), Picris radicata (Ell-

ner & Shmida 1984) and Bidens pilosa (Rocha 1996) 

central achenes are heaviest. Gardocki et al. (2000) 

found no relation between flower position and seed 

morph in Calendula sp., and all seed types can be produced 

by peripheral flowers. 

Because the capitulum is a very condensed structure, 

constraints for space are not the same in the periphery as 

in the centre. For instance, the package of central achenes 

implies that they are straight, while peripheral achenes 

can be curved-shaped, as observed in Crepis sancta. Furthermore, 

in some species (e.g. Crepis leontodontoides, 

Hedypnois cretica, Picris echioides, Picris galilea), peripheral 

achenes are enclosed in involucral bracts. Several 

authors (Zohary 1950; McEvoy 1984; Venable 

1985a) have argued that the condensed inflorescence of 

Asteraceae favours heterocarpy. 

The position of seeds within the individual can also 

influence the chemical composition, in particular of the 

seed coat (Gutterman 1983; Gonzalez-Rabanal et al. 

1994; Gutterman 1994; Maxwell et al. 1994). Jaimand 

& Rezaee (1995) reported that the chemical composition 

of achenes of sunflowers varies according to their 

position within the capitulum. This observation is consistent 

with the variations in the concentration in germination 

inhibitor of some heterocarpic Asteraceae. 

Developmental constraints can easily explain bimodality 

of seed size, and the curved shape of peripheral 

achenes in the Asteraceae, but are not sufficient to explain 

the tremendous morphological differentiation observed 

in certain species. Whatever the ontogenetic process initialising 

the differentiation among seed morphs, there 

must exist, as for phenotypic plasticity, a genetically controlled 

mechanisms that either inhibits or enforces 

morphological differentiation (Bachmann 1983). For instance 

in Malva moschata (Malvaceae), leaf morphology 

varies with leaf position within stems, and esterase activities 

show striking differences between leaf types 

(Bachmann 1983). The tremendous morphological differentiation 

among seed morphs necessarily implies the 

production of at least one chemical component. 

Bachmann (1983) proposed a model largely based 

upon observations on the ontogeny of the capitulum: 

Assuming that there (1) is only one hormone involved 

in the differentiation between peripheral and central 

achenes, (2) C i is the concentration of this hormone at 

time i, and (3) the hormone is only produced when the 

meristem is in a vegetative stage or quiescent. When environmental 

conditions (i.e. temperature or photoperiod) 

are suitable for plants to reproduce, the vegetative 

meristem transforms into flower buds. The concentration 

of the hormone has thus an initial and maximal 

value (C 1). Peripheral parts of the meristem stop mitotic 

activity and start to differentiate into florets. Therefore, 

in these peripheral cells C i has the value C 1, or less 

if the hormone is not time-stable. Conversely, central 


parts of the bud still show mitotic activity, and C i is divided 

by two for each cell division. Such a model leads 

to a gradient in hormone concentration from the periphery 

towards the centre of the capitulum. Bachmann 

(1983) suggested that this model can also be applied to 

floret differentiation (ligulate in periphery and tubulate 

in centre) and sexual differentiation. 

This model is based upon a morphogen gradient 

and it may also apply for other types of inflorescence, 

where the flower buds in the lower part having higher 

hormonal concentrations. For instance, in the Araceae, 

sexual morphs vary along the inflorescence: in the 

lower part, flowers are female, median flowers are 

hermaphroditic and male in the upper part. Such variation 

may be due to a similar morphogen gradient 

(Boubes & Barabé 1996; Barabé & Jean 1996). Furthermore, 

it is important to note that the model leads 

to a cell-specific development, i.e. the gradient of the 

morphogen is independent of primordium boundaries 

(Bachmann 1983). For instance in Carduus species, 

the outer side of achenes of intermediate morphology 

have a peripheral-like morphology while the inner side 

is morphologically close to central achenes (Olivieri et 

al. 1983; see also Fig. 4 in Bachmann 1983). Finally, 

we have to note that in many examples of heterospermy 

and heterocarpy, the morphological differentiation 

relies upon the importance of development of a 

particular structure (beak in Hypochoeris glabra, wing 

in Spergularia marina, pappus in several Asteraceae 

species etc.), which can be the result of heterochrony. 

Heterochrony has been invoked to explain other differentiation 

such as evolution of corolla shape in the 

Delphinium genus (Guerrant 1982) or differentiation 

between gamopetaly and sympetaly (Stebbins 1974). 

Therefore, the hormonal factor could be a growth factor 

(Bachmann et al. 1984). Note that the model could 

also work with an inhibitor agent. 

This model explaining the ontogeny of differentiation 

between seed types leads to the conclusion that 

morphological differentiation is independent of any paternal 

contribution. Indeed, the differentiation among 

morphs only results from maternal effects, and there is 

no genetic difference among seed morphs that control 

for morphological differentiation. For instance, in Calendula 

arvensis (Asteraceae), differentiation between 

peripheral and central ovules started before anthesis 

(Pomplitz 1956). The same observations have been 

made in Carduus sp. (I. Olivieri, pers. comm.). Consequently, 

differences among morphs are non-genetic maternal 

effects (Imbert et al. 1999). Furthermore, seed 

heteromorphism is considered as intra-individual 

variation, i.e. a variation within a single plant, and a 

relevant way to interpret the character is to consider 

the respective proportions of each seed type produced 

by a single individual (e.g. Imbert 2001). 


26 E. Imbert 

Conclusion 

Considering species with heteromorphic seed, several 

characters are involved in the differentiation. This is 

particularly true for heterocarpy in the Asteraceae, 

where achenes differ in mass, the size of the pappus 

and the structure of the pericarp. Species with seed heteromorphism 

are therefore biological models which are 

suitable to test some theoretical predictions about the 

evolution of dispersal rates or germination strategies. 

In most amphicarpic species, subterranean fruits are 

produced first, while aerial fruits are only produced 

when conditions are good enough (Zeide 1978; Cheplick 

& Quinn 1982). Therefore, considering aerial seeds 

have a better dispersal ability than subterranean ones 

(which often not disperse at all), dispersal rate is higher 

in good than in poor habitats. However, the interpretation 

of results obtained in amphicarpic species, and 

more generally in species producing both chasmogamous 

and cleistogamous flowers (see Clay 1982), is 

complex because the proportions of flower types are 

also influenced by allocation to different reproductive 

strategies (obligate self-pollination vs. open pollination). 

In the Asteraceae Crepis sancta, the observed pattern 

was the reverse: in bad conditions plants increase 

allocation to dispersed achenes (the central ones). Conversely, 

in Hypochoeris glabra (Baker & O’Dowd 

1982) and Catananche lutea (Ruiz de Clavijo & Jiminez 

1998) the proportion of central achenes decreases when 

plant density increases (see also Imbert & Ronce 2001). 

Environmental conditions also affect the proportions of 

seed morphs in Atriplex triangularis (Ungar 1987) and 

Atriplex sagittata (Mandák & Pysˇek 1999a). Concerning 

genetic variation of seed morph proportions, some 

experiments have been made with species producing 

cleistogamous flowers (Clay 1982; Cheplick & Quinn 

1988), and significant heritabilities have been obtained 

in Crepis sancta (Imbert 2001) and Heterosperma pinnatum 

(Venable & Burquez 1989), but data are scarce. 

Along the same topic, the observed genetic variation 

under controlled conditions or the phenotypic variation 

observed in natural populations suggest that some individuals 

do not present the character, i.e. some individuals 

are not heteromorphic. Those individuals should 

represent the basis for future research on the genetics of 

the presence/absence of the character. 

Although few observations have been collected on 

proximal mechanisms leading to heterospermy and 

heterocarpy, the importance of developmental constraints 

is often suggested (Dowling 1933; Zohary 

1950; McEvoy 1984; Venable 1985a). Few experiments 

have examined the genetic regulation required to 

produce heteromorphic fruits and seeds. In the genus 

Microseris, interspecific cross-breeding showed that 

the hairy character was under the control of two 

epistatic loci (Bachmann & Chambers 1981; Bach- 


mann et al. 1984), and the expression of each locus 

seems to be under the control of a third locus (Mauthe 

et al. 1984). With the same materials, Mauthe et al. 

(1984) have also shown that at least two loci control 

for the colour of the pericarp. In the genus Spergularia, 

crossing between monomorphic and heteromorphic individuals 

suggested a genetic system with two loci involved 

(Sterk & Dijkhuizen 1972). Developmental genetics 

should help to study the ontogenetic processes. 

For instance, investigation of capitulum development 

of cultivated ornamental Gerbera showed that the induction 

of genes contributing to organ differentiation 

within the floret proceeds centripetally in the capitulum 

(Yu et al. 1999; Kotilainen et al. 2000). Furthermore, 

gene expression is known to vary according to 

cell position. For instance, the cycloidea gene is known 

to control floral asymmetry in Antirrhinum (Luo et al. 

1996), and recent experiments have shown that the differentiation 

between ligulate florets (in the periphery of 

the capitulum) and tubulate florets (in the centre of the 

capitulum) is correlated to differences in expression of 

this gene in Senecio vulgaris (E. Coen, pers. comm.). 

Acknowledgement. I am very grateful to Isabelle Olivieri, 

Ophélie Ronce, Anders Telenius and Carl Freeman for critical 

reading of the manuscript, and to Joel Mathez for his help with 

the taxonomy of the cited species. Johannes Kollmann, Gregory 

Cheplick and an anonymous reviewer improved the clarity of 

the presentation. The final version of this manuscript was 

written while I was supported by a postdoctoral fellowship 

from European Community “Plant Dispersal” allocated to 

B. Vosman. This is contribution ISEM 2002–011 of the “Institut 

des Sciences de l’Evolution” in Montpellier. 

References 

Andersson IA, Carlström A, Franzén R, Karlén Th & 

Nybom H (1983) A revision of the Aethionema saxatile 

complex (Brassicaceae). Willdenowia 13: 3–42. 

Augspurger CK & Franson SE (1993) Consequences for seed 

distribution of intra-crop variation in wing-loading of 

wind-dispersed species. Vegetatio 107/108: 121–131. 

Austenfeld F-A (1988) Seed dimorphism in Salicornia europaea, 

nutrient reserves. Physiologia Plantarum 73: 502–504. 

Babcock EB (1947) The Genus Crepis. California Press, 

Berkeley. 

Bachmann K (1983) Evolutionary genetics and the genetic 

control of morphogenesis in flowering plants. Evolutionary 

Biology 16: 157–208. 

Bachmann K & Chambers KL (1981) Genes regulating the 

appearance of two kinds of fruits in Microseris strain B87 

(Asteraceae, Compositae). Experientia 37: 29–31. 

Bachmann K & Chambers KL (1990) Heritable variation for 

heterocarpy in Microseris bigelovii (Asteraceae-Lactuceae). 

Beiträge zur Biologie der Pflanzen 65: 123–146.

Bachmann K & Price HJ (1979) Variability of the inflorescence 

of Microseris laciniata (Compositae, Cichoriaceae). 

Plant Systematics and Evolution 131: 17–34. 

Bachmann K, Chambers KL & Price HJ (1984) Genetic components 

of heterocarpy in Microseris hybrid B87 (Asteraceae, 

Lactuceae). Plant Systematics and Evolution 148: 149–164. 

Baker GA & O’Dowd DJ (1982) Effects of parent plant density 

on the production of achene type in the annual 

Hypochoeris glabra. Journal of Ecology 70: 201–215. 

Barabé D & Jean RV (1996) The constraints of global form 

on phyllotactic organization, the case of Symplocarpus 

(Araceae). Journal of Theoretical Biology 178: 393–397. 

Barbour MG (1970) Germination and early growth of the 

strand plant Cakile maritima. Bulletin of the Torrey 

Botanical Club 97: 13–22. 

Baskin JM & Baskin CC (1976) Germination dimorphism in 

Heterotheca subaxillaris var. subaxillaris. Bulletin of the 

Torrey Botanical Club 103: 201–206. 

Baskin CC & Baskin JM (1998) Seeds, Ecology, Biogeography, 

and Evolution of Dormancy and Germination. Academic 

Press, San Diego. 

Battandier MA (1883) Sur quelques cas d’hétéromophisme. 

Bulletin de la Société Botanique de France 238–244. 

Beadle NCW (1952) Studies on halophytes I. The germination 

of seeds and establishment of seedlings of 5 species of 

Atriplex in Australia. Ecology 53: 49–52. 

Becker W (1913) Uber die Keimung verschiedenartiger 

Früchte und Samen bei derselben Species. Beihefte 

Botanisches Centralblatt 29: 216–243. 

Bendall GM (1973) Some aspects of the biology, ecology and 

control of slender thistles, Carduus tenuiflorus Curt. and 

C. pycnocephalus L. (Compositae) in Tasmania. M. 

Agric. thesis, University of Tasmania. 

Beneke K, von Teichman I, van Rooyen MW & Theron GK 

(1992a) Fruit polymorphism in ephemeral species of 

Naquamaland. I. Anatomical differences between polymorphic 

diaspores of two Dimorphotheca species. South 

African Journal of Botany 58: 448–455. 

Beneke K, von Teichman I, van Rooyen MW & Theron GK 

(1992b) Fruit polymorphism in ephemeral species of 

Naquamaland. II. Anatomical differences between polymorphic 

diaspores of Arctotis fastuosa and Ursinia cakilefolia. 

South African Journal of Botany 58: 456–460. 

Beneke K, van Rooyen MW, Theron GK & van de Venter HA 

(1993a) Fruit polymorphism in ephemeral species of Naquamaland. 

III. Germination differences between the polymorphic 

diaspores. Journal of Arid Environments 24: 333–344. 

Beneke K, van Rooyen MW, Theron GK & van de Venter 

HA (1993b) Fruit polymorphism in ephemeral species of 

Naquamaland. IV. Growth analyses of plant cultivated 

from the dimorphic diaspores. Journal of Arid Environments 

24: 345–360. 

Berger A (1985) Seed dimorphism and germination behaviour 

in Salicornia patula. Vegetatio 61: 137–143. 

Bischof F (1978) Common Weeds from Iran, Turkey, the 

Near East and North Africa. GTZ, Eschborn. 

Bongard-Pierce DK, Evans MMS & Poethig RS (1996) Heteroblastic 

features of leaf anatomy in maize and their genetic 

regulation. International Journal of Plant Sciences 

157: 331–340. 


Boubes C & Barabé D (1996) Développement de l’inflorescence 

et des fleurs du Philodendron acutatum Schott 

(Araceae). Canadian Journal of Botany 74: 909–918. 

Briggs D & Walters SM (1997) Plant Variation and Evolution. 

Cambridge University Press, Cambridge. 

Brown NAC & Mitchell JJ (1984) Germination of the polymorphic 

fruits of Bidens bipinnata. South Africa Journal 

of Botany 3: 55–58. 

Budd GD, Thomas EL & Allison JCS (1979) Vegetative regeneration 

depth of germination and seed dormancy in 

Commelina benghalensis L. Rhodesian Journal of Agricultural 

Research 17: 151–153. 

Burke A (1995) Geigeria alata in the Namib desert, seed heteromorphism 

in an extremely arid environment. Journal 

of Vegetation Science 6: 473–478. 

Burtt BL (1977) Aspects of diversification in the capitulum. 

The Biology and Chemistry of the Compositae (eds. VH 

Heywood, JB Harborne & BL Turner), pp. 41–59. Academic 

Press, London. 

Callahan H & Waller DM (2000) Phenotypic integration 

and the plasticity of integration in an amphicarpic annual. 

International Journal of Plant Sciences 161: 89–98. 

Campbell CS, Quinn JA, Cheplick GP & Bell TJ (1983) 

Cleistogamy in grasses. Annual Review of Ecology and 

Systematics 14: 411–441. 

Cavers PB & Harper JL (1966) Germination polymorphism 

in Rumex crispus and Rumex obtusifolius. Journal of 

Ecology 54: 367–382. 

Cheplick GP (1983) Differences between plants arising from 

aerial and subterranean seeds in the amphicarpic annual 

Cardamine chenopodifolia (Cruciferae). Bulletin of the 

Torrey Botanical Club 110: 442–448. 

Cheplick GP (1996a) Do seed germination patterns in cleistogamous 

annual reduce the risk of sibling competition? 

Journal of Ecology 84: 247–255. 

Cheplick GP (1996b) Cleistogamy and seed heteromorphism 

in Triplasis purpurea (Poaceae). Bulletin of the Torrey 

Botanical Club 123: 25–33. 

Cheplick GP & Clay K (1989) Convergent evolution of cleistogamy 

and seed heteromorphism in two perennial grasses. 

Evolutionary Trends in Plants 3: 127–136. 

Cheplick GP & Grandstaff K (1997) Effects of sand burial 

on purple sandgrass (Triplasis purpurea), the significance 

of seed heteromorphism. Plant Ecology 133: 79–89. 

Cheplick GP & Quinn JA (1982) Amphicarpum purshii and 

the “pessimistic strategy” in amphicarpic annuals with 

subterranean fruit. Oecologia 52: 327–332. 

Cheplick GP & Quinn JA (1988) Quantitative variation of 

life history traits in amphicarpic peanutgrass (Amphicarpum 

purshii) and its evolutionary significance. American 

Journal of Botany 75: 123–131. 

Cheplick GP & Sung LY (1998) Effects of maternal nutrient 

environment and maturation position on seed heteromorphism, 

germination, and seedling growth in 

Triplasis purpurea (Poaceae). International Journal of 

Plant Sciences 159: 338–350. 

Cheplick GP & Wickstrom VM (1999) Assessing the potential 

for competition on a coastal beach and the significance 

of variable seed mass in Triplasis purpurea. Journal 

of the Torrey Botanical Club Society 126: 296–306. 


28 E. Imbert 

Clay K (1982) Environmental and genetic determinants of 

cleistogamy in a natural population of the grass Danthonia 

spicata. Evolution 36: 734–741. 

Clay K (1983) The differential establishment of seedlings 

from chasmogamous and cleistogamous flowers in natural 

populations of the grass Danthonia spicata. Oecologia 

57: 183–188. 

Cohen D (1966) Optimizing reproduction in a randomly 

varying environment. Journal of Theoretical Biology 

12: 119–129. 

Cook AD, Atsatt PR & Simon CA (1971) Doves and dove 

weed, multiple defenses against avian predation. Bio- 

Science 21: 277–281. 

Corkidi L, Rincon E & Vazquez-Yanes C (1991) Effets of 

light and temperature on germination of heteromorphic 

achenes of Bidens odorata (Asteraceae). Canadian Journal 


Correns C (1906) Das Keimen der beiderlei Früchte der Dimorphoteca 

pluvialis. Berichte der Deutschen Botanischen 

Gesellschaft 24: 173–176. 

Crochemore ML, Huyghe C, Papineau J & Julier B (1994) 

Intra-plant variability in seed size and seed quality in 

Lupinus albus L. Agronomie 14: 5–13. 

Dakshini KMM & Aggarwal SK (1974) Intracapitular 

cypsele dimorphism and dormancy in Bidens bipinnata. 

Biologia Plantarum (Praha) 16: 469–471. 

Davy AJ, Bishop GF & Costa CSB (2001) Salicornia L. (Salicornia 

pusilla J. Woods, S. ramosissima J. Woods, S. europaea 

L., S. obscura P.W. Ball & Tutin, S. nitens P.W. Ball 

& Tutin, S. fragilis P.W. Ball & Tutun and S. 

dolichostachya Moss). Journal of Ecology 89: 681–707. 

Diggle PK (1995) Architectural effects and the interpretation 

of patterns of fruit and seed development. Annual Review 

of Ecology and Systematics 26: 531–552. 

Dowling RE (1933) The reproduction of Plantago coronopus, 

an example of morphological and biological seed dimorphism. 

Annals of Botany 47: 861–872. 

Dyksterhuis EJ (1945) Axillary cleistogenes in Stipa leucotricha 

and their role in nature. Ecology 26: 195–199. 

Ellison AM (1987) Effect of seed dimorphism on the densitydependent 

dynamics of experimental populations of 

Atriplex triangularis (Chenopodiaceae). American Journal 


Ellner S (1986) Germination dimorphism and parent-offspring 

conflict in seed germination. Journal of Theoretical 

Biology 123: 173–185. 

Ellner S & Shmida A (1981) Why are adaptations for long-range 

seed dispersal rare in desert plants ? Oecologia 51: 133–144. 

Ellner S & Shmida A (1984) Seed dispersal in relation to 

habitat in the genus Picris (Compositae) in mediterranean 

and arid regions. Israel Journal of Botany 33: 25–39. 

Ernst A (1906) Das Keimen der dimorphen Früchte von 

Synedrella nodiflora (L.) Grtn. Berichte der Deutschen 

Botanischen Gesellschaft 24: 450–458. 

Evenari M (1963) Zur Keimungsökologie zweier 

Wüstenpflanzen. Mitteilungen der Floristisch-Soziologischen 

Arbeitsgemeinschaft 10: 70–81. 

Feinbrun-Dothan N & Zohary M (1978) Flora Palaestina, 

Part 3 – Ericaceae to Compositae. The Israel Academy of 

Sciences and Humanities, Jerusalem. 


Fenner M (1985) Seed Ecology. Chapman and Hall, London. 

Fenner M, Cresswell JE, Hurley RA & Baldwin T (2002) Relationship 

between capitulum size and pre-dispersal seed 

predation by insect larvae in common Asteraceae. Oecologia 

130: 72–77. 

Flint SD & Palmblad IG (1978) Germination dimorphism 

and developmental flexibility in the ruderal weed Heterotheca 

grandiflora. Oecologia 36: 33–43. 

Forsyth C & Brown NAC (1982) Germination of the dimorphic 

fruits of Bidens pilosa L. New Phytologist 90: 

151–164. 

Frankton C & Bassett IJ (1968) The genus Atriplex 

(Chenopodiaceae) in Canada. I. Three introduced species, 

A. heterosperma, oblinfolia and hortensis. Canadian Journal 


Gardocki ME, Zablocki H, El-Keblawy A & Freeman DC 

(2000) Heterocarpy in Calendula micrantha (Asteraceae), 

the effects of competition and availability of water on the 

performance of offspring from different fruit morphs. 

Evolutionary Ecology Research 2: 701–718. 

Geritz SAH (1995) Evolutionarily stable seed polymorphism 

and small-scale variation in seedling density. The American 

Naturalist 146: 685–707. 

Geritz SAH (1998) Coevolution of seed size and seed predation. 

Evolutionary Ecology 12: 891–911. 

Gibson JP (2001) Ecological and genetic comparison between 

ray and disc achene pools of the heteromorphic 

species Prionopsis ciliata (Asteraceae). International Journal 

of Plant Sciences 162: 137–145. 

Gillespie JH (1977) Natural selection for variances in offspring 

numbers, a new evolutionary principle. The American 

Naturalist 111: 1010–1014. 

Gleeson SK & Tilman D (1994) Plant allocation, growth 

rate and successional status. Functional Ecology 8: 

543–550. 

Gonzalez-Rabanal F, Casal M & Trabaud L (1994) Effects 

of high temperatures, ash and seed position in the inflorescence 

on the germination of three Spanish grasses. 

Journal of Vegetation Science 5: 289–294. 

Greene DF & Johnson EA (1989) A model of wind dispersal 

of winged or plumed seeds. Ecology 70: 339–347. 

Grouzis M, Berger A & Heim G (1976) Polymorphisme et 

germination des graines chez trois espèces annuelles du 

genre Salicornia. Oecologica Plantarum 11: 41–52. 

Guerrant EOJ (1982) Neotenic evolution of Delphinium 

nudicaule (Ranunculaceae), a humming-bird pollinated 

larkspur. Evolution 36: 699–712. 

Gutierrez D, Menendez R & Obeso JR (1996) Effect of 

ovule position on seed maturation and seed weight in 

Ulex europeaus and Ulex gallii (Fabaceae). Canadian 


Gutterman Y (1983) Mass germination of plants under 

desert conditions. Effects of environmental factors during 

seed maturation, dispersal, germination and establishment 

of desert annual and perennial plants in the Negev 

highlands, Israel. Developments in Ecology and Environmental 

Quality (ed. HI Shuval), pp. 1–10. Balaban ISS, 

Rehovot, Philadelphia. 

Gutterman Y (1993) Seed Germination in Desert Plants. 

Springer-Verlag, Heidelberg.

Gutterman Y (1994) Long-term seed position influences on 

seed germinability of the desert annual, Mesembryathenum 

nodiflorum L. Israel Journal of Plant Sciences 42: 

197–205. 

Hannan GL (1980) Heteromericarpy and dual seed germination 

modes in Platystemon californicus (Papaveraceae). 

Madroño 27: 164–170. 

Harper JL (1965) Establishment, aggression, and cohabitation 

in weedy species. The Genetics of Colonizing Species 

(eds. HG Baker & GL Stebbins), pp. 243–268. Academic 

Press, New York. 

Harper JL (1977) Population Biology of Plants. Academic 

Press, London. 

Harper JL, Lovell PH & Moore KG (1970) The shapes and 

sizes of seeds. Annual Review of Ecology and Systematics 

1: 327–356. 

Harris EM (1995) Inflorescence and floral ontogeny in 

Asteraceae, a synthesis of historical and current concepts. 

The Botanical Review 61: 93–278. 

Hendrix SD (1984) Variation in seed weight and its effects 

on germination in Pastinaca sativa L. (Umbelliferae). 

American Journal of Botany 71: 795–802. 

Heyn CC, Dagan O & Nachman B (1974) The annual Calendula 

species, taxonomy and relationships. Israel Journal 


Hickey M & King C (2000) The Cambridge Illustrated 

Glossary of Botanical Terms. Cambridge University Press, 

Cambridge. 

Imbert E (1999) The effects of achene dimorphism on the 

dispersal in time and space in Crepis sancta (Asteraceae). 

Canadian Journal of Botany 77: 508–513. 

Imbert E (2001) Capitulum characters in the seed heteromorphic 

species Crepis sancta (Asteraceae), variance partioning 

and inference for the evolution of dispersal rate. 

Heredity 86: 78–86. 

Imbert E & Ronce O (2001) Phenotypic plasticity for dispersal 

ability in the seed heteromorphic Crepis sancta (Asteraceae). 

Oikos 93: 126–134. 

Imbert E, Escarré J & Lepart J (1996) Achene dimorphism 

and among-population variations in some biological traits 

in Crepis sancta (Asteraceae). International Journal of 

Plant Sciences 157: 309–315. 

Imbert E, Escarré J & Lepart J (1997) Seed heteromorphism 

in Crepis sancta (Asteraceae), performance of two morphs 

in different environments. Oikos 79: 325–332. 

Imbert E, Escarré J & Lepart J (1999) Local adaptation and 

non-genetic maternal effects among three populations of 

Crepis sancta (Asteraceae). Écoscience 6: 223–229. 

Jaimand K & Rezaee MB (1995) Variability in seed composition 

due to plant population and capitula zones of sunflower. 

Agrochimica 39: 177–183. 

Johnson ML & Gaines MS (1990) Evolution of dispersal, 

theoretical models and empirical tests using birds and 

mammals. Annual Review of Ecology and Systematics 21: 

449–480. 

Joley DB, Maddox DM, Mackey BE, Schoenig SE & 

Casanave KA (1997) Effect of light and temperature on 

germination of dimorphic achenes of Centaurea solstitialis 

in California. Canadian Journal of Botany 75: 

2131–2139. 


Kaplan RH & Cooper WS (1984) The evolution of developmental 

plasticity in reproduction characteristics, an application 

of the “adaptive coin-flipping” principle. The 

American Naturalist 123: 393–410. 

Khan MA & Gul B (1998) High salt tolerance in germinating 

dimorphic seeds of Arthrocnemum indicum. International 

Journal of Plant Sciences 159: 826–832. 

Khan MA, Ungar IA & Gul B (1998) Action of compatible 

osmotica and growth regulators in alleviating the effect of 

salinity on the germination of dimorphic seeds of Arthrocnemun 

indicum L. International Journal of Plant Sciences 

159: 313–317. 

Kigel J (1992) Diaspore heteromorphism and germination in 

populations of the ephemeral Hedypnois rhagadioloides 

(L.) FW Schmidt (Asteraceae) inhabiting a geographic 

range of increasing aridity. Acta Oecologica 13: 45–53. 

Koller D (1957) Germination-regulating mechanisms in 

some desert seeds. IV. Atriplex dimorphostegia Kar. et Kir. 

Ecology 38: 1–13. 

Koller D & Roth N (1964) Studies of the ecological and physiological 

significance of amphicarpy in Gymnarrhena micrantha 

(Compositae). American Journal of Botany 51: 26–35. 

Kotilainen M, Elomaa P, Uimari A, Albert VA, Yu D & Teeri 

TH (2000) GRC1, an AGL2-like MADS box gene, participates 

in the C function during stamen development in 

Gerbera hydrida. The Plant Cell 12: 1893–1902. 

Lloyd DG (1984) Variation strategies of plants in heterogeneous 

environments. Biological Journal of the Linnean 

Society 21: 357–385. 

Lokker C & Cavers PB (1995) The effects of physical damage 

on seed production in flowering plants of Saponaria 

officinalis. Canadian Journal of Botany 73: 235–243. 

Luo D, Carpenter R, Vincent C, Copsey L & Coen E (1996) Origin 

of floral asymmetry in Antirrhinum. Nature 383: 794–799. 

Mabberley DJ (1997) The Plant Book. Cambridge University 

Press, Cambridge. 

Maire R (1965) Dicotyledonae, Rhoedales, Papaveracea, 

sf. Fumarioidae p.p.; Capparidaceae, Cruciferae p.p. 

Flore de l’Afrique du Nord (ed. P Quézel), vol. 12. Paul 

Lechevalier, Paris. 

Mandák B (1997) Seed heteromorphism and the life cycle of 

plants, a literature review. Preslia, Praha 69: 129–159. 

Mandák B & Pysˇek P (1999a) Effects of plant density and 

nutrient levels on fruit polymorphism in Atriplex 

sagittata. Oecologia 119: 63–72. 

Mandák B & PysˇekP (1999b) How does density and nutrient 

stress affect allometry and fruit production in the heterocarpic 

species Atriplex sagittata (Chenopodiaceae). 


Mandák B & Pysˇek P (2001a) The effects of light quality, nitrate 

concentration and presence of bracteoles on germination 

of different fruit types in the heterocarpous 

Atriplex sagittata. Journal of Ecology 89: 149–158. 

Mandák B & Pysˇek P (2001b) Fruit dispersal and seed banks 

in Atriplex sagittata, the role of heterocarpy. Journal of 

Ecology 89: 159–165. 

Marañon T & Grubb PJ (1993) Physiological basis and ecological 

significance of the seed size and relative growth 

rate relationship in Mediterranean annuals. Functional 

Ecology 7: 591–599. 


30 E. Imbert 

Martin A (1996) Germination et dispersion des graines chez 

Glaucium flavum Crantz (Papaveraceae). Acta Botanica 

Malacitana 21: 71–78. 

Mathez J & Xena de Enrech N (1985) Heterocarpy, fruit 

polymorphism and discriminating dissemination in the 

genus Fedia (Valerianaceae). Genetic Differentiation and 

Dispersal in Plants (eds. P Jacquard, G Heim & J 

Antonovics), pp. 431–441. NATO, Berlin. 

Mattatia J (1977a) The amphicarpic species Lathyrus ciliolatus. 

Botanical Notiser 129: 437–444. 

Mattatia J (1977b) Amphicarpy and variability in Pisum fulvum. 

Botanical Notiser 130: 27–34. 

Maun MA & Payne AM (1989) Fruit and seed polymorphism 

and its relation to seedling growth in the genus 

Cakile. Canadian Journal of Botany 67: 2743–2750. 

Maurya AN & Ambasht RS (1973) Significance of seed dimorphism 

in Alyscarpus monolifer DC. Journal of Ecology 

61: 213–217. 

Mauthe S, Bachmann K, Chambers KL & Price HJ (1984) 

Independent responses of two fruit characters to developmental 

regulation in Microseris douglasii (Asteraceae, 

Lactuceae). Experientia 40: 1280–1281. 

Maxwell CD, Zobel A & Woodfine D (1994) Somatic polymorphism 

in the achenes of Tragopogon dubius. Canadian 


McDonough WT (1975) Germination polymorphism in 

Grindelia squarrosa. Northwest Science 49: 190–200. 

McEvoy PB (1984) Dormancy and dispersal in dimorphic achenes 

of tansy ragwort Senecio jacobaea. Oecologia 61: 160–168. 

McEvoy PB & Cox CS (1987) Wind dispersal distance in dimorphic 

achenes of ragwort, Senecio jacobaea. Ecology 

68: 2006–2015. 

McGinley MA (1989) Within and among plant variation in 

seed mass and pappus size in Tragopogon dubius. Canadian 


McGinley MA, Temme DH & Geber MA (1987) Parental 

investment in offspring in variable enviroments, theoretical 

and empirical considerations. The American Naturalist 

130: 370–398. 

McNamara J & Quinn JA (1977) Resource allocation and 

reproduction in populations of Amphicarpum purshii 

(Gramineae). American Journal of Botany 64: 17–23. 

Mehlman DW (1993) Seed size and seed packaging variation 

in Baptisia lanceolata (Fabaceae). American Journal of 

Botany 80: 735–742. 

Mohamed-Yasseen Y, Barringer SA, Splittstoesser WA & 

Costanza S (1994) The role of seed coats in seed viability. 

The Botanical Review 60: 426–439. 

Montégut J (1970) Clé de détermination des semences et des 

mauvaises herbes. Versaille, Ecole Nationale Supérieure 

d’Horticulture de Versailles. 

Negbi M & Tamari B (1963) Germination of chlorophyllous 

and achlorophyllous seeds of Salsola volkensii and 

Aellinia autrani. Israel Journal of Botany 12: 124–135. 

Niklas KJ (1997) The Evolutionary Biology of Plants. The 

Chicago University Press, Chicago. 

Olivieri I (2001) The evolution of dispersal and other traits 

in metapopulation. Integrating Ecology and Evolution in 

a Spatial Context (eds. J Antonovics & J Silvertown), pp. 

245–268. Blackwell Science, Oxford. 


Olivieri I & Berger A (1985) Seed dimorphism for dispersal, 

physiological, genetic and demographic aspects. Genetic 

Differentiation and Dispersal in Plants (eds. P Jacquard, 

G Heim & J Antonovics), pp. 413–429. NATO ASI series, 

Springer-Verlag, Berlin. 

Olivieri I & Gouyon PH (1985) Seed dimorphism for dispersal, 

theory and implications. Structure and Functioning of 

Plant Populations (eds J Hack & JW Woldentrop), pp. 

77–99. North Holland Publishing Company, Amsterdam. 

Olivieri I, Swan M & Gouyon PH (1983) Reproductive system 

and colonizing strategy of two species of Carduus 

(Compositae). Oecologia 60: 114–117. 

Payne AM & Maun MA (1981) Dispersal and floating ability 

of dimorphic fruit segments of Cakile edentula var. lacustris. 


Petit DP (1990) Contribution à l’étude de l’évolution des 

Carduées et Lactucées (Composées). PhD thesis, University 

of Montpellier. 

Philipupillai J & Ungar IA (1984) The effect of seed dimorphism 

on the germination and survival of Salicornia europaea L. 

populations. American Journal of Botany 71: 542–549. 

Plitmann U (1973) Biological flora of Israel. 4. Vicia sativa 

subsp. amphicarpa (Dorth) Aschers & Graebn. Israel 


Plitmann U (1986) Alternative modes in dispersal strategies 

with an emphasis on herbaceous plants of the Middle 

East. Proceedings of the Royal Society of Edinburg 89: 

193–202. 

Pomplitz R (1956) Die Heteromorphie der Früchte von Calendula 

arvensis unter besonderer Berücksichtigung der 

Stellungs- und Zahlenverhältnisse. Beiträge zur Biologie 

der Pflanzen 32: 331–369. 

Porras R & Muñoz JM (2000) Achene heteromorphism in 

the cleistogamous species Centaurea melitensis. Acta Oecologica 

21: 231–243. 

Priestley DA (1986) Seed Aging, Implications for Seed Storage 

and Persistence in the Soil. Cornell University Press, 

New York. 

Quézel P & Santa A (1962) La nouvelle flore de l’Algérie et 

des régions désertiques méridionales. Paris, CNRS. 

Rabinowitz D & Rapp JK (1979) Dual dispersal in hairgrass, 

Agrostis hiemalis (Walt.) B.S.P. (Graminea). Bulletin 

of the Torrey Botanical Club 106: 32–36. 

Rai JPN & Tripathi RS (1987) Germination and plant survival 

and growth of Galingosa parviflora Cav. as related 

to food and energy content of its ray- and disc-achenes. 

Acta Oecologica 8: 155–165. 

Redbo-Torstensson P & Telenius A (1995) Primary and secondary 

seed dispersal by wind and water in Spergularia 

salina. Ecography 18: 230–237. 

Roach DA (1987) Variation in seed and seedling size in Anthoxanthum 

odoratum. The American Midland Naturalist 

117: 258–264. 

Rocha OJ (1996) The effects of achene heteromorphism on 

the dispersal capacity of Bidens pilosa L. International 


Ronce O, Olivieri I, Clobert J & Danchin E (2001) Perspectives 

on the study of dispersal evolution. Dispersal (eds. J 

Clobert, E Danchin, AA Dhondt & JD Nichols), pp. 

341–357. Oxford University Press, Oxford.

Ruiz de Clavijo E (1994) Heterocarpy and seed polymorphism 

in Ceratocapnos heterocarpa (Fumariaceae). International 


Ruiz de Clavijo E (1995) The ecological significance of fruit 

heteromorphism in the amphicarpic species Catananche 

lutea (Asteraceae). International Journal of Plant Sciences 

156: 824–833. 

Ruiz de Clavijo E (2001) The role of dimorphic achenes in 

the biology of the annual weed Leontodon longirrostris. 

Weed Research 41: 275–286. 

Ruiz de Clavijo E & Jimenez MJ (1998) The influence of 

achene type and plant density on growth and biomass allocation 

in the heterocarpic annual Catananche lutea 

(Asteraceae). International Journal of Plant Sciences 159: 

637–647. 

Salisbury EJ (1958) Spergularia salina and Spergularia 

margina and their heteromorphic seeds. Kew Bulletin 1: 

41–51. 

Schaal BA (1980) Reproductive capacity and seed size in 

Lupinus texensis. American Journal of Botany 67: 

703–709. 

Schat H (1981) Seed polymorphism and germination ecology 

of Plantago coronopus L. Acta Oecologica 2: 367–380. 

Schnee BK & Waller DM (1986) Reproductive behavior of 

Amphicarpaea bracteata (Leguminosae), an amphicarpic 

annual. American Journal of Botany 73: 376–386. 

Senseman SA & Oliver LR (1993) Flowering patterns, seed 

production and somatic polymorphism of three weed 

species. Weed Science 41: 418–425. 

Sheldon JC & Burrows FM (1973) The dispersal effectiveness 

of the achene-pappus units of selected Compositae in 

steady winds with convection. New Phytologist 72: 

665–675. 

Shull CA (1911) The oxygen minimum and the germination 

of Xanthium seeds. Botanical Gazette 52: 453–476. 

Silvertown JW (1984) Phenotypic variety in seed germination 

behavior, the ontogeny and evolution of somatic polymorphism 

in seeds. The American Naturalist 124: 1–16. 

Simons AM & Johnston MO (1997) Developmental instability 

as a bet-hedging strategy. Oikos 80: 401–406. 

Simons AM & Johnston MO (2000) Variation in seed traits 

of Lobelia inflata (Campanulaceae), sources and fitness 

consequences. American Journal of Botany 87: 124–132. 

Slatkin M (1974) Hedging one’s evolutionary bets. Nature 

250: 704–705. 

Smith CC & Fretwell SD (1974) The optimal balance between 

size and number of offspring. The American Naturalist 

108: 499–506. 

Smith M & Keevin TM (1998) Achene morphology, production 

and germination, and potential for water dispersal in 

Boltonia decurrens (decurrent false aster), a threatened 

floodplain species. Rhodora 100: 69–81. 

Sorensen AE (1978) Somatic polymorphism and seed dispersal. 

Nature 276: 174–176. 

Stebbins GL (1974) Flowering Plants. Evolution above the 

Species Level. Arnold, London. 

Sterk AA (1969) Biosystematic studies on Spergularia media 

and Spergularia marina in Netherlands. III. The variability 

of S. media and S. marina in relation to the environment. 

Acta Botanica Neerlandica 18: 561–577. 


Sterk AA & Dijkhuizen L (1972) The relation between the 

genetic determination and the ecological significance of 

the seed wing in Spergularia media and S. marina. Acta 

Botanica Neerlandica 21: 481–490. 

Susko DJ & Lovett-Doust L (1998) Variable patterns of seed 

maturation and abortion in Alliaria petiolata (Brassicaceae) 


Susko DJ & Lovett-Doust L (2000) Patterns of seed mass variation 

and their effects on seedling traits in Alliaria petiolata 

(Brassicaceae). American Journal of Botany 87: 56–66. 

Takeno K & Yamaguchi H (1991) Diversity in seed germination 

behavior in relation to heterocarpy in Salsola komarovii 

Iljin. The Botanical Magazine 104: 207–215. 

Tanowitz BD, Salopek PF & Mahall BE (1987) Differential germination 

of ray and disc achenes in Hemizonia increscens 

(Asteraceae). American Journal of Botany 74: 303–312. 

Taylorson RB & Hendricks SB (1977) Dormancy in seeds. 

Annual Review of Plant Physiology 28: 331–354. 

Tébar FJ & Llorens I (1993) Heterocarpy in Thymelea velutina 

(Poiret ex Camb.) Endl., a case of phenotypic adaptation 

to Mediterranean selective pressures. Botanical 

Journal of the Linnean Society 111: 295–300. 

Telenius A (1992) Seed heteromorphism in a population of 

Spergularia media in relation to the ambient vegetation 

density. Acta Botanica Neerlandica 41: 305–318. 

Telenius A & Torstensson P (1989) The seed dimorphism of 

Spergularia marina in relation to dispersal by wind and 

water. Oecologia 80: 206–210. 

Telenius A & Torstensson P (1991) Seed wings in relation to 

seed size in the genus Spergularia. Oikos 61: 216–222. 

Thompson K, Band SR & Hodgson JG (1993) Seed size and shape 

predict persistence in soil. Functional Ecology 7: 236–241. 

Thornton NC (1935) Factors influencing germination and 

developement of dormancy in Cocklebur seeds. Contribution 

Boyce Thompson Institut 7: 477–496. 

Trapp EJ (1988) Dispersal of heteromorphic seeds in Amphicarpus 

bracteata (Fabaceae). American Journal of Botany 

75: 1535–1539. 

Troumbis A & Trabaud L (1987) Dynamique de la banque 

de graines de deux espèces de cistes dans les maquis grecs. 

Acta Oecologica 8: 167–179. 

Ungar IA (1971) Atriplex patula var. hastata (L.) Gray seed 

dimorphism. Rhodora 73: 548–551. 

Ungar IA (1979) Seed dimorphism in Salicornia europaea L. 

Botanical Gazette 140: 102–108. 

Ungar IA (1987) Population ecology of halophyte seeds. The 

Botanical Review 53: 301–334. 

Venable DL (1985a) The evolutionary ecology of seed heteromorphism. 

The American Naturalist 126: 577–595. 

Venable DL (1985b) Ecology of achene dimorphism in Heterotheca 

latifolia III. Consequences of varied water availibility. 

Journal of Ecology 73: 757–763. 

Venable DL & Brown JS (1988) The selective interactions of 

dispersal, dormancy and seed size as adaptations for reducing 

risk in variable environments. The American Naturalist 

131: 360–384. 

Venable DL & Burquez AM (1989) Quantitative genetics of 

size, shape, life-history and fruit characteristics of the seedheteromorphic 

composite Heterosperma pinnatum. I. Variation 

within and among populations. Evolution 43: 113–124. 


32 E. Imbert 

Venable DL & Lawlor L (1980) Delayed germination and 

dispersal in desert annuals, escape in space and time. Oecologia 

46: 272–282. 

Venable DL & Levin DA (1985a) Ecology of achene dimorphism 

in Heterotheca latifolia. I. Achene structure, 

germination and dispersal. Journal of Ecology 

73: 133–145. 

Venable DL & Levin DA (1985b) Ecology of achene dimorphism 

in Heterotheca latifolia. II. Demographic variation 

within populations. Journal of Ecology 73: 743–755. 

Venable DL, Burquez AM, Corral G, Morales E & Espinosa 

F (1987) The ecology of seed heteromorphism in 

Heterosperma pinnatum in Central Mexico. Ecology 

68: 65–76. 

Vuillemin J & Bulard C (1981) Ecophysiologie de la germination 

de Cistus albidus L et Cistus monspeliensis L. Naturalia 

monspeliensia 46: 1–11. 

Wagenknecht BL (1960) Revision of Heterotheca section 

Heterotheca (Compositae). Rhodora 62: 61–76/97–107. 

Weiss PW (1980) Germination, reproduction and interference 

in the amphicarpic annual Emex spinosa. Oecologia 

45: 244–251. 

Wells CL & Pigliucci M (2000) Adaptive phenotypic plasticity, 

the case of heterophylly in aquatic plants. Perspectives 

in Plant Ecology, Evolution and Systematics 

3: 1–18. 

Werker E & Many T (1974) Heterocarpy and its ontogeny 

in Aellinia autrani (Post) Zoh., light and electron-microscope 

study. Israel Journal of Botany 23: 132–144. 

Wertis BA & Ungar IA (1986) Seed demography and 

seedling survival in a population of Atriplex triangularis 

Willd. The American Midland Naturalist 116: 

152–162. 

Westoby M (1981) How diversified seed germination behavior 

is selected? The American Naturalist 118: 882–885. 

Wiggins IL (1980) Flora of Baja California. Stanford University 

Press, Stanford. 


Williams CM (1960) Biochemical analyses, germination and 

production of black and brown seeds of Halogeton glomeratus. 

Weeds 8: 452–461. 

Williams JT & Harper JL (1965) Seed dimorphism and germination. 

I. The influence of nitrates and low temperatures 

on the germination of Chenopodium album. Weed 

Research 5: 141–150. 

Wilson RC (1974) Abronia, II. Anthocarp polymorphism 

and anatomy for the nine species of Abronia found in California. 

Aliso 8: 113–128. 

Wulff RD (1986a) Seed size variation in Desmodium paniculatum. 

I. Factors affecting seed size. Journal of Ecology 74: 87–98. 

Wulff RD (1986b) Seed size variation in Desmodium paniculatum. 

II. Effects on seedling growth and physiological 

performance. Journal of Ecology 74: 99–114. 

Yu D, Kotilainen M, Pöllänen E, Mehto M, Elomaa P, Helariutta 

Y, Albert VA & Teeri TH (1999) Organ identity genes 

and modified patterns of flower development in Gerbera 

hybrida (Asteraceae). The Plant Journal 17: 51–62. 

Zeide B (1978) Reproductive behavior of plants in time. The 

American Naturalist 112: 636–639. 

Zhang J (1993) Seed dimorphism in relation to germination 

and growth of Cakile edentula. Canadian Journal of 

Botany 71: 1231–1235. 

Zhang J (1995) Differences in phenotypic plasticity between 

plants from dimorphic seeds of Cakile edentula. Oecologia 

102: 353–360. 

Zohary M (1950) Evolutionary trends in the fruiting head of 

Compositae. Evolution 4: 103–109. 

Zohary M (1962) Plant Life of Palestine. The Ronald Press 

Company, USA. 

Zohary M (1966) Flora Palaestina, Part 1 – Equisetaceae to 

Moringaceae. The Israel Academy of Sciences and Humanities, 

Jerusalem. 

Zohary M (1972) Flora Palaestina, Part 2 – Plantanaceae to 

Umbelliferae. The Israel Academy of Sciences and Humanities, 

Jerusalem.

Appendix 


List of seed heteromorphic species. An asterisk indicates that the taxon is not referenced in the Global Provisional Checklist made by the International Organization 

for Plant Information (www.bgbm.fu-berlin.de/IOPI/GPC/default.htm, last updated 27 November 2000). The name of the species is given in parentheses 

when the named used in the cited reference is different from the name given in the checklist. 

Family Species References 

Apiaceae * Peucedanum spreitzenhoferi Dingl. Zohary (1972) 

Apiaceae * Tordylium aegyptiacum (L.) Lam. Zohary (1972) 

Apiaceae Torilis nodosa (L.) Gaertner Montégut (1970) 

Asteraceae * Aaronsohnia factorovskyi Warb. & Eig. Zohary (1962) 

Asteraceae Achyrachaena mollis Schauer Becker (1913) 

Asteraceae Anacyclus clavatus (Desf.) Pers. Bischof (1978) 

Asteraceae Anacyclus radiatus Loisel. Petit (1990) 

Asteraceae Anthemis chia L. Feinbrun-Dothan & Zohary (1978) 

Asteraceae * Anthemis cornucopiae Boiss. Feinbrun-Dothan & Zohary (1978) 

Asteraceae * Anthemis leucanthemifolia Boiss. & Bl. Feinbrun-Dothan & Zohary (1978) 

Asteraceae * Arctotis fastuosa Jacq. Beneke et al. (1992b, (1993a, b) 

Asteraceae Bidens bipinnata L. Dakshini & Aggarwal (1974), Brown & Mitchell (1984) 

Asteraceae Bidens pilosa L. Forsyth & Brown (1982), Corkidi et al. (1991) (B. odorata Cav.), Rocha (1996) 

Asteraceae Bidens tripartita L. Montégut (1970) (B. tripartitus) 

Asteraceae Boltonia decurrens (Torr. & Gray) Wood Smith & Keevin (1998) 

Asteraceae Buphthalmum salicifolium L. Becker (1913) 

Asteraceae Calendula arvensis L. Zohary (1962) (C. aegyptiaca), Heyn et al. (1974), 

Gardocki et al. (2000) (C.micrantha) 

Asteraceae * Calendula eriocarpa Becker (1913) 

Asteraceae Calendula officinalis L. Becker (1913) 

Asteraceae * Calendula pachysperma Zoh. Heyn et al. (1974) 

Asteraceae Calendula palaestina Boiss. Heyn et al. (1974) 

Asteraceae Calendula stellata Cav. Becker (1913), Heyn et al. (1974), Petit (1990) 

Asteraceae Calendula suffruticosa Vahl. Becker (1913) (C. microphylla) 

Asteraceae Calendula tripterocarpa Rupr. Heyn et al. (1974), Feinbrun-Dothan & Zohary (1978) 

Asteraceae Carduus pycnocephalus L. Olivieri et al. (1983), Olivieri & Gouyon (1985) 

Asteraceae Carduus tenuiflorus Curt. Olivieri et al. (1983), Olivieri & Gouyon (1985) 

Asteraceae Carthamus arborescens L. Quézel & Santa (1962) 

Asteraceae Carthamus lanatus L. Petit (1990) 

Asteraceae Catananche caerula L. Petit (1990) 

Asteraceae Catananche lutea L. Becker (1913), Ruiz de Clavijo (1995), Ruiz de Clavijo & Jimenez (1998) 

Asteraceae * Centaurea aegyptiaca L. Zohary (1962) 

Asteraceae Centaurea hyalolepis Boiss. Zohary (1962) 

Asteraceae Centaurea melitensis L. Porras & Muñoz (2000) 

Asteraceae Centaurea solstitialis L. Olivieri & Berger (1985), Petit (1990), Joley et al. (1997) 

Asteraceae * Chardinia xeranthemoides Desf. Becker (1913) 

Asteraceae * Charieis heterophylla Becker (1913) 

Asteraceae Chrysanthemum carinatum Schousboe Becker (1913) (C. carinatum album) 

Asteraceae Chrysanthemum coronarium L. Becker (1913) 

Asteraceae Chrysanthemum frutescens L. Becker (1913) 

Asteraceae Chrysanthemum segetum L. Becker (1913) (C. segetum grandiflorum L.), Montégut (1970) 

Asteraceae * Chrysanthemum viscosum L. Becker (1913) 

Asteraceae Coleostephus myconis (L.) Reichenb. fil. Becker (1913) 

Asteraceae * Crepis aculeata (DC) Boiss. Babcock (1947) 

Asteraceae Crepis alpina L. Babcock (1947) 

Asteraceae * Crepis amplexifolia (Godr.) Willk Babcock (1947) 

Asteraceae Crepis aspera L. Becker (1913) (Endoptera aspera DC), Babcock (1947) 

Asteraceae Crepis atheniensis Babc. Babcock (1947) 

Asteraceae * Crepis Balliana Babc. Babcock (1947) 

Asteraceae * Crepis connexa Babc. Babcock (1947) 

Asteraceae Crepis dioscoridis L. Becker (1913) (Endoptera dioscoridis DC), Babcock (1947) 

Asteraceae * Crepis eritreënsis Babc. Babcock (1947) 

Asteraceae Crepis foetida L. Babcock (1947), Petit (1990) 

Asteraceae Crepis hokkaidoensis Babc. Babcock (1947) 

Asteraceae * Crepis juvenalis Delile Babcock (1947) 

Asteraceae Crepis leontodontoides All. E. Imbert, pers. observ. 

Asteraceae * Crepis Muhlisii Babc. Babcock (1947) 

Asteraceae Crepis multiflora Sibth & Sm. Babcock (1947) 


34 E. Imbert 


Asteraceae Crepis neglecta L. Babcock (1947) (C. corymbosa Ten., C. cretica Boiss.) 

Asteraceae * Crepis nigricans Viv. Babcock (1947) 

Asteraceae * Crepis palaestina (Boiss.) Bornm. Babcock (1947), Zohary (1962) 

Asteraceae Crepis pulchra L. Babcock (1947) 

Asteraceae Crepis rubra L. Becker (1913), Babcock (1947) 

Asteraceae Crepis sancta (L.) Babc. Babcock (1947) 

Asteraceae * Crepis Shimperi Schultz-Bip. Babcock (1947) 

Asteraceae * Crepis syriaca (Bornm.) Babc. Babcock (1947) 

Asteraceae * Crepis Thomsonii Babc. Babcock (1947) 

Asteraceae Crepis tybakiensis Vierh. Babcock. (1947) 

Asteraceae Crepis vesicaria L. Babcock (1947), Petit (1990) 

Asteraceae * Crepis xylorrhiza Sch. & Bip. Babcock (1947) 

Asteraceae Crepis zacintha (L.) Babc. Becker (1913) (Zacintha verrucosa Grtn.), Babcock (1947) 

Asteraceae Dimorphotheca hybrida Becker (1913) 

Asteraceae * Dimorphotheca montana E. Imbert, pers. observ. 

Asteraceae Dimorphotheca pluvialis (L.) Moench. Correns (1906), Becker (1913) 

Asteraceae * Dimorphotheca polyptera DC Beneke et al. (1992a, 1993a) 

Asteraceae Dimorphotheca sinuata DC Beneke et al. (1992a, 1993a, b) 

Asteraceae * Dimorphotheca zeyhea E. Imbert, pers. observ. 

Asteraceae Filago vulgaris Lam. Petit (1990) (F. germanica) 

Asteraceae Galinsoga parviflora Cav. Becker (1913), Rai & Tripathi (1987) 

Asteraceae Garhadiolus angulosus Jaub. & Spach. Feinbrun-Dothan & Zohary (1978) 

Asteraceae * Geigeria alata Burke (1995) 

Asteraceae Grindelia papposa Nesom & Suh Gibson (2001) (Prionopsis ciliata (Nutt.) Nutt.) 

Asteraceae Grindelia squarrosa (Pursh.) Dunal McDonough (1975) 

Asteraceae Gymnarhena micrantha Desf. Evenari (1963), Koller & Roth (1964) 

Asteraceae Hedypnois arenaria (Schousboe) DC. Petit (1990) 

Asteraceae Hedypnois cretica (L.) Dum.-Cours. Becker (1913), Kigel (1992) (H. rhagadioloides (L.) F.W. Schmidt) 

Asteraceae Hemizonia increscens (Hall ex Keck) Tanowitz Tanowitz et al. (1987) 

Asteraceae Heterosperma pinnatum Cav. Venable et al. (1987) 

Asteraceae * Heterospermun Xanthii Becker (1913) 

Asteraceae Heterotheca chrysopsides DC. Wagenknecht (1960) 

Asteraceae Heterotheca grandiflora Nutt. Wagenknecht (1960), Flint & Palmblad (1978) 

Asteraceae Heterotheca inuloides Cass. Wagenknecht (1960) 

Asteraceae Heterotheca leptoglossa DC. Wagenknecht (1960) 

Asteraceae Heterotheca psammophila Wagenkn. Wagenknecht (1960) 

Asteraceae Heterotheca subaxillaris (Lam.) Britt. & Rusby Becker (1913) (H. Lamarckii), Wagenknecht (1960) (H. latifolia Buckl.) 

Baskin & Baskin (1976), Venable & Levin (1985a, b) (H. latifolia Buckl.) 

Asteraceae Hyoseris radiata L. E. Sahnoune, pers. comm. 

Asteraceae Hyoseris scabra L. Petit (1990), E. Imbert, pers. observ. 

Asteraceae Hypochoeris achyrophorus L. Petit (1990) 

Asteraceae Hypochoeris glabra L. Becker (1913), Baker & O’Dowd (1982) 

Asteraceae Hypochoeris radicata L. Petit (1990) 

Asteraceae * Laya elegans Becker (1913) 

Asteraceae * Laya glandulosa Becker (1913) 

Asteraceae * Laya heterotricha Becker (1913) 

Asteraceae * Laya platyglossa Becker (1913) 

Asteraceae Leontodon maroccanus (Pers.) Ball. Petit (1990) 

Asteraceae Leontodon muelleri (Schultz-Bip.) Fiori Quézel & Santa (1962) (L. hispidulus (Del.) Boiss.), Petit (1990) 

Asteraceae Leontodon salzmanii (Schultz-Bip.) Ball Petit (1990) 

Asteraceae Leontodon taraxacoides (Vill.) Mérat Becker (1913) (Thrincia hirta Roth.), Quézel & Santa (1962) (L. saxatilis Lam.), 

Burtt (1977), Ruiz de Claivo (2001) (L. longirrostris (Finch & PD Sell) Talavera) 

Asteraceae Leontodon tuberosus L. Zohary (1962) (Thrincia tuberosa), Feinbrun-Dothan & Zohary (1978) 

(Thrincia tuberosa L.) 

Asteraceae Microseris bigelovii (Gray) Schultz-Bip. Bachmann & Chambers (1990) 

Asteraceae Microseris douglasii (DC.) Schultz-Bip. Bachmann & Price (1979) 

Asteraceae Pallenis spinosa (L.) Cass. Feinbrun-Dothan & Zohary (1978) 

Asteraceae * Picris amalecitana (Boiss.) Eig Feinbrun-Dothan & Zohary (1978), Ellner & Shmida (1984) 

Asteraceae * Picris asplenioides Petit (1990) 

Asteraceae * Picris cupuligera Petit (1990) 

Asteraceae * Picris damascena Boiss & Gaill. Zohary (1962), Feinbrun-Dothan & Zohary (1978), Ellner & Shmida (1984) 

Asteraceae Picris echioides L. Sorensen (1978), Petit (1990) (Helminthotheca echioides) 

Asteraceae * Picris galilea (Boiss.) Benth. & Hook Feinbrun-Dothan & Zohary (1978), Ellner & Shmida (1984) 

Asteraceae Picris hispanica (Willd.) P.D. Sell Quézel & Santa (1962) (Leontodon hispanicus Poiret) 

Asteraceae * Picris intermedia Zohary (1962), Ellner & Shmida (1984) 

Perspectives in Plant Ecology, Evolution and Systematics (2002) 5, 13–36



Asteraceae * Picris radicata (Forssk.) Less. Feinbrun-Dothan & Zohary (1978), Ellner & Shmida (1984) 

Asteraceae Picris sprengeriana (L.) Poir. Feinbrun-Dothan & Zohary (1978) 

Asteraceae Podolepis canescens DC. Becker (1913) 

Asteraceae Reichardia intermedia (Schultz-Bip) Coutinho Feinbrun-Dothan & Zohary (1978) 

Asteraceae Reichardia tingitana (L.) Roth Zohary (1962), Feinbrun-Dothan & Zohary (1978), Ellner & Shmida (1981) 

Asteraceae Rhagadiolus stellatus (L.) Gaertn. Becker (1913) (R. edulis), Petit (1990) 

Asteraceae Sanvitalia procumbens Lam. Becker (1913) 

Asteraceae Senecio gallicus Chaix Zohary (1972) (S. coronopifolius) 

Asteraceae Senecio jacobaea L. McEvoy (1984), McEvoy & Cox (1987) 

Asteraceae Sigesbeckia orientalis L. Becker (1913) 

Asteraceae Synedrella nodiflora (L.) Gaertn Ernst (1906), Becker (1913) 

Asteraceae Thrincia hispida Roth. Becker (1913) 

Asteraceae Tolpis barbata (L.) Gaertn. Becker (1913) 

Asteraceae Tragopogon dubius Scop. Maxwell et al. (1994), McGinley (1989) (Tragopogon dubious L.) 

Asteraceae Tragopogon hybridus (L.) Schultz-Bip. Becker (1913) (Geropogon glaber L.), Feinbrun-Dothan & Zohary (1978) 

(Geropogon hybridus (L.) Schultz-Bip.), Petit (1990) 

Asteraceae * Ursinia cakilefolia DC Beneke et al. (1992b, 1993a) 

Asteraceae Xanthium strumarium L. Shull (1911) (X. pennsylvanicum and X. glabratum), 

Thornton (1935) (X.canadense Mill.), Senseman & Oliver (1993) 

Asteraceae Xanthocephalum gymnospermoides (Gray.) Bent. & Hook. Becker (1913) 

Asteraceae Ximenesia enceliodes (Cav.) Bent. & Hook. fil. Becker (1913) 

Asteraceae Zinnia elegans Jacq. Becker (1913) 

Asteraceae Zinnia peruviana (L.) L. Becker (1913) (Z. pauciflora) 

Asteraceae * Zinnia verticillata Becker (1913) 

Brassicaceae Aethionema carneum (Banks & Sol.) Fedtsch. Zohary (1966) 

Brassicaceae Aethionema heterocarpum Trev. Zohary (1966) (A. heterocarpum J. Gay) 

Brassicaceae Aethionema saxatile (L.) R. Br. Andersson et al. (1983) 

Brassicaceae Cakile edentula (Bigelow) Hook. Maun & Payne (1989) (C. edentula var. edentula et var. lacustris), 

Zhang (1993, 1995) 

Brassicaceae Cakile maritima Scop. Becker (1913), Barbour (1970), Maun & Payne (1989) (C. maritima var. maritima) 

Brassicaceae * Cardamine chenopodifolia Pers. Battandier (1883), Becker (1913), Cheplick (1983) 

Brassicaceae Erucaria microcarpa Boiss. Ellner & Shmida (1981) (Reboudia pinnata) 

Brassicaceae Erucaria rostrata Boiss. Zohary (1962) (Erucaria boveana) 

Brassicaceae Fezia pterocarpa Pitard Maire (1965) 

Brassicaceae Hirschfeldia incana (L.) Lagrze-Fossat Zohary (1962) 

Brassicaceae Rapistrum rugosum (L.) All. Becker (1913) 

Brassicaceae Sinapis alba L. Zohary (1966) 

Caryophyllaceae Pteranthus dichotomus Forssk. Evenari (1963) 

Caryophyllaceae Spergularia canadensis (Pers.) G. Don Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia echinosperma Celak. Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia embergeri Monnier Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia fasiculata Phil. Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia fimbriata Murb. Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia macrotheca Robinson Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia marina (L.) Griseb. Salisbury (1958) (S. salina J.S.& C.B. Presl), Sterk (1969), 

Telenius & Torstensson (1989), Redbo-Torstensson & Telenius (1995) 

Caryophyllaceae Spergularia maritima (All.) Chiov. Salisbury (1958) (S. marginata Kittel), Sterk (1969) (S. media), 

Telenius (1992), Redbo-Torstensson & Telenius (1995) (S. media (L.) C. Presl.) 

Caryophyllaceae Spergularia tangerina Monnier Telenius & Torstensson (1991) 

Caryophyllaceae Spergularia villosa Cambess. Telenius & Torstensson (1991) 

Chenopodiaceae * Aellenia autrani (Post) Zoh. Negbi & Tamari (1963), Werker & Many (1974) 

Chenopodiaceae Arthrocnenum macrostachyum (Moric.) Moris Khan et al. (1998), Khan & Gul (1998) (A. indicum Willd.) 

Chenopodiaceae Atriplex dimorphostegia Kar & Kir Koller (1957) 

Chenopodiaceae Atriplex hortensis L. Becker (1913), Frankton & Basset (1968) 

Chenopodiaceae Atriplex micrantha Ledeb. Frankton & Basset (1968) (A. heterosperma Bunge) 

Chenopodiaceae Atriplex oblongifolia Waldst. & Kit Frankton & Basset (1968) 

Chenopodiaceae Atriplex patula L. Ungar (1971) 

Chenopodiaceae Atriplex prostrata (Boucher) ex. DC Wertis & Ungar (1986) (A. triangularis Willd.), Ellison (1987) (A. triangularis) 


36 E. Imbert 


Chenopodiaceae Atriplex sagittata Borkh. Becker (1913) (A. nitens Schkuhr), Mandák & Pysˇek (1999a, b, 2001a, b) 

Chenopodiaceae Atriplex semibaccata R.Br. Beadle (1952) 

Chenopodiaceae Axyris amaranthoides L. Becker (1913) 

Chenopodiaceae Blackiella inflata (F. Mueller) Aaelen Beadle (1952) (Atriplex inflata) 

Chenopodiaceae Chenopodium album L. Williams & Harper (1965) 

Chenopodiaceae Halogeton glomeratus (Bieb.) C.A. Mey. Williams (1960) 

Chenopodiaceae Salicornia europaea L. Ungar (1979), Philipupillai & Ungar (1984), Austenfeld (1988) 

Grouzis et al. (1976), Berger (1985) (S. patula Duval-Jouve) 

Chenopodiaceae * Salsola komarovii Iljin Takeno & Yamaguchi (1991) 

Chenopodiaceae Salsola volkensii Asch. & Schw. Negbi & Tamari (1963) 

Chenopodiaceae Sennellia spongiosa (F. Mueller) Aellen Beadle (1952) (Atriplex spongiosa) 

Cistaceae Cistus albidus L. Vuillemin & Bullard (1981) 

Cistaceae Cistus creticus L. Troumbis & Trabaud (1987) 

Cistaceae Cistus monspeliensis L. Vuillemin & Bulard (1981) 

Cistaceae Cistus salviifolius L. Troumbis & Trabaud (1987) 

Commelinaceae Commelina benghalensis L. Budd et al. (1979) 

Euphorbiaceae Croton setigerus (Hook.) Benth. Cook et al. (1971) (Emerocarpus setigerus) 

Fabaceae * Alysicarpus monilifer DC Maurya & Ambasht (1973) 

Fabaceae Amphicarpaea bracteata (L.) Fern. Schnee & Waller (1986), Trapp (1988), Callahan & Waller (2000) 

Fabaceae * Lathyrus ciliolatus Sam. ex. Rech. f. Mattatia (1977a) 

Fabaceae Pisum fulvum Sibth. & Sm. Mattatia (1977b) (P. fulvum Sibth. & Sm. var amphicarpum Warb & Eig.) 

Fabaceae Vicia sativa subsp. amphicarpa (Dorth.) Aschers & Graebn Plitmann (1973) 

Fumariaceae Ceratocapnos heterocarpa Durieu Ruiz de Clavijo (1994) 

Nyctaginaceae Abronia alpina Brandeg. Wilson (1974) 

Nyctaginaceae Abronia crux-maltae Kell. Wilson (1974) 

Nyctaginaceae Abronia latifolia Eschs. Wilson (1974) 

Nyctaginaceae Abronia maritima Nutt. ex S. Wats. Wilson (1974), Wiggins (1980) 

Nyctaginaceae Abronia nana S. Wats. Wilson (1974) 

Nyctaginaceae Abronia pogonantha Heimerl. Wilson (1974) 

Nyctaginaceae Abronia turbinata Torr. ex. S. Wats. Wilson (1974) 

Nyctaginaceae Abronia umbellata Lam. Wilson (1974), Wiggins (1980) 

Nyctaginaceae Abronia villosa S. Wats. Wilson (1974), Wiggins (1980) 

Papaveraceae Glaucium flavum Crantz Martin (1996) 

Papaveraceae Platystemon californicus Benth. Hannan (1980) 

Plantaginaceae Plantago coronopus L. Dowling (1933), Schat (1981) 

Poaceae Agrostis hyemalis (Walt) B.S.P. Rabinowitz & Rapp (1979) 

Poaceae Amphibromus scabrivalvis (Trin) Swallen Cheplick & Clay (1989) 

Poaceae Amphicarpum purshii Kunth. McNamara & Quinn (1977), Cheplick & Quinn (1982) 

Poaceae Danthonia spicata (L.) Beauv. Clay (1982, 1983), Cheplick & Clay (1989) 

Poaceae Echinochloa crus-galli (L.) Beauv. Montégut (1970) 

Poaceae Nasella leucotricha (Trin. & Rupr.) Pohl. Dyksterhuis (1945) (Stipa leucotricha Trin. & Rupr.) 

Poaceae Triplasis purpurea (Walt) Chapm. Cheplick (1996b), Cheplick & Grandstaff (1997), Cheplick & Sung (1998) 

Poaceae Cheplick & Wickstrom (1999) 

Polygonaceae Emex spinosa (L.) Campd. Weiss (1980) 

Rubiaceae Asperula arvensis L. Montégut (1970) 

Thymeleaceae * Thymelea velutina (Poiret ex Camb.) Endl. Tébar & Llorens (1993) 

Valerianaceae Fedia cornucopiae (L.) Gaertn. Mathez & Xena de Enrech (1985) (F. graciliflora Fisch. & Meyer) 

Valerianaceae * Fedia pallescens Mathez Mathez & Xena de Enrech (1985) 

Perspectives in Plant Ecology, Evolution and Systematics (2002) 5, 13–36

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