Nectar and flower production in Vicia faba L. (field bean) at ambient and elevated carbon dioxide

Patron: Her Majesty The Queen Rothamsted Research Harpenden, Herts, AL5 2JQ

Telephone: +44 (0)1582 763133 Web: http://www.rothamsted.ac.uk/

Rothamsted Research is a Company Limited by Guarantee Registered Office: as above. Registered in England No. 2393175. Registered Charity No. 802038. VAT No. 197 4201 51. Founded in 1843 by John Bennet Lawes.

Rothamsted Repository Download

A - Papers appearing in refereed journals

Osborne, J. L., Awmack, C. S., Clark, S. J., Williams, I. H. and Mills, V. C.

1997. Nectar and flower production in Vicia faba L. (field bean) at

ambient and elevated carbon dioxide. Apidologie. 28, pp. 43-55.

The publisher's version can be accessed at:

•

https://dx.doi.org/10.1051/apido:19970105

The output can be accessed at:

https://repository.rothamsted.ac.uk/item/8797x/nectar-and-flower-production-in-vicia-faba-l-field-bean-at-ambient-and-elevated-carbon-dioxide

.

© Please contact [email protected] for copyright queries.

Original

article

Nectar

and

flower

_production

in

_{Vicia faba}

L

(field

bean)

at

ambient

and elevated carbon

dioxide

JL

Osborne

1

CS Awmack

SJ

Clark

IH

Williams

VC

Mills

1

Department

of Entomology and Nematology, IACR-Rothamsted;

2

Department

of Statistics,

IACR-Rothamsted,

Harpenden, Hertfordshire

AL5 _2JQ;

3

NERC

_Centre,for

_Population

_{Biology, Imperial}

College, Silwood Park, Ascot,

Berkshire SL5 7PY, UK

(Received 23

_July

1996;

accepted

31 October 1996)

Summary —

Atmospheric

CO

2

has been

_predicted

to double

_by

_{the year 2100. Elevated}

_CO

₂

causes an increase in

_{photosynthetic}

rate and extra assimilate is allocated to

_plant

_growth,

_{seed and fruit}

pro-duction. Increased investment in flowers may have

implications

for

_pollination

in

_{entomophilous plants.}

Floral nectar

_standing

crop, flower

production

and

_longevity

were examined in

_{Vicia faba,}

field

bean, at ambient and elevated

_CO

₂

_.

_Nectar

_standing

crop did not differ

_{significantly}

between treat-ments but

_plants

_grown at elevated

_CO

₂

_produced

_{approximately}

25% more _{flowers per}

_plant

and these lived 17%

_longer

_{than those grown} at ambient

_CO

₂

_.

A

_plant

grown at elevated

_CO

₂

_{may thus} pro-duce more nectar in total and,

together

with its increased floral

_display,

may be more attractive to

pol-linators, but

_pollen

flow will not

_necessarily

be

_improved.

Vicia faba

/ carbon dioxide / climate

_change

/ nectar / flower

_longevity

INTRODUCTION

The concentration of

_CO

₂

in the

_atmosphere

has been

_predicted

to

_{approximately}

dou-ble from the current 350

_μL·L

_-1

to

700 μL·L

-1

by

2100

_{(Pearman, 1988).}

Ele-vated

_CO

₂

affects the metabolism and

growth

of

_plants

_(Cure

and

Acock, 1986;

Bazzaz,

1990)

and could have

_profound

effects on _crop

production

_{(Parry, 1992).}

Photosynthetic

rate of

_plants

_grown at

elevated

_CO

₂

₍₇₀₀

_μL·L

_-1

₎

can increase

_by

up to 40% relative to those _grown at

ambi-ent

_CO

₂

₍₃₅₀

μL·L

-1

),

_leading

to increased

carbon fixation in most

_C

₃

_plant

_species

(Cure

and

_{Acock, 1986).}

The extra carbon

*

Correspondence

and

_reprints

fixed is allocated to

_vegetative

_growth

(Baz-zaz,

1990; Pitelka, 1994)

and to

_reproduction

(Kimball, 1986; Pitelka, 1994).

Beneficial effects of extra

_CO

₂

on the seed and/or fruit

yields

of

_glasshouse

_crops have been under

investigation

for at least 100 _years

_(Wittwer

and

_{Robb, 1964)}

and elevated

_CO

₂

has been

used in

_glasshouses

since the 1960s to

improve yields

of _{crops such} as tomato,

let-tuce and cucumber

_(Wittwer

and

Robb,

1964)

and

_production

_{of flower crops}

(Goldsberry,

1986).

Kimball (1986)

reviews the effects of

_CO

₂

on the

_yields

of field

crops such as

_wheat,

cotton and

_soybean.

Though

increased fruit and seed

_yields

have been

_widely

demonstrated,

there have

been fewer studies on how elevated

_CO

₂

might

affect the floral

_biology

of a

_plant

species,

for

_example

flower

_production,

flower

_longevity

and the rewards available

to

_visiting

insects. For

_{insect-pollinated}

species,

these factors may affect

reproduc-tive success of the

_{plant by altering}

insect visitation rates and

_consequently

_pollen

flow and the effectiveness of

_pollination.

The

possibility

that climate

_change

could affect

plants’ reproductive

success is of economic

importance.

How is elevated

_CO

₂

_likely

to affect

flo-ral characters of a

_plant?

Flower initiation

(production)

and maintenance

_(flower

longevity

and reward

_production)

are

_costly

to a

_plant

_(reviewed

_by

Ashman and

Schoen,

1996)

and _{may be} limited

_by

resources. In

such cases, increased resource

_{availability,}

for

_example

extra carbon fixed at elevated

CO

2

,

would allow added investment in

either the initiation of flowers or the

main-tenance of flowers or

both,

_leading

to more

longer-lived

flowers with extra rewards such

as nectar. No studies were found

_examining

the effects of elevated

_CO

₂

on nectar

pro-duction in any

species.

Floral

_display

_(the

number of flowers

open at _{any one}

_time)

is determined

_by

flower

_number,

floral

_longevity

and the

period

for which the

_plant

is

_flowering

and

in this

_respect

_plant

_species

_vary in their

response to elevated

_CO

₂

_(Goldsberry,

1986).

In

_general,

elevated

_CO

₂

leads to

increased initiation and retention of

flow-ers

_(Acock

and

_{Pasternak, 1986; Kimball,}

1986)

and earlier initiation of

_flowering

(Garbutt

and

_{Bazzazz, 1984);}

these effects

have been

_reported

in

_carnations,

roses and

several other flower _crops

_(Goldsberry,

1986; Kimball, 1986),

and in tomato

_plants

(Wittwer and Robb, 1964;

Hicklenton and

Jolliffe, 1978).

In

wheat,

rice _{and pea,}

tiller-ing

is increased

_(Acock

and

Pasternak,

1986).

Garbutt and Bazzazz

₍₁₉₈₄₎

found

that

_populations

of a wild

_plant

_species,

Phlox drummondii

_Hooker,

_generally

flow-ered earlier and

_produced

twice as _many,

longer-lived

flowers at elevated

_CO

₂

than

at ambient

_CO

₂

_.

This

_study

considers the effect of

ele-vated

_CO

₂

on nectar

_production

_(volume,

concentration and _sugar

_weight),

_flower

pro-duction,

longevity

and bloom

_period

(phe-nology)

in

_{Vicia faba,}

the field

bean,

which benefits from bee

_pollination

(Stoddard

and

Bond, 1987).

MATERIALS AND METHODS

Sixteen _{V faba} (cv Sutton)

plants

were _grown

from seed in each of two bee-free rooms in the

Envirocon®

_facility

at Rothamsted (Lawlor et

al, 1993). One room had a

_CO

₂

concentration of 350

_μL·L

_-1

and the other 700

_μL·L

_-1

_.

All other conditions were similar:

_plants

were _grown in individual 1 L _pots in _{Terra-Green® (Oil-Dri,}

Colorado) and each was

_given

_{1.6 g slow release} fertiliser (Osmacote

mini®,

Sierra, UK). Seeds were _grown at 18 °C and

_exposed

to a

_light

regime

of 16 h

_light

₍₀₂ 00-18 00 _hours) and 8 h dark. _Every 7

_days

the

_plants

and the _CO2 con-ditions were

_swapped

between rooms to

min-imise any external effects

owing

to rooms or

positions

within rooms.

_{Flowering began}

when

plants

were 4-5 weeks old and

_flowering

_stages

Nectar

_standing

_crop

Although

nectar secretion rate

_might

have been the most

_appropriate

measure of nectar

produc-tion

_(emptying

a flower of nectar,

_leaving

the

flower to accumulate nectar

_again

and then

resampling

after a set

_period

of time), destruc-tive

_sampling

of flowers was _{necessary for} accu-rate measurement of nectar content so flowers

could not be

_sampled

twice. The measurement taken was nectar

_standing

crop, but the flowers were not visited

_by

bees so this

_approximates

to nectar secretion over the flower’s life, minus any nectar that is reabsorbed

_by

the flower.

Nectar

_standing

crop of flowers in different

CO

2

conditions was determined

_{by sampling}

flowers from the first

_eight

nodes on the

_primary

stems of six of the

_plants

in each treatment room once a

_day

between 15 30 and 17 30 hours. The

sampling period

lasted 28

_days.

The nodes _(1-8) and the

_position

of the first

_eight

flowers on the raceme at each node formed the rows and columns of an 8 x 8 Latin

_Square.

The

_following

procedure

was used to

_investigate

differences in nectar

_standing

_{crop with respect} to _{flower age} and

_position

on the

_plant.

When a flower reached at least _stage 1

_(unfurling

bud; table I), it was

assigned

a

_{sampling day}

_(to obtain a

_given

_age at

sampling) according

to a randomised Latin

Square

and the actual _stage at this time was

recorded. A different Latin

_Square

was used for

each

_plant.

The corolla was marked with a _pen so

that on the

_{following day}

it was _easy to

distin-guish

which flowers were

_{newly opened. Eight}

different flower ages, from 1 to 8

_days,

were obtained in this way on each node; in the field,

flowers can remain

_receptive

_{for up} to 6

_days

after anthesis _{(Stoddard, 1986).} Some nodes

produced

fewer than

_eight

flowers and some

flowers aborted, so _many

_missing

values resulted,

but

_despite

this a

_large

number of flowers (441)

were

_sampled.

The flower to be

_sampled

for nectar was removed from the

_plant

and its

_{developmental}

stage was noted (table I). The standard

_petal

was

removed

_according

to the

_technique

of Davis and

Gunning

( 1993) and the nectar from around the nectaries withdrawn into a 0.5

_{μL, 1 μL}

or 5

_μL

disposable microcapillary

tube

_(depending

on the volume _present). Vicia _faba nectaries are

described

_by

Davis et al ₍₁₉₈₈₎ and illustrated in Davis and

_Gunning

_(1992). The

_length

of the nec-tar column in the tube was measured and the

vol-ume of nectar

_(μL

_per flower) calculated. The concentration (% =

was estimated

_using

a

_pocket

refractometer

(Bellingham

and

_Stanley

Ltd,

Tunbridge

Wells)

and sugar

weight (mg

sugar per flower) calcu-lated from the volume and concentration

(Pr&jadnr;s-Jones and Corbet, 1991).

Although

the refrac-tometer was modified to take low volumes, nectar

concentration, and hence sugar

weight,

could not be determined if the volume was less than 0.05

_μL.

Flower

_longevity

and

_production

Bees are most

_likely

to visit

_fully

_{open flowers} in _stages 4-6 as

_they

are the easiest to

_manipulate

and

_probably

the most attractive and

_rewarding,

but all flowers

_(stages

1-7) may

help

to attract

bees from a distance. The

_longevity

_{of every} flower on alternate nodes of the

_remaining

ten

plants

in each

_CO

₂

treatment was determined. When

_{flowering began}

₍₂₃

_January),

the

_plants

were labelled and, on each afternoon, the buds in _stage 0 or _stage I were marked on the

_sepals.

The

_{developmental}

_stage reached

_by

each marked flower was recorded

_daily

(at some time between 16 00 and 18 00 _hours) until the flower had with-ered

_(stage

_8). For odd-numbered

_plants,

flowers

on nodes _{1, 3, 5,} etc, were observed and for the

even-numbered

_plants,

flowers on nodes _{2, 4, 6,}

etc, were observed. Flowers were followed until 25

_February

(not the end

_{of flowering,}

but

_plants

were not watered on 24

_February

and

_drought

is known to induce flower shed; Gates et al, 1983).

The total number of flowers

_{produced by}

each

plant

was recorded until 5 March when all the

plants

had

_finally

finished

_flowering.

Floral

_display

On each

_day

from 24

_January

to 25

_February,

the total number of flowers in stages 1-7 (inclu-sive) and _stages 4-6 (inclusive) on each

_plant

were counted.

Methods of

_analysis

Nectar

_standing

_crop

For nectar volume per flower, data for the 441

ambient

_CO

₂

and 100 at elevated

_CO

₂

_),

concen-tration and sugar

weight

per flower could not be measured so these flowers were omitted from the

_analyses

of these variables (n = 217 for each

analysis).

Data were transformed if necessary

(table II),

analyses

of variance tables were

con-structed

_{using regression techniques,}

and treat-ment differences were tested with F-tests

(table II).

Flower

_longevity

_{and production}

Analyses

of variance _{(table II)} were

_computed,

using regression techniques,

to assess the effect

of CO

2

on (i) the number

of days

that each flower spent in _stages 1-7 (inclusive) and (ii) the

num-ber of

_days

that each flower _spent in _stages 4-6

(inclusive). Residual

_{plots suggested}

transfor-mation of the data was _{unnecessary. Some} flow-ers were missed

_during

examination but their

stage could often be inferred from the records

on the

_previous

and

_{following day.}

The total numbers of flowers per

plant

were transformed to natural

_logarithms,

and treatment

means were

_{compared using}

a

_two-sample

t-test.

Floral

_display

The counts of flowers in stages 1-7 and 4-6 form sets of

_repeated

measurements, one set for each of the 20

_plants.

Data of this kind can be con-sidered as _analogous to those

_arising

from a

split-plot design

with

_{plants equivalent}

to whole

_plots

and time

_{periods equivalent}

to

_subplots.

How-ever,

adjacent

time

_periods

may be more

_highly

correlated than those further _apart. To allow for this the

_degrees

of freedom in the

_subplot

stratum of the

_{resulting analysis}

of variance tables were

adjusted by multiplying

them

_by

ϵ (Greenhouse

and Geisser, 1959), a measure of the correlation between successive time

_periods,

before

_testing

treatment differences with F-tests. Before

anal-ysis, missing

values were estimated

_given

the observed level of

_{ante-dependence}

in the data.

RESULTS

Nectar

_standing

_crop

Flowers contained 0-3.44

_μL

nectar _per

(equiv-alent to 0-1.01

_mg

_{sugar per}

_flower).

There

was no

_significant

effect of

_CO

₂

on

_weight

of _{sugar per flower}

_{(table II);}

and the

inter-action between

_CO

₂

and flower _age was

only weakly significant.

However,

there

was a

_significant

effect of flower age on

sugar

weight

per flower. New flowers and

old flowers contained less _{sugar per} flower

than

_3-5-day

old flowers

_(fig

_{1). Flowers}

in _stages 1-7 contained some _nectar,

_though

there was little in

_{newly opening}

flowers

and most in

_fully

_open flowers

_{(stages 4-6)}

(fig

2).

Carbon dioxide had no

_significant

effect on nectar concentration or volume whilst

the interaction between

_CO

₂

and _age was not

_significant

for concentration and was

only weakly significant

for nectar volume

(table II).

Flower age,

however,

had a

_highly

significant

effect on both nectar

concentra-tion and volume. The trends for nectar

con-centration and volume per flower with age

were similar to those for _{sugar weight per} flower

_(fig

1).

Flower

_longevity

and

_production

There was a

_significant

difference in flower

longevity (days

spent

in _stages

_1-7)

between

CO

2

treatments, and also in the number of

days

each flower remained

_fully

_open

(stages 4—6) (table II).

Flowers lived

_longer

and remained

_fully

open

longer

at elevated

CO

2

(table II).

Plants _grown at elevated

_CO

₂

_produced

significantly

more flowers

_{[ 156.8 (± 9.2)}

flowers _per

_plant]

than

those _grown at

ambi-ent

_CO

₂

_{[ 124.8 (± 13.1)}

_flowers

_per

_plant].

These means _may be underestimates as the

plants

were water-stressed towards the end

of

_flowering.

Floral

_display

and bloom

_period

of flowers in _stages 1-7 _per

_plant

_per

_day

or for those in

_stages

_{4-6 per}

_plant

_per

_day

(P >

0.05).

Over the whole

_flowering

period,

there were

_always

more flowers on

plants

at elevated

_CO

₂

than on

_plants

at

ambient

_CO

₂

_(fig

_3a;

_F

_1,18

=

_13.47;

P <

0.05).

There were also

_{more fully}

_open flowers

_(stages

_4-6)

_per

_plant

_per

_day

(fig

3b;

_F

_1,

18=

24.32;

P <

0.01).

Time

of _{flowers per}

_plant

_per

_day

_(F

_3,57

₌

39.94;

P <

_0.01)

and on the number

of fully

_open

flowers _per

_plant

_{per day}

_(F

_4,74

=

28.73;

P <

_0.01).

Plants at elevated

_CO

₂

started

flowering

earlier

_(by

2 or 3

_days)

_{and many}

finished later than those at ambient

_CO

₂

_.

DISCUSSION

Nectar

_standing

_{crop per} flower was

_highly

variable,

with many flowers

containing

no

extractable nectar; volumes recorded were

similar to those obtained

_by

others

(Stod-dard and

_Bond,

1987; Davis et

al, 1988;

Free,

1993).

Fully

open flowers contained the most nectar and there was a

_strong

rela-tionship

with flower _age. The accumulated

nectar

_approximates

to the nectar secreted

_by

the flower and since the flowers were not

visited

_by

insects,

the decrease _{in sugar}

con-tent _{with flower age suggests}

_reabsorption

is

taking

place

(Búrquez

and

_{Corbet, 1991).}

Surprisingly,

elevated

_CO

₂

had no

signifi-cant effect on mean nectar

_standing

_crop

per flower.

Individual flowers _grown at elevated

_CO

₂

lasted for about

_{1 day longer}

than those at

ambient

_CO

₂

₍₇

_days

instead of

_6).

In both

treatments,

the

flowers took

_{approximately}

I

_day

to open, but

they

remained

_fully

_open for 4

_days

at elevated

_CO

₂

and 3

_days

at

ambient

_CO

₂

_,

_making

each flower at

ele-vated

_CO

₂

_potentially

available for bees’ visits for 15-25%

_longer

than _{flowers grown}

at ambient

_CO

₂

_.

In both treatments, the

flowers took about 2

_days

to wither

_fully.

The measurements for floral

_longevity

in

this

_experiment

are

_comparable

with those of

Bond et al

₍₁₉₈₀₎

who note

that,

in the

field,

the standard

_petal

of a

_{V faba}

flower

col-lapses (stage

7)

3-5

_days

after

_opening.

Our estimates of flower

_production

are

higher

than those

_{previously reported}

(50-80

flowers _per

_plant;

Free,

1993).

Most V faba

cultivars are indeterminate

_(Gates

et

_al,

1983;

though

see

Stoddard, 1993),

and in

the absence of insect visitation

_vegetative

growth

and

_flowering

continue for

_longer,

but even so, the greater number of flowers

on

_{plants grown}

at elevated

_CO

₂

_(25%

more)

and the

_prolonged

_flowering

_period

suggest that at least some extra assimilate

is used to increase initiation and

mainte-nance of flowers.

Individual flowers did not contain more nectar _{when grown} in elevated rather than ambient

_CO

₂

_,

but if one assumes that the

active nectar secretion

_period

is when the

flower is

_fully

_open

_(stages

4&mdash;6:

_fig

2)

then,

because the flowers at elevated

_CO

₂

were

fully open

for

_longer,

one would _expect them to accumulate more nectar

_by

the time

_they

started to

wither,

even if secretion rates were

similar for both treatments. Mean nectar

standing

crop in

5-day

old flowers was still

increasing

in elevated

_CO

₂

_,

but had

_begun

to

decline for flowers in ambient

_CO

₂

_(fig

1).

On this

_day,

flowers in elevated

_CO

₂

are

still

_likely

to be

_fully

_open

_(stage

₆₎

and

secreting

nectar, while those at ambient

_CO

₂

are

_beginning

to wither and

_presumably

to

reabsorb nectar

_(fig

_2).

After the 5th

_day,

flowers at elevated

_CO

₂

also

_begin

to wither.

At elevated

_CO

₂

the

_period

of nectar

secre-tion lasts

_{longer but}

it seems to be balanced

by

increased

_reabsorption

_(when

the flowers

begin

to

_wither)

since the overall

_standing

crop is similar between treatments.

On any one

day

there is

_likely

to be a

larger

floral

_display

on a

_plant

_{grown in} ele-vated rather than ambient

_CO

₂

_(fig

₃₎

so

that,

in a future elevated

_CO

₂

environment,

the rewards available to bees from the

_plants

will be _greater than in current

_conditions,

though

how this will affect flower visita-tion rate is uncertain.

At elevated

_CO

₂

_{V faba}

flowers do not secrete more nectar

_{individually:}

increased

nectar may not

_{necessarily improve pollen}

flow,

since increased _{rewards may lead} to

longer-lasting

insect visits

_{(Kato, 1988).}

This may enhance

pollen

removal or

_deposition

on the individual flower but overall

reduc-ing pollen

flow. Nor would increased nectar

levels

_help

in the attraction of

_pollinators

from a distance.

_{Vicia faba}

_{does, however,}

invest extra assimilate in initiation and

main-tenance of flowers at elevated

_CO

₂

_,

increas-ing

the floral

_display.

How

_might

these

changes

influence insect visitation? Harder

and Barrett

_{( 1996)}

_suggest that floral

dis-play

acts

_{antagonistically}

in the roles of

pol-linator attraction and

_{pollen dispersal.}

When

floral

_display

is

_increased,

either

_by

an

increase in total flower

_production,

an

increase in flower

_longevity,

or both, more

pollinators

are

_likely

to be attracted to the

plant.

This could reduce the number of

pol-linators

_visiting

other

_{plant species}

in the

area which do not have the same _response

to

_CO

₂

_(Garbutt

and

Bazzazz, 1984)

and

thereby

increase

_{V faba’s}

share of

_pollinators.

But in many cases,

_larger

floral

_displays

result in more

_pollinator

visits per

_plant,

but

fewer visits _per flower

_(Harder

and

Barrett,

1996;

Snow et

al,

1996)

and increased levels of

_{self-pollination,}

_{particularly geitonogamy}

(Handel,

1983;

Harder and

_Barrett,

1995,

1996).

Pollen flow per flower can

some-times, therefore,

be reduced

_{by increasing}

floral

_display

_(Harder

and Barrett,

1995).

This is

_likely

to have severe _{consequences in}

species

where

_{inbreeding depression}

is pro-nounced.

_{Vicia faba}

can

_produce

viable

seeds from

_{geitonogamy although}

cross-pol-lination

_produces

better seed.

Thus,

over the

_{flowering period,}

a

_{V faba}

plant

growing

at elevated

_CO

₂

is

_likely

to

produce

more nectar in total than one at

ambient

_CO

₂

_which,

combined with its

increased floral

_{display, may make}

it more

attractive to

_pollinators

_(in

relation to other

plants

which do not

_respond

this

_way)

but

may not

_necessarily

enhance

_pollen

flow.

The increased floral

_display

will also

increase the resources available to _the

pop-ulations of bees and other insects

_feeding

on these flowers.

Carbon dioxide _{enhancement may also}

affect the bees

_directly

(Nicolas

and Sillans,

1989).

Short bursts of _pure

_CO

₂

_,

used to

anaesthetise

_honey

_bees,

have been shown to

alter

_{subsequent foraging}

behaviour

(Rib-bands, 1950;

Ebadi et

_{al, 1980)}

and

hor-monal

_activity

_(Bühler

et

_al,

₁₉₈₃₎

but it is

possible

that even small

_changes

in

atmo-spheric

_CO

₂

may alter the bees’

behaviour,

though

to lesser extent.

_Receptors

on

_honey

bees’ antennae

_respond

to

_{tiny changes}

in

CO

2

concentration

_{(Lacher, 1967;}

_Stange

and

_{Diesendorf, 1973)}

and when

_CO

₂

con-centrations rise in the hive

_(for

_example

from 1 to 3%

_CO

₂

in

_atmosphere),

bees alter

their entrance

_fanning

behaviour to

_improve

hive ventilation

_(Seeley,

1974).

Such small

changes

in

_CO

₂

_{may also alter their} moti-vation to

_forage

_(Bühler

et

_al,

₁₉₈₃₎

which

may in turn affect

_pollination.

In

glasshouses,

there is no noticeable effect on

bumble bee behaviour or

colony

develop-ment when

_CO

₂

levels are doubled to pro-mote fruit set

(van Doorn,

personal

com-munication),

although

there may be effects

on

_colony

_development

when

_CO

₂

levels are 20 or 30 times

_ambient,

near the

_CO

₂

distribution lines. Such effects are

_currently

being investigated

(van

Doorn,

personal

communication)

and _{may have}

_implications

for

_pollination

levels in a future

_CO

₂

_-rich

environment.

The effects of increased

_CO

₂

concentra-tions on the floral

_biology

of

_plants

are

_likely

to have

_important

_{consequences,} whether

good

or

_bad,

on

_{insect-pollinated}

_systems.

To

_investigate

these _consequences

further,

studies

_{of plants}

in the _presence

_of

pollina-tors at elevated

_CO

₂

are

_required.

ACKNOWLEDGMENTS

Thanks are due to C Williams for

_developing

the flower _stage

_key.

IACR Rothamsted receives

grant-aided

support from the

_{Biotechnology}

and

Résumé &mdash; Production de nectar et de fleurs chez la

_féverole,

Vicia

_{faba L,}

au

taux de

_CO

₂

ambiant et à un taux

_plus

élevé. On a

_prédit

le doublement du

_CO

₂

atmosphérique

d’ici l’an 2100. Une teneur

élevée en

_CO

₂

_provoque une

_augmentation

de la

_{photosynthèse}

chez la

_plupart

des

plantes

étudiées et une _grosse

_partie

du

car-bone

_{supplémentaire}

fixé sert à la croissance

et à la

_reproduction

de la

_plante.

Les

rende-ments en

_graines

ou en fruits sont souvent accrus en

_présence

d’un taux élevé de

_CO

₂

_,

mais la

_biologie

florale _peut être elle aussi

affectée,

ce

_qui

a des

_{conséquences}

_pour la

pollinisation

des

_{plantes entomophiles.}

Chez

certaines

_espèces

la

_production

de fleurs et

leur

_longévité

sont accrues sous

_CO

₂

_élevé,

mais nous n’avons trouvé aucune étude por-tant sur la

_production

de nectar. Nous avons

étudié chez la féverole la

_production

de nec-tar floral

(volume,

concentration et

_poids

des

_{sucres/fleur),}

la

_production

de fleurs et

leur

_longévité.

Les

_plantes

ont été cultivées dans deux

_pièces

_dépourvues

_{d’abeilles,}

l’une avec un taux de

_CO

₂

ambiant

(350

&mu;L/L),

l’autre avec un taux

_plus

élevé

(700

&mu;L/L).

Des fleurs

_d’âge

connu

_(1-8

jours)

ont été

_prévelées,

leur stade de

déve-loppement

noté

_{(tableau I)}

et leur nectar

extrait à l’aide de

_{microcapillaires}

de

0,5

&mu;L,

1

_&mu;L

et 5

_&mu;L.

Le volume de nectar a été

obtenu en mesurant la hauteur de la colonne de nectar dans le tube

_{(&mu;L/fleur).}

La

concen-tration du nectar

_(%;

_{g saccharose pour}

100 g de

solution)

a été déterminée à l’aide

d’un réfractomètre de

_poche.

Le

_poids

des

sucres dans le nectar

_(mg/fleur)

a été

cal-culé à

_partir

du volume et de la concentration

(Pr&jadnr;s-Jones

et

_{Corbet, 1991). La}

_longévité

de

_chaque

fleur sur les noeuds alternés de

dix

_plantes

_(non

_{échantillonnées pour le}

nec-tar)

a été notée pour chacune des deux teneurs en

_CO

₂

_.

_{Chaque après-midi,}

les

bou-tons floraux au stade 0-1 étaient

_marqués

et leur stade de

_{développement}

noté

_chaque

jour

entre 16.00 et 18.00 h

_jusqu’au

flétris-sement

_{(stade 8).}

Le nombre total de fleurs

produites

par chacune de ces

_plantes

a été

noté

_jusqu’à

ce

_qu’elles

aient toutes fleuri.

La

_production

de nectar a varié de 0 à

3,44

&mu;L/fleur

avec des

concentrations

allant

de 6 à 50 %

_(0-1,01

_mg de

_{sucre/fleur).}

Le

traitement au

_CO

₂

n’a pas eu d’effet

signi-ficatif sur le

_poids

de

sucre/fleur,

mais

_l’âge

de la fleur en a eu un

_{(tableau II):}

les fleurs

pleinement

ouvertes

_âgées

de 3 à 5

_jours

contenaient

_plus

de nectar _{que les} fleurs

_plus

jeunes

ou

_plus

vieilles

_(fig

2).

Les

_plantes

cultivées sous

_CO

₂

élevé ont eu en _moyenne

significativement plus

de

_{fleurs/plante}

_que les

_plantes

cultivées sous

_CO

₂

ambiant:

res-pectivement

156,8 (±9,2)

et

_{124,8 (±13,1)}

fleurs/plante.

Elles ont

_également

vécu

signi-ficativement

_{plus longtemps}

₍₇

_jours

au lieu

de

₆₎

et sont restées

_pleinement

ouvertes

pendant

4

_jours

au lieu de 3. En

consé-quence, une

_plante

cultivée sous

_CO

₂

élevé

avait,

à

_n’importe

_{quel jour}

donné,

signifi-cativement

_plus

de fleurs ouvertes

_qu’une

plante

cultivée sous

_CO

₂

ambiant

_(fig

_3).

Donc, sur la

_période

de

floraison,

elle est

susceptible

de

_produire

au total

_plus

de nec-tar ce

_qui,

combiné avec son offre accrue

de

fleurs,

peut la rendre

_plus

attractive _pour

les

_{pollinisateurs (par}

_rapport

à d’autres

plantes répondant

différemment),

mais

n’augmente

pas nécessairement sa

produc-tion de

_pollen.

L’offre accrue de fleurs aug-mente aussi les ressources

_disponibles

_pour

les

_populations

d’abeilles et d’autres insectes

floricoles. Il est

_probable

_que les effets de

concentrations accrues en

_CO

₂

sur la

bio-logie

florale des

_plantes

aura des

consé-quences

importantes,

bonnes ou

_mauvaises,

sur les

_{systèmes entomophiles.}

Les

don-nées de la littérature montrent que le

com-portement des

_{pollinisateurs}

_peut être

direc-tement affecté _par un

_léger

accroissement du niveau de

_CO

₂

_.

Pour connaître ces

consé-quences, il est nécessaire d’étudier les

plantes

en

_présence

des

_{pollinisateurs}

dans des conditions de

_CO

₂

élevé.

Zusammenfassung &mdash;

Nektar-und

Blü-tenproduktion

bei

_{Vicia faba}

(Pferde-bohne)

bei normalem und bei erhöhtem

Kohlendioxid-Gehalt in der

Umgebung.

Nach einer

_Vorhersage

könnte sich der

Gehalt des

_{atmosphärisches}

Kohlendioxid

bis zum Jahr 2100

_verdoppeln.

Erhöhte

_CO

₂

Konzentrationen hat bei den meisten

unter-suchten Pflanzen eine erhöhte

Photosyn-theserate zur

_Folge,

wobei das zusätzliche

CO

2

für das Wachstum und die

Vermeh-rung der Pflanzen genutzt wird.

_Häufig

ist

die Ernte von Samen oder Früchten bei erhöhtem

_CO

₂

_verbessert,

die

Blütenbiolo-gie

könnte aber ebenfalls beeinflu&szlig;t

wer-den,

was

_Folgen

für die

_Bestäubung

der

insektenabhängigen

Pflanzen haben könnte.

Einige

Arten

_zeigen

bei erhöhtem

_CO

₂

eine

erhöhte

_{Blütenproduktion}

und

_Blühdauer,

aber es wurden keine

_{Untersuchungen}

über

die

_{Nektarproduktion gefunden.}

Bei Vicia

faba

wurden deshalb der florale

_Nektarertrag

(Volumen,

Konzentration und Gewicht des Zuckers pro

Blüte),

die Anzahl der Blüten

und die Blühdauer untersucht. Die

Pflan-zen der Pferdebohne wuchsen in zwei

bie-nenfreien Versuchsräumen: einer bei

nor-malem

_CO

₂

_-Gehalt

der

_Umgebung

(350

&mu;L·L

-1

),

der andere mit erhöhtem

_CO

₂

- Gehalt

₍₇₀₀

_&mu;L·L

_-I

_{).Altersmarkierte}

Blü-ten

_{(1 -}

8

_Tage)

wurden

entfernt,

ihr

Ent-wicklungsstadium

(Tabelle I)

notiert und

der Nektar mit einer

_{Mikrokapillare}

_(0,5

_&mu;L,

1

_&mu;L

oder

_{5 &mu;L)}

extrahiert. Die

_Länge

der Nektarsäule in der

_Kapillare

wurde

gemes-sen, um das Nektarvolumen

_(&mu;L

_pro

_Blüte)

zu bestimmen. Die Konzentration des

Nek-tars

_(%;

_g Saccharose _{pro 100 g}

_Lösung)

wurde mit einem Taschenrefraktometer

bestimmt. Das

_{Zuckergewicht (mg}

_pro

Blüte)

wurde aus dem Volumen und der

Konzentration berechnet

_{(Pr&jadnr;s-Jones}

und

Corbet, 1991).

Die

Lebensdauer von allen

Blüten auf alternierenden Knoten von 10

Pflanzen

_(die

nicht für

Nektaruntersuchun-gen besammelt

waren)

wurden bei beiden

CO

2

Behandlungen

notiert. Jeden

Nach-mittag

wurden die

_Knospen

im Stadium

0-1 markiert und ihre

_{Entwicklungszeit}

täg-lich zwischen 16.00 und 18.00 Uhr

proto-kolliert, bis sie verwelkt waren

_{(Stadium 8).}

Die Gesamtzahl der _{Blüte pro Pflanze wurde}

für jede

einzelne Pflanze

_bestimmt,

bis alle

abgeblüht

waren. Der

_{Nektarertrag betrug}

zwischen 0 und

_{3,44 &mu;L}

_{Nektar pro Blüte}

mit einer Konzentration von 6 - 50%

(0-1,01

mg Zucker pro

Blüte).

Die

_CO

₂

Behandlung zeigte

keinen deutlichen

Ein-flu&szlig; auf die

_Zuckermenge

_pro Blüte. Das Alter der Blüten hatte

_dagegen

einen

signi-fikante

_Wirkung

auf das

_{Zuckergewicht}

_pro Blüte

_{(Tabelle II):}

_{3-5tägige, vollständig}

geöffnete

Blüten enthielten mehr Nektar als

jüngere

oder ältere Blüten

_(Abb

1 und

_2).

Pflanzen,

die unter erhöhtem

_CO

₂

gewach-sen

_sind,

hatten im Durchschnitt

_156,8

(±9,2)

Blüten _{pro Pflanze.} Das sind

signifi-kant mehr als bei normalem

_CO

₂

_-Gehalt

gewachsenen

Pflanzen, die

_124,8

_{(±13,1 )}

Blüten hatten. Bei erhöhtem

_CO

₂

Gehalt

hielten sich die Blüten

_{signifikant länger}

₍₇

statt 6

_Tage)

und blieben 4 statt 3

_Tage

in

voller Blüte.

_Entsprechend

hatte eine

Pflanze,

die unter erhöhtem

_CO,

gewach-sen waren, an

_jedem

_beliebigen

Tag

signi-fikant mehr offene Blüten als die

Normal-pflanzen

(Abb 3).

Demnach ist es

wahrscheinlich,

da&szlig;

_{V faba}

Pflanzen,

die

unter erhöhtem

_CO

₂

_wachsen,

_insgesamt

mehr Nektar

_produzieren

als unter

Normal-bedingungen.

Das würde

sie,

in

Kombina-tion mit erhöhtem

_{Blütenangebot,}

attraktiver für Bestäuber machen

_(im

_Vergleich

zu

anderen

Pflanzen,

die nicht in

_gleicher

Weise

_reagieren).

Das bedeutet nicht

not-wendigerweise

eine

_Erhöhung

der

Pollen-verbreitung.

Eine erhöhtes

_{Blütenangebot}

wird auch die

_{Nahrungsquellen}

für die

Popu-lationen von Bienen und anderen sich von

Blüten ernährenden Insekten erhöhen. Die Effekte von erhöhten

_CO

₂

_{-Konzentrationen}

auf die

_{Blütenbiologie}

von Pflanzen haben wahrscheinlich

_{wichtige Konsequenzen,}

gute oder schlechte, auf das

_System

der

Bestäubung

durch Insekten. In der

Bestäuberverhalten von

_{geringfügigen}

Erhöhungen

des

_CO

₂

_-Gehaltes

direkt beein-flu&szlig;t wird. Um diese

_Folgen

_genauer zu

erforschen,

sind weitere Versuche mit

Pflan-zen zusammen mit ihren Bestäubern unter

erhöhter

_CO

₂

_{Atmosphäre nötig.}

Vicia faba

/ Kohlendioixid /

Klimawech-sel / Nektar / Blühdauer /

REFERENCES

Acock B, Pasternak D (1986) Effects of _CO,

concen-tration on _{composition, anatomy,} and _morphology of _plants. In: Carbon Dioxide Enrichment of Green-house Crops. Volume II, Physiology, Yield and

Eco-nomics _(Enoch HZ, Kimball BA, eds), CRC Press

Inc, Florida, USA, 41-52

Ashman TL, Schoen DJ ₍₁₉₉₆₎ Floral _longevity: fitness consequences and resource costs. In: Floral Biol-ogy: Studies on Floral Evolution in Animal-Polli-nated Plants (Lloyd DG, Barrett SCH, eds),

Chap-man & Hall, New York, USA, 112-139 Bazzaz FA (1990) The response of natural ecosystems

to the _{rising global}

_CO

₂

levels. Ann Rev Ecol Syst

21, 167-196

Bond DA, Lawes DA, Poulsen MH ₍₁₉₈₀₎ Broadbean

(Faba bean). In: Hybridization of Crop Plants (Fehr

WH, Hadley HH, eds), American _Society of Agron-omy, Crop Science _Society of America, Madison, USA, 203-213

Bühler A, Lanzrein B, Wille H (1983) Influence of

temperature and carbon dioxide concentration on

juvenile hormone titre and _dependent parameters

of adult worker _honey bees (Apis mellifera L). J Insect _Physiol 29, 885-893

Búrquez A, Corbet SA (1991) Do flowers reabsorb nectar? Funct Ecol 5, 369-379

Cure JD, Acock B _{(1986) Crop responses} to carbon dioxide _doubling: a _{literature survey.} Agric For

Meteorol 38, 127-145

Davis AR, Gunning BES (1992) The modified stomata

of the floral _nectary of _{Vicia faba} L. 1. Develop-ment, anatomy and ultrastructure. Protoplasma

166, 134-152

Davis AR, Gunning BES (1993) The modified stomata

of the floral _nectary of Vicia faba L. 3. Physiolog-ical _{aspects, including comparisons} with foliar

stomata. Bot Acta 106, 241-253

Davis AR, Peterson RL, Shuel RW (1988)

Vascula-ture and ultrastructure of the floral and _stipular

nec-taries of _{Vicia faba (Leguminosae).} Can J Bot 66,

1435-1448

Ebadi R, Gary NE, Lorenzen _{K (1980)} Effects of

car-bon dioxide and low temperature narcosis on _honey

bees, Apis mellifera. Environ Entomol 9, 144-147 Free JB (1993) Insect Pollination of Crops (2nd ed).

Academic Press, London, UK

Garbutt K, Bazzazz FA ₍₁₉₈₄₎ The effects of elevated

CO

2

on _plants III. Flower, fruit and seed _production and abortion. New Phytol 98, 433-446

Gates P, Smith ML, White G, Boulter D (1983)

Repro-ductive _physiology and yield stability in Vicia faba

L. In: Temperate Legumes: Physiology, Genetics and Nodulation. (Jones DG, Davies DR, eds),

Pit-man Advanced _{Publishing Program,} Boston, USA,

43-54

Goldsberry KL (1986) CO2fertilization of carnations and some other flower

_crops.

In: Carbon Dioxide Enrichment _{of Greenhouse Crops.} Volume II, Phys-iology, Yield and Economics (Enoch HZ, Kimball

BA, eds), CRC Press Inc, Florida, USA, 117-140 Greenhouse SW, Geisser S (1959) On methods in the

analysis of _profile data. Psychometrika 24, 95-112 Handel SN ₍₁₉₈₃₎ Pollination _{ecology, plant population} structure, and gene flow. In: Pollination Biology

(Real L, ed), Academic Press, Orlando, USA, 163-211

Harder LD, Barrett SCH (1995) Mating cost of _large floral _displays in _{hermaphrodite plants.} Nature 373,

512-515

Harder LD, Barrett SCH (1996) Pollen _dispersal and

mating patterns in _{animal-pollinated plants.} In: Flo-ral Biology: Studies on Floral Evolution in Ani-mal-Pollinated Plants _(Lloyd DG, Barrett SCH,

eds), Chapman & Hall, New York, USA, 140-190 Hicklenton PR, Jolliffe PA _{(1978) Effects of} green-house CO2enrichment on the _yield and photosyn-thetic

_physiology

of tomato plants. Can J Plant Sci

58, 801-817

Kato M (1988) Bumblebee visits to Impatiens spp: pat-tern and _{efficiency. Oecologia 76,} 364-370 Kimball BA ₍₁₉₈₆₎ Influence of elevated

_CO

₂

on _crop

yield. In: Carbon Dioxide Enrichment of Green-house _Crops. Volume II, Physiology, Yield and Eco-nomics (Enoch HZ, Kimball BA, eds), CRC Press

Inc, Florida, USA, 105-115

Lacher V (1967) Verhaltenreaktionen der Beinenar-beiterin bei Dressur auf Kohlendioxid. Z _Vgl

Phys-iol 54, 75-84

Lawlor RA, Mitchell RAC, Franklin J, Mitchell VJ,

Driscoll SP, Delgado E (1993) Facility for _studying the effects of elevated carbon dioxide

concentra-tion and increased _temperature on _{crops. Plant Cell}

Environ 16, 603-608

Nicolas _G, Sillans D (1989) Immediate and latent effects of carbon dioxide on insects. Ann Rev

Ento-mol 34, 97-116

Parry ML ₍₁₉₉₂₎ The _potential effect of climate

changes on _agriculture and land use. Adv Ecol Res

Pearman GI ₍₁₉₈₈₎ Greenhouse gases: evidence for

atmospheric changes and _{anthropogenic} causes. In: Greenhouse: _{planning for} climate change (Pear-man _{GI, ed),} EJ Brill, Leiden, the Netherlands, 3-21 Pitelka LR (1994) Ecosystem responses to elevated

CO

2

.

Trends Ecol & Evol 9, 6, 204- 207

Pr&jadnr;s-Jones OE, Corbet SA (1991) Bumblebees _(2nd

ed). Richmond _{Publishing Company, Slough,} UK Ribbands CR (1950) Changes in the behavior of honey-bees following their recovery from anaesthesia. J

Exp Biol 27, 302-310

Seeley TD _{(1974) Atmospheric} carbon dioxide regu-lation in _{honey-bee (Apis mellifera)} colonies. J Insect _Physiol 20, 2301-2305

Snow AA, Spira TP, Simpson R, Klips RA (1996) The

ecology of geitonogamous pollination. In: Floral

Biology: Studies on Floral Evolution in Animal-Pollinated Plants. (Lloyd DG, Barrett SCH, eds),

Chapman & _Hall, New York, USA 191-216

Stange G, Diesendorf M (1973) The response of the

honeybee antennal _{CO2-receptors} to

_N

₂

_O

and Xe. J Comp Physiol 86, 139-158

Stoddard FL (1986) Floral viability and _pollen tube

growth in _{Vicia faba} L. J Plant _Physiol 123, 249-262

Stoddard FL (1993) Termination _{of flowering} in ’inde-tenninate’ faba beans (Vicia faba). J Agric Sci 120,

79-87

Stoddard FL, Bond DA (1987) The _pollination

require-ments of the faba bean. Bee World 68, 3, 144-152 Wittwer SH, Robb WM ₍₁₉₆₄₎ Carbon dioxide