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OIKOS 109: 521 /534, 2005

Individuals as the basic accounting unit in studies of ecosystem


function: functional diversity in shepherds purse, Capsella
C. Hawes, G. S. Begg, G. R. Squire and P. P. M. Iannetta

Hawes, C., Begg, G. S., Squire, G. R. and Iannetta, P. P. M. 2005. Individuals as the
basic accounting unit in studies of ecosystem function: functional diversity in
shepherds purse, Capsella. / Oikos 109: 521 /534.
Agricultural intensification has led to a systematic erosion of the biodiversity in arable
ecosystems. Despite this, densities of plant species in the seedbank of arable fields are
still sufficient to provide the potential for recovery of the arable flora and associated
fauna. Identification of management practices to achieve this, while minimising
negative effects of weed competition on crop yield, requires a mechanistic
understanding of functional diversity in arable systems. However, a review of the
ecological, physiological and genetic characteristics of 66 representative UK arable
weed species revealed major gaps in this knowledge for even the most common species.
Even less is known about the degree of variation between individuals within these
species that contributes to overall levels of functional diversity. Classification of
organisms into functional groups on the basis of species-level taxonomy is inadequate
to describe the functional diversity of a system, since variability in a particular
physiological trait can be as great between individuals within a species as between
species. We therefore propose an individual based approach to examine the functional
attributes of arable plants that affect resource acquisition, partitioning and energy
transfer through the food web. Capsella (shepherds purse) is proposed as a key species
that is widespread, ecologically important, and physiologically and genetically diverse.
Current understanding of Capsella systematics is therefore reviewed and a
methodological approach is described that establishes a foundation for studies of
biodiversity and function in arable systems.
C. Hawes, G. S. Begg, G. R. Squire and P. P. M. Iannetta, Ecosystem Management and
Biotechnology, Scottish Crop Research Institute, Invergowrie Dundee DD2 5DA
Scotland, UK (chawes@scri.sari.ac.uk).

Since the 1920s farming practice in the UK has


intensified and now approximately 70% of Britains
cultivated land surface is agricultural, of which 40% is
under arable production (National Statistics, June 2001).
Over this period, an increase in the intensity of herbicide
use and the proportion of long-season (autumn-sown)
crops have contributed to a decline in the abundance and
diversity of the arable flora (Preston et al. 2002,
Marshall et al. 2003). This loss of diversity can disrupt
a range of system functions including retention of
nutrients and water, regulation of pest populations, and
detoxification of chemical deposits including pesticides

(Altierri 1999, Hector et al. 1999, 2001, Knops et al.


1999, Tilman 1999, Deutschman 2001, Petchey et al.
2002). In addition, evidence from surveys of arable
diversity (Krebs et al. 1999, Moreby and Southway
1999, Chamberlain et al. 2000, Hawes et al. 2003,
Marshall et al. 2003), and manipulative experiments in
arable and grassland habitats (Siemann et al. 1998,
Knops et al. 1999, Buckelew et al. 2000, Koricheva
et al. 2000, Haddad et al. 2001, Asteraki et al. 2003)
show that a reduction in the diversity of primary
producers is related to a decline in abundance and
diversity of associated invertebrate communities. A

Accepted 11 November 2004


Copyright # OIKOS 2005
ISSN 0030-1299
OIKOS 109:3 (2005)

521

Arable diversity and crop productivity


The above ground arable weed flora depends largely on
annual replenishment from the buried seedbank. In the
absence of re-seeding, the seedbank is subject to decay
rates of about 50% a year (Brenchley and Warington
1933, Roberts 1962, Wilson and Lawson 1992). The
diversity and abundance of the arable flora are therefore
strongly dependent on the type and frequency of
opportunities for re-seeding. Where this is prevented,
populations of all species in the seedbank decline
(Roberts 1958, 1962, Fig. 1a), particularly those that
decay rapidly such as Poa annua , Polygonum aviculare
and Stellaria media . Similarly, reduced re-seeding of
late-flowering annuals can rapidly alter plant community
composition (Brenchley and Warington 1933, Fig. 1b).
The importance of flowering period to species survival
in such disturbed systems is also illustrated in
Table 1. Common species (those found at over 50%
of 200 sites surveyed across the UK, Heard et al.
2003) are predominantly annual, displaying a range of
522

1955 seed density m 2 (log N+1)

(a)

0
0

5
1930 seed density m 2 (log N+1)

diverse plant community tends to be associated with a


lower herbivore load, fewer outbreaks of pests, and
higher numbers of non-pest species (Root 1973, Cromartie 1975, Powell et al. 1985, reviewed by Andow
1991). Weed diversity is therefore essential for maintaining both function and resilience in arable systems.
Enhanced system function, usually measured as total
productivity, can occur through niche complementarity,
where greater variation among species in a diverse
community results in a more efficient use of the available
resources (Grime 1998, Loreau 2000, Cottingham et al.
2001). Resilience may be increased through functional
redundancy, where greater numbers of species performing similar roles reduce the likelihood that a system
process will be disrupted if a species is lost (Walker 1992,
Walker et al. 1999, Yachi and Loreau 1999).
There is a potential to exploit these mechanisms to
allow increased diversity of the arable flora and associated fauna, while minimising any negative effect of
weed competition on crop yield. Identification of management practices to achieve this goal requires a mechanistic understanding of the relation between diversity and
function in arable systems, and detailed knowledge of the
ecology and genetics of arable plants. This paper brings
together existing information on the weed diversity of
UK arable fields, and the ecological, physiological and
genetic characteristics of 66 representative weed species.
Key functional traits are identified, and the genetic basis
of variation in these traits for a model species, shepherds
purse (Capsella species), is reviewed. A novel trait-based
approach to the study of arable diversity and system
function is then proposed, focussing initially on individual variation in Capsella species.

1
2
3
4
1953 seed density m 2 (logN+1)

(b)

0
0

1
2
3
4
1925 seed density m 2 (log N+1)

Fig. 1. Changes in the seed density of arable weed species in the


seedbank (a) showing the decline in total seed density for each
species after two years of no seed return (data from Roberts
1958), and (b) showing change in seedbank densities where
disturbance regimes favoured species with short time to flowering (data from Brenchley and Warington 1933).

germination and flowering characteristics. Spring, autumn and year-round germination types are equally
represented, and a third of species have the potential
to flower throughout the year. These common species
therefore possess life history traits that enable them to
persist despite the high levels of disturbance characteristic of arable systems. All of these common species are
adapted to high soil nutrient conditions and a high
proportion (about 40%) are thought to be increasing in
population density (Ecological flora of the British Isles
database, Table 1). By contrast, those classified as rare
(occurring in 2% of sites or less) are less well adapted to
arable conditions and many of these species populations
are declining (Table 1). A greater proportion are
restricted to autumn-germination, have flowering periods of just one to two months a year, and display
preferences for lower fertility soils. Field management
practices therefore select for particular plant traits and
can have a major impact on the range of plant types
represented in the arable seedbank.
OIKOS 109:3 (2005)

OIKOS 109:3 (2005)

Apiaceae

Asteraceae

Aethusa
cynapium
Petroselinum
segetum
Scandix
pectin-veneris
Torilis
arvensis
Centaurea
cyanus
Chrysanthemum
segetum
Cirsium arvense
Filago apiculata

Boraginaceae

Filago
pyramidata
Matricaria
recutita
Senecio vulgaris
Sonchus
oleraceus
Tripleurospermum
inodorum
Lithospermum
arvense
Myosotis arvensis

Chromosome
number

Ploidy level

DNA content

Mycorrhizal
association

Fertilization

Seed weight (mg)

/ /

Typical height (cm)

Flowering period
(months)

Germination

Life history

Number of insect
species supported

Competitive
ability

Soil nutrient
requirement

Frequency
(and dynamics)

Species

Family

Common
name

Table 1. A representative list of 66 arable weed species with ecological, physiological and genetic information collated from Marshall et al. (2003), Cussons and Courtney (1995),
Clapham et al. (1962), Naylor (2002), from unpublished seedbank data held at SCRI, and from http://www.rbgkew.org.uk/cvalues/ and http://www.york.ac.uk/res/ecoflora/cfm/ecofl/
index.cfm/. Frequency of occurrence in the 200 sites sampled for the Farm-Scale Evaluations (Champion et al. 2003)-rare (R): B/1%; frequent (F): 1 /50%; common (C): /50% of sites;
(/) indicates declining populations, (/) increasing population, (s) stable populations from references in the ecoflora database. Soil nutrient preferences / very fertile (VF), fertile (F),
infertile (I), very infertile (VI). Competitive ability is classified by competitive index (CI) or numbers of plants per m 2 to cause 5% yield loss: low (L) CI B/0.05//50 plants per m 2;
medium (M) CI/0.5 /1/10 /50 plants m 2; High (H) CI/1/ B/10 plants m 2. Life history is summarized as A (annual), B (biennial) or P (perennial). Germination is predominantly Sp
(spring), Au (autumn), W (winter) or Y (all year round). Flowering period is given as the number of months a year in which the species has the potential to flower. Fertilization is
described as primarily outcrossing (X) and/or selfing (S). Significance of each species to microbial communities is indicated in terms of their known mycorrhizal associations, where 0/no
known association, 1/rarely, 2/occasionally and 3/normally mycorrhizal. Genetic information is summarised as the 1C nuclear DNA content, ploidy level and chromosome number
of each species. / indicates that no data were available for the species.

fools parsley

/

/

Sp

7 /8

5 /125

1.64

X, S

/

/

20

corn parsley

/

/

Au

8 /9

30 /100

2.2

/

/

/

/

18

shepherds-needle

R (/)

/

/

Au, (Sp)

4 /7

15 /50

/

/

/

16

spreading
hedge-parsley
corn flower

R (/)

/

/

Au

7 /9

/

/

/

/

2.05

12

R (/)

F-I

/

/

Au, Sp

6 /8

20 /90

2.6 /4.5

/

/

24

corn marigold

R (/)

/

/

Au, (Sp)

6 /8

20 /60

1.9

X, S

7.35

18

creeping
thistle
red-tipped
cudweed
broad-leaved
cudweed
scented
mayweed
groundsel
smooth
sow-thistle
scentless
mayweed
field gromwell

VF-F

50

Au

7 /9

30 /90

1.2

X, S

1.55

34

/

/

/

/

7 /8

/

/

/

/

/

/

/

VI

/

/

/

/

/

5 /30

0.05

/

/

/

/

/

C (/)

15

6 /7

15 /60

0.06

/

/

/

/

/

C (s)
C (/)

VF-VI
F

L
/

47
28

A
A

Y
Sp

1 /12
6 /8

8 /45
20 /150

0.22
0.27

S
S

2
3

1.58
1.60

4
4

40
32

C (/)

31

7 /9

15 /60

0.29

/

1.95

/

18

VF-F

/

/

Au, (Sp)

5 /7

30 /80

6.0

/

/

/

28

VF-F

Au, (Sp)

4 /9

15 /60

0.29

/

/

24/48/52

field forgetme-not

523

524

Brassicaceae

Caryphyllaceae

Alyssum
alyssoides
Arabidopsis
thaliana
Capsella
bursa-pastoris/
rubella
Sinapsis arvensis
Cerastium
fontanum
Silene gallica
Silene noctiflora

Spergula arvensis
Stellaria media
Chenopodiaceae
Euphorbiaceae

Fabaceae
Fumariaceae

Chenopodium
album
Euphorbia
helioscopia
Euphorbia
platyphyllos
Vicia tenuissima
Fumaria bastardii
Fumaria
officinalis
Fumaria purpurea

OIKOS 109:3 (2005)

Geraniaceae
Lamiaceae

Geranium
dissectum
Ajuga
chamaepitys
Galeopsis
augustifolia

small Alison

I-VI

/

/

5 /6

7 /25

0.56

X, S

/

/

thale cress

F-VI

/

Au

4 /5

5 /50

0.03

shepherds purse

/

13

1 /12

3 /40

0.1

X, S

charlock
common
mouse-ear
smallflowered catchfly
nightflowering
catchfly
corn spurrey
common
chickweed
fat-hen

F (/)
F (s)

VF-F
F-I

M
/

38
22

A
P/A

Sp
Au

5 /7
4 /9

30 /80
45

2.0
0.16

R (/)

/

/

Sp

6 /10

15 /45

R (/)

VF-F

/

/

Sp

7 /9

15 /45

F (/)
C

F
F

/
M

/
71

A
A

Sp, (Au)
Au, Sp

6 /9
1 /12

C ( /)

31

Sp, (Au)

sun spurge

VF-F

/

/

broad-leaved
spurge
slender tare
tall rampingfumitory
common
fumitory
purple
rampingfumitory
cut-leaved
cranes-bill
ground- pine

VF-F

/

/

R
R (s)

/
VF-F

/
/

VF-VI

red hemp-nettle

Chromosome
number

Ploidy level

DNA content

Mycorrhizal
association

Fertilization

Seed weight (mg)

/ /

Typical height (cm)

Flowering period
(months)

Germination

Life history

Number of insect
species supported

Competitive
ability

Soil nutrient
requirement

Frequency
(and dynamics)

Species

Family

Common
name

Table 1 (Continued )

/

32

0.2

2/4

10

0.7

32

X, S
X, S

/
1

0.38 2
2.93 16

18
144

0.5

/

/

/

24

0.92

/

/

/

/

24

5 /60
5 /40

0.42
0.37 /0.67

X, S
X, S

1
2

1.05
1.05

/
7

18
42

7 /10

10 /100

0.77 /1.5

X, S

2.33

54

Sp

5 /10

10 /50

2.49

/

/

42

Au, (Sp)

6 /10

15 /80

/

/

/

/

18/28

/
/

A
A

/
Au, Sp

6 /8
4 /10

/
100

/
/

/
S

/
/

/
/

/
/

14
/

/

/

Sp, (Au)

5 /10

100

/

X, S

/

/

28

F-I

/

/

/

7 /10

100

/

/

/

/

/

VF-F

Au, Sp

5 /8

10 /60

/

/

22

VI

/

/

Au

5 /9

5 /20

1.16

/

/

/

/

28

R (/)

/

/

Sp

7 /10

10 /80

5.4

X, S

/

/

/

16

2.0 /3.0

Galeopsis tetrahit

Papaveraceae

Poaceae

Lamium
purpureum
Papaver
argemone
Papaver hybridum
Papaver rhoeas
Alopecurus
myosuroides
Anisantha sterilis
Apera spica-venti
Avena fatua
Elytrigia repens
Phleum phleoides
Poa annua

Polygonaceae

Primulaceae

Fallopia
convolvulus
Persicaria
maculosa
Polygonum aviculare
Polygonum
rurivagum
Rumex
obtusifolius
Anagallis arvensis

Chromosome
number

Ploidy level

DNA content

Mycorrhizal
association

Fertilization

Seed weight (mg)

/ /

Typical height (cm)

Flowering period
(months)

Germination

Life history

Number of insect
species supported

Competitive
ability

Soil nutrient
requirement

Frequency
(and dynamics)

Common
name

Species

Family

OIKOS 109:3 (2005)

Table 1 (Continued )

common hempnettle
red dead-nettle

F (///)

VF-F

/

Sp

7 /9

10 /100

4.83

/

/

32

C (/)

/

Au, Sp

3 /10

10 /45

0.7

X, S

1.10

18

prickly poppy

R (/)

I-VI

/

/

Au, Sp

6 /7

10 /50

0.15

X, S

/

/

/

12/42

rough poppy
common
poppy
black grass

R
F (/)

F-I
F-VF

/
M

/
8

A
A

Au, Sp
Au, (Sp)

6 /7
6 /8

10 /50
10 /50

0.16
0.14

S
X

/
1

2.48
2.63

2
2

14
14

C ( /)

VF-F

Au, (Sp)

5 /9

20 /70

2.0

4.33

/

14

barren brome
loose silky-bent
winter wild oat
Couch grass
purple-stem
cats-tail
annual
meadow grass
black
bindweed
redshank

F (/)
R
F (/)
F (/)
R

VF-F
/
VF-I
F
/

M
/
H
/
/

/
/
4
/
/

A
/
/
P
P

Au
Au
(Au), Sp
Au, Sp
/

5 /7
6 /7
7 /9
6 /9
6 /7

5 /100
20 /100
30 /100
30 /120
10 /40

8.4
0.12
14.1
2.02
/

S
X
S
X
X

/
3
2
3
3

3.35
5.40
14.15
/13.0
/

/
2
6
/
/

14
14
42
42
14/28

C (/)

52

1 /12

5 /30

0.48

2.88

28

/

/

Sp

5 /10

30 /120

1.28

0.72

40

F (/)

/

20

Sp

6 /10

25 /75

2.05

X, S

/

/

knotgrass
cornfield
knotgrass
broad leafed
dock
scarlet
pimpernel

C (/)
R

F
I

L
/

61
/

A
A

Sp
Sp

7 /10
7 /10

1.69
/

S
S

1
/

0.85
/

4
/

60
60

F (/)

VF-F

/

/

Sp

6 /10

15 /120

1.10

1.53

40

Sp

6 /8

6 /30

0.4

/

1.75

40

pheasants eye
corn buttercup

R (/)
R (/)

F-VI
I-VI

L
/

/
/

A
A

Sp, (Au)
Au

7
6 /7

10 /40
15 /60

/
X

/
/

/
6.13

/
4

32
32

common
cleavers
corn cleavers

F (/)

30

Au, (Sp)

6 /8

15 /120

7.25

X, S

1.03

/

44

/

/

/

/

6 /9

/

/

/

/

/

/

44

200
30

Ranunculaceae

Rubiaceae

Adonis annua
Ranunclus
arvensis
Galium aparine

525

Galium
tricornutum

4.8 /18.4
12

526
Scrophulariaceae

Melampyrum arvense
Veronica persica
Veronica praecox

Solanaceae
Urticaceae
Valerianaceae

Violaceae

Veronica
triphyllos
Solanum nigrum
Urtica dioica
Urtica urens
Valerianella
dentate
Valerianella
rimosa
Viola arvensis

field
cow-wheat
common
field-speedwell
brecklandspeedwell
fingered
speedwell
black
nightshade
common nettle
small nettle
narrow-fruited
cornsalad
broad-fruited
cornsalad
field pansy

R (/)

VF-I

/

/

Sp

6 /9

20 /60

Au, Sp

1 /12

10 /40

I-VI

/

/

/

3 /6

R (/)

VI

/

/

/

3 /6

VF-F

/

Sp

7 /9

C (/)
C
R (/)

F
F
F /I

/
/
L

/
/
/

P
A
A

Sp
Sp, (Au)
Au, Sp

/

VF-F

18.7

Chromosome
number

Ploidy level

DNA content

Mycorrhizal
association

Fertilization

Seed weight (mg)

/ /

Typical height (cm)

Flowering period
(months)

Germination

Life history

Number of insect
species supported

Competitive
ability

Soil nutrient
requirement

Frequency
(and dynamics)

Species

Family

Common
name

Table 1 (Continued )

X, S

/

/

18

0.52

X, S

0.78

28

5 /20

/

/

/

/

/

18

5 /20

/

X, S

/

/

/

14

60

0.97

3.10

72

6 /8
4 /10
6 /7

30 /150
10 /60
7 /40

0.2
0.5
1.0

X
/
S

2
0
/

1.58
0.33
/

4
/
/

52
24/26/52
14

/

7 /8

7 /40

/

/

/

/

14

Au, Sp

4 /10

15 /45

0.2

/

/

34

OIKOS 109:3 (2005)

Although crop and weed productivity are stereotyped


as antagonistic, seedbank densities could be allowed to
increase above the current level of 1000 /2000 m 2
without loss to yield if the community is dominated by
weed species with low competitive ability (Cussons and
Courtney 1994, Young et al. 2001). Quantitative data on
competitive abilities of different weed species are scarce
(only available for 36% of the species in Table 1), and
where they are given, are difficult to generalise. However,
negative effects of competition between plants can be
reduced through spatial and temporal segregation in
resource capture (May 1973, Tilman 1982, Chesson
2000, Barot and Gignoux 2004), and stable coexistence
maintained through processes such as phenotypic plasticity, resource specialisation, facilitation and immigration (Bengtsson et al. 1994, Mouquet et al. 2002,
Callaway et al. 2003). Coexistence between weeds and
crop plants may therefore be enhanced through variation
in life history traits relating to resource acquisition,
reproduction and recruitment, e.g. germination and seed
dispersal characteristics, root and above ground architecture, conversion efficiency of solar radiation, and time
to reproduction. The degree of variation in arable weed
assemblages with respect to these traits needs to be
quantified to identify ideal combinations of plant types
necessary to optimise biodiversity and crop yield.
Since the 1960s, the arable seed bank decline has been
estimated at approximately 4% a year (Robinson and
Sutherland 2002). However, measurements taken between 2000 and 2002 (Champion et al. 2003, Heard et al.
2003, Squire et al. 2003), were comparable to densities
recorded in the 1990s (Fig. 2). In addition, the common
species recorded from 1910 /19 by Brenchley (1920) are
still present (Marshall et al. 2003, Squire et al. 2003)

Mean seedbank density m log(N+1)

5.2

4.6

4.0

3.4

2.8

2.2

19151930

19401944

19531962

19661978

19891999

20002003

Fig. 2. Seedbank densities recorded from various studies since


1915, indicating the change in the median values (middle point),
the interquartile ranges (box) and the range of values (whiskers). Data for 2000 /2002 are from 200 sites sampled for the
Farm-Scale Evaluations of GMHT crops (Champion et al.
2003), previous data sets are from Brenchley (1918), Brenchley
and Warington 1933, Milton 1943, Champness and Morris
1948, Roberts (1958, 1962), Roberts and Stokes (1966), Roberts
and Neilson 1982), Froud-Williams et al. (1983), Roberts and
Chancellor (1986), Squire et al. (2000), Young et al. (2001).
OIKOS 109:3 (2005)

albeit at reduced density. Species richness might therefore be recoverable by improved land management, such
as: reducing herbicide use (Cussons and Courtney 1994,
Young et al. 2001), altering the timing and frequency of
herbicide application (Champion et al. 2003), and
shifting the balance in favour of spring-sown crops in
the rotation (Squire et al. 2000, Young et al. 2001).
Many of the species whose populations can be
enhanced have an important role in supporting a diverse
arthropod community. Although data on the insect
associations for arable weeds is only available for 60%
of the species listed in Table 1, many are known to
support a wide range of insect taxa. Species that are
thought to be beneficial to higher trophic levels include
members of the Chenopodiacea, Compositae, Leguminosae, Polygonaceae and Umbelliferae (Altierri 1999,
Wilson et al. 1999, Marshall et al. 2003). An understorey
of these types of species could also have positive impacts
on crop productivity and health through reduction in
pest and disease populations. In contrast, some of the
most competitive weeds that are targets of weed control,
such the competitive grass weeds Alopecurus myosuroides and Bromus sterilis, provide a lower quality of
resource and may therefore be less important to invertebrate consumers (Table 1).

Traits for functional diversity in arable communities


Life-history theory predicts that different environments
should select for different optimal patterns in the
allocation of resource between reproductive and vegetative structures (Charnov 1982). An important property
for stability of arable seedbank species populations, in
addition to longevity and persistence of seed in the soil,
is the period available for reproductive growth. A longer
time to flowering, or for reproduction, allows greater
resource accumulation and correspondingly greater allocation to seed production. There is therefore a strong
correlation between plant size and fecundity both
between species and among individuals within a species
(Salisbury 1942, Aarssen and Taylor 1992, Aarssen and
Jordan 2001). In arable fields, the amount of time
available for growth will select for a level of precocity
that allows seed production before death.
The dependence of seed mass on the reproductive
period is shown for several arable species in Fig. 3. Two
of the species, Thlaspi arvense and Anchusa arvensis, are
both annuals / the former highly determinate, usually
maturing before the end of the season, the latter
indeterminate, its reproductive period ended by low
autumn temperature. Despite differences in determinacy,
individual plants form a common relation between
reproductive period and seed mass. A theoretical framework for relating such reproductive phenology to
composition of a community was offered by the
527

Seed mass (g)

100

10

0.1
0

20

40

60

80

100

120

140

Reproductive period (days)

Fig. 3. Variation in the relation between reproductive period


(days from first flowering to maturity or harvest) and seed mass
(grams per plant) from data collected at SCRI (Squire and
Crawford, 1996) for Brassica napus population 1 (open
squares), Brassica napus population 2 (crosses), Brassica rapa
(asterisks), Capsella bursa-pastoris (closed circles), Anchusa
arvensis (closed squares), Thlaspi arvense (open triangles). Data
are averages for individuals sampled within weekly periods
during 1995 (Thlaspi and Anchusa species,), 2001 (Brassica
species), and 2003 (Capsella species).

individual-based model of Bown (2000) and Pachepsky


et al. (2001). Plant types, defined by physiological traits,
interacted over a resource to give communities whose
structure changed over time: early-flowering, short-lived
types were gradually replaced by the more competitive,
later-flowering, longer-lived types. The coexistence of
plant types in the assemblage was explained largely by
this tradeoff between the time to reproduction and
fecundity. The time taken to flower and set viable seeds
depended on an individuals reproductive phenology,
defined by life history and resource uptake traits such as
seed dormancy and longevity, annuality, determinacy
and time- or mass-dependent reproduction (seed mass
per unit plant mass). Traits relating to resource uptake
included maximum growth rate, leaf area, and allocation
and redistribution of resource between plant structures.
Quantitative measures of life-history traits are
rare, with the exception of decay rates in soil which
have been measured for ca 50 species (Roberts 1962),
and growth rates relative to cereals, which are known
for about 20 species (Cussons and Courtney 1994).
Work is therefore required to define, for the main traits
listed here, the range of values that the arable flora
could occupy whilst minimising competition with
crop plants. To achieve this, it is first necessary to
identify the scale at which functional diversity should be
assessed.

Intraspecific variants: the unit of functional diversity


Functional diversity is frequently studied by categorising
species into functional groups with common biological
528

characteristics that determine either their effect on, or


response to, a system process (Lavorel et al. 1997, Wilson
1999, Lavorel and Garnier 2002). These functional
groups are similar to the ecological guilds defined by
Gleason (1939) as, a group of species exploiting
resources in a similar way, and who also suggested
that, proportions of various guilds in a community; can
describe functional organisation of the system without
reference to species whose abundance may vary according to individualistic responses. In most cases, such
classifications have resulted in fewer groups than the
number of genera or species that constitute them. For
example, plant species have been classified as legume,
forb, C3 grass, C4 grass, or woody. Similarly, insects have
been categorised as either herbivores, predators, parasitoids, detritivores or omnivores (Siemann et al. 1998,
Haddad et al. 2001). Weed control in arable fields
commonly targets very broad categories such as grass
weeds or broadleaved weeds, defined by a selective
response of a plant to toxins.
However, grouping at the species-level ignores the
potentially high levels of variability that exist among
populations or individuals within a species and that
might influence important properties of the habitat, such
as net primary production (Epstein et al. 2001). In a
review of 91 species from a wide range of different taxa,
Bolnick et al. (2003) argued that niche differentiation
frequently occurs at an individual level; individual
specialists are those whose niche is narrower than that
of the whole population for reasons other than sex, age
or morphological group. This is supported by data in
Fig. 3, which shows high variation within and between
species across the relation between reproductive period
and fecundity. Thlaspi arvense and Anchusa arvensis
both had relatively short reproductive periods (between 33 and 73 days) compared to Brassica rapa (91
to 116 days). Two populations of Brassica napus showed
much greater variability, overlapping in both seed mass
and reproductive period with individuals of all other
species. Similarly, the variation between Capsella ecotypes was as great as the variation between Anchusa and
Thlaspi. Classification at the species level into functional
response types would therefore fail to account for the
different strategies displayed by individuals under different environmental conditions, particularly in species
that are phenotypically plastic. System function is
determined not by the number of species per se, but by
variation in functional traits that create complementarity between individuals in the way they use resource and
occupy space (Tilman et al. 1997, Loreau 1998, Peterson
et al. 1998, Stevens and Carson 2001, Qin et al. 2003).
Assessment of functional diversity must therefore be
based on measurements of individual variation in
relevant traits such as time to reproduction or the
relation between growth and fecundity.
OIKOS 109:3 (2005)

Individuals can be characterized at both the phenotypic and molecular level, since genes have been identified that regulate patterns of resource allocation and lifehistory tradeoffs (Mitchell-Olds 1996). A suite of
methods is available to study these properties in crop
species for the development of new crop varieties.
Accessions are gathered that represent diverse phenotypes from different climatic and geographic regions.
These are cultured in controlled or standard conditions
and characterized using genetic markers capable of
identifying individuals with desirable phenotypic traits.
Transfer of these common agronomic approaches to
arable weeds would allow the genetic basis for observed
phenotypic variation to be quantified. This is necessary
to determine the heritability of expressed traits, thereby
placing measures of functional diversity in an evolutionary context. However, to achieve this, information is
required on the structure of the genome, the mating
system, the genetic distinctness of individuals (as indicated by genetic marking techniques), and the shift in
trait values that occurs through cross-breeding. The
genetic, physiological and ecological attributes of 66
representative arable species, summarised in Table 1, are
used for illustration below.

Genomic characteristics of arable species


Information for the representative species
There are large gaps in the most basic genomic
information for even some of the commonest taxa
(Table 1). Haploid nuclear DNA content, chromosome
number and ploidy level exist for only 25 species (35%)
of those shown. Of the remaining species, 13 (18%) have
no cytogenetic data recorded at all and the nuclear DNA
content has still not been measured from 33 species
(46%). Even at the level of genera, 25% (18) have data
describing only chromosome number while 7% (5) have
none of the associated cytogenetic data.
The only species for which very detailed genetic
information exists is Arabidopsis thaliana (thale- or
mouse eared-, cress), the accepted model organism for
plant molecular genetics (Meyerowitz 1989). A. thaliana ,
although included in Table 1, has only very occasionally
occurred at high population densities (Roberts 1958) and
is now rare in the in-field arable seedbank, contributing
negligible biomass for higher trophic groups. However,
several related members of the Cruciferae are widespread and important.

Genetic basis of life history traits in Arabidopsis


and related Cruciferae
Aspects of the phenology of A. thaliana have been well
characterised. For instance, the two main environmental
OIKOS 109:3 (2005)

factors that promote flowering in Arabidopsis are long


days and exposure to low temperatures (Blazquez et al.
2001). By crossing early and late flowering Arabidopsis
varieties, Sanda et al. (1997) identified the chromosomal
locations of genes for shoot development and time to
flowering (Lagercrantz et al. 1996, Osborn et al. 1997,
Michaels and Amasino 2000, Schmidt 2002). At the top
of A. thaliana chromosome 4, the homologous QTLs
FRI and LD have also been found (Napp-Zinn 1985,
Osborn et al. 1997, Sanda et al. 1997). FRI and FLC
interact epistatically to control flowering time, such that
late-flowering alleles at both loci are needed to confer
late flowering (Koornneef et al. 1994, Lee et al. 1994). In
addition, at the top of chromosome 5 the EMF1 locus
possess genes essential for shoot development and this
locus may encode a floral inhibitor (Sung et al. 1992,
Yang et al. 1995).
While genomic data from Arabidopsis might be
duplicated in distantly related dicotyledonous species
(Rossberg et al. 2001, Horvarth 2003) the closest
correspondence should be among other Cruciferous
species. Of those in the UK, the most widespread and
common are Capsella sp. (most commonly, C. bursapastoris) , Sinapis arvensis, feral Brassica napus and B.
rapa and Sysimbrium officinale. Aspects of the genetic
content and organisation found in Arabidopsis are
mimicked in other species of the Cruciferae, including
members of the Capsella complex (Kowalski et al. 1994,
Lagercrantz and Lydiate 1996, Lagercrantz et al. 1996,
Schmidt 1998, Acarkan et al. 2000, Arabidopsis Genome
Initiative 2000). The small genome of Arabidopsis
(0.2 pgs of DNA representing 164 Mbps in 5 chromosomes per haploid genome, 2n/2x /10; Schmidt 1998)
is similar to that of C. rubella that has 170 Mbps on
8 chromosomes (Bennett and Smith 1976). Furthermore,
detailed analysis of 60 kbp in A. thaliana and C. rubella
showed virtually complete conservation of gene-repertoire, -order and orientation with 90% identity for exon
sequences (Acarkan et al. 2000). In addition, a comparison of genes controlling vernalisation responsive flowering time of Brassica napus and B. rapa has identified two
quantitative trait loci in each that may correspond to the
FLC and FRI genes of Arabidopsis (Osborn et al. 1997,
Kole et al. 2001).
However, the genetic basis of life history traits may
differ between species, even those of the same genus. For
example, flowering time variability in Brassica nigra is
associated with the gene Constans Like1 , not FLC/FRI
sterberg et al. 2002). This emphasises that
(Kruskopf O
while similarities may be exploited to identify functionally different types, the genetic basis of key life history
traits is likely to vary between species. Consequently,
there is greater utility in being able to diagnose the
presence of ecological traits using specific and robust
molecular marker technologies that can be applied
across different plant communities (Sunnucks 2000),
529

rather than attempting to discern the exact genetic


basis of complex and interacting key life history traits.
For example, SSRs designed to distinguish different
functional types among one brassicaceous species
may be used on others (Kresovich et al. 1995, Clauss
et al. 2002). It is possible that existing genetic sequence information tools can be exploited to quickly
facilitate molecular diagnostics for diverse Capsella
ecotypes.
Relying on molecular markers instead of a detailed
molecular dissection to identify key traits is also
supported by other examples, where small genetic
differences in phenotype that have potentially large
ecological consequences would otherwise be arduous to
localise. A comparison of flowering periods for two
Brassica species (Fig. 3) showed lower variation in the
time from first flowering to maturity in B. rapa
compared to B. napus. Though well quantified genetically compared to many other species, B. napus and
B. rapa are both recent feral weeds, and only the former
has become widespread and abundant. They would be
valuable subjects for study of the evolution of weeds
from crop plants, but are not yet certain or longstanding members of the UKs weed flora. Due to its
synteny with Arabidopsis, and its ubiquity and importance in fields (Table 1) and other disturbed habitats,
Capsella more closely fits the requirements of a species
suitable for testing the proposed trait based approach to
understanding functional diversity.

Known variation in Capsella


The genus Capsella has been noted for phenotypic
variation, having been divided variously into 5, 6, 8,
16 /12 and 200 different species, sub-species, varieties,
classes or micro-species (Jordan 1864, Hopkirk 1869,
Mott 1885, Almquist 1921, 1923). These studies often
assessed individuals that were cultured in non-standard
growth conditions, so failed to distinguish heritable
differences between individuals. However, this limitation
was originally addressed by growing the plant material
for comparison under standard conditions (Shull 1909).
This identified distinct groups based mainly upon leafshape and capsule size. The genetic basis of these
differences was confirmed by showing that the phenotypic characters of each type were maintained over
successive generations, and that the progeny of the
cross-fertilised parents segregated in a Mendelian fashion. In an impressive display of plant systematic analysis,
Shull (1909, 1914, 1918, 1929) measured phenotypic
traits of around half a million individuals from approximately four thousand pedigreed families, and established
that Capsella comprised what he chose to defined as two
species and ten sub-species.
530

More recent classifications recognise three Capsella


species (Neuffer and Eschner 1995). Two diploid species,
C. grandiflora (Fauche and Chamb.) and C. rubella
(both 2n/2x /16), are found predominantly in Mediterranean clines (Love and Love 1956, Davis 1965,
Clapham et al. 1987, Aksoy 1996, 1999, Aksoy et al.
1998) while C. bursa-pastoris is tetraploid (2n/4x/32),
distributed throughout temperate regions worldwide
(Almquist 1929, Shull 1929, Svensson 1983, Neuffer
and Eschner 1995, Hurka and Neuffer 1997). In
semi-natural habitats, Capsella species occur in mixed
populations of C. rubella and C.bursa-pastoris (Steinmayer et al. 1985, Neuffer 1989) and in the UK,
C. bursa-pastoris is abundant in the seedbank of arable
land. From analysis of aspartate aminotransferase isoenzymes, C. bursa-pastoris is predominantly (90 to 98%)
self-fertilising and C. rubella is highly inbred (Shull 1929).
In addition, both species possess only small nectaries
and there is little likelihood of inter-specific hybrids:
C. rubella /C. bursa-pastoris triploid hybrids (Capsella /
gracilis ) are rare and usually sterile due to the abortion of the siliculae (Keble-Martin 1991). Consequently,
the twelve taxa that Schull distinguished span two
sexually isolated species: four ecotypes of the diploid
C. rubella and eight of the tetraploid C. bursa-pastoris.
The species- or within-species variants have commonly
been distinguished by characters of the petals, seed pods
or leaf shape (Clapham et al. 1987, Tutin et al. 1993,
Neuffer and Eschner 1995). However, little of this data
pertains to functional traits mediating the uptake of
resource or its transmission to the food web. Experimental evidence exists nevertheless to indicate that the
length of time between seed germination and flowering:
(i) differs between individuals within a species; (ii) is
heritable; and therefore, (iii) that such differences have a
genetic basis (Svensson et al. 1983, Neuffer 1989).
Individual differences in flowering time and architecture
also relate to ploidy level. The tetraploid of the genus
flowers after 30 /60 days, the diploid after 60 /100 days
resulting in taller plants having greater branching of the
inflorescence-bearing stem (Neuffer and Eschner 1995,
Aksoy et al. 1999). Crossing ecotypes of Capsella from
different geographical regions established that three
major quantitative trait loci account for time to flowering and are associated with rosette leaf number (Linde
et al. 2001). Rosette diameter is an indicator of resource
capturing ability and also appears to be negatively
correlated with the time from germination to flowering,
later flowering plants possessing markedly smaller
rosettes (Neuffer and Bartelheim 1989, Neuffer and
Eschner 1995).
No extensive in-field habitat surveys of Capsella have
been made in recent times, and the assumption that most
individuals are C. bursa-pastoris may not be true for all
populations. This lack of information is compounded by
scant detail regarding how these poorly characterised
OIKOS 109:3 (2005)

populations interact with the physical environment, field


management or type of crop. Capsella has nevertheless
many suitable properties as a tool for developing
definitions of the minimum unit of diversity, notably
the genetically distinct types that appear to differ slightly
but systematically in relevant functional traits and
tradeoffs.

Conclusions
The important traits for survival of arable plants, given
the high levels of disturbance within fields, are those that
relate to germination, flowering time, seed production
and seedbank persistence. The spread of these traits
among individuals in an arable community will determine the level of functional diversity and the amount of
different resource types that are available for consumers.
The abundance and diversity of arable weeds may be
enhanced with little impact on crop yield if field
management practices can be designed that select for
weeds with particular characteristics: high resource
acquisition and utilisation efficiency, low nutrient and
light requirements, a spread of germination and flowering periods within the window between disturbance
events, and high resource quality for invertebrate and
other consumers. If within-field communities with these
characteristics are to be achieved, detailed information is
required on the ecological, physiological and genetic
traits of arable weeds. However, there are major gaps in
current knowledge for even the most common species.
Even less is known about the degree of variation within
these species that contributes to overall levels of functional diversity. We therefore propose an individual,
trait-based approach to define functional diversity in
arable systems using, in the first instance, Capsella as the
target species. Systematic investigation of phenotypic
and genotypic variation at the individual level is now
required to understand the mechanisms underlying the
maintenance of diversity in productive arable systems.
This can be achieved through phenotypic measurements
of individual plants, exhaustively sampled from the
seedbank at a range geographic locations with varying
management histories, and grown ex situ in a controlled
environment from seed germination to death (Gaudet
and Keddy 1988). These measurements should be
associated with genetic characterisation of individuals
of known phenotypes using molecular markers for key
life history strategies and trade-offs. If successful, it will
be necessary to extend this approach from Capsella to
other species that collectively account for most of the
primary productivity of arable ecosystems. Quantifying
functional diversity according to variation in traits
between individual plants will provide the basis for
future assessment of the impact of biodiversity on
system functions such as resilience and productivity.
OIKOS 109:3 (2005)

Acknowledgements / This work is funded by the Scottish


Executive Environment and Rural Affairs Department under
projects SCR/571 and SCR/568.

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