- Email: [email protected]
Obligate mutualism between Trollius europaeus and its seed-parasite pollinators Chiastocheta flies in the Alps
0 Acad6mie
des
Population
sciences
biology
/ Elsevier.
f Biologic
des
Paris populafions
Obligate mutualism between Trollius eurOpaeus and its seed-parasite pollinators Chiastocheta flies in the Alps Mtitudisme obliptoire entre Trollius europaeus et sespollinisateurs pmusites de pines dzns /esAlpes N icolas Jaeger, Laboratoire
de
(Received
18
Laurence
biologie May
des 1998,
Despr&*
populations
accepted
d’altitude, after
revision
CNRS-UMR 21
August
5553,
BP 53,
38041
Grenoble
cedex
1998)
Abstract - Trolhs europaeus (Ranunculaceae) is involved in a mutualistic interaction with several species of Chiastocheta flies (Anthomyiidae) that are both seed predators and pollinators. In the present work, the pollination biology of T. europaeus and its association with Chiastocheta were studied for 3 years in six populations along an elevational gradient in the northern French Alps. We showed that T. europaeus is mainly xenogamous and Chiastocheta represented 90 % of all visitors. We suggest that almost all seed production was achieved by these obligate seed-parasites. Despite high variability in Chiastocheta activity, the pollination service they provided was high and reliable in all populations during this 3-year study and the seed set was not pollenlimited. The ability of T. europaeus to extend flower longevity during rainy periods and a long stigmatic receptivity in the absence of pollinators may help to explain the high female reproductive success observed at all elevations. (10 Acad6mie des sciences / Elsevier, Paris.) Trollius
europaeus
/ Chiastocheta
/ mutualism
/self-incompatibility
/ visitation
rates
/ pollination
R&urn6 - Trolh europaeur (Ranunculaceae) est engage dans une inter.lction mutualiste avec plusieurs esptces de mouches du genre Chiastocheta (Anthomyiidae) qui sent B la fois des pollinisateurs et des parasites de graines. Nous avons &udie la biologie de la pollinisation du trolle d’Europe et son association avec les Chiastochkes pendant 3 ans dans six populations du nord des Alpes frangaises ktagees le long d’un gradient alticudinal. NOLIS avons montrP que le trolle d’Europe est essentiellement allogamc et que les Chiastochktes reprksentent 90 % des visites de la fleur. Nous suggkons que la production de graines est essentiellement assuree par ces parasites de graines spCcifiques. Bien que I’activite des Chiastochktes soit t&s variable, les taux de pollinisation sont klev& dans toutes les populations pendant ies trois an&es d’ktude et la production de graines n’est jamais 1imitPe par le transfert de pollen. La capacitk du trolle j allonger sa duke de floraison pendant les Cpisodes pluvieux et la longue rkceptivitt stigmatique en cas d’absence des pollinisaleurs pourraient contribuer g expliquer le bon succ~s reproducteur femelle du trolle. (0 Acadtmie des sciences / Elsevier, Paris.) Tr0Uk.s
Note
europaew
communicated
*Correspondence E-mail:
/ Chiastochez~
by Claude and
/ mutualisme
I auto-incompatibih2
Combes
reprints
[email protected]
C. R. Acad. Sci. Paris. 1998 321,789-796
Sciences
de
la vie
/ Life
Sciences
/ faux
de visite
/ pollinisation
09,
France
N. Jaeger,
L. Despres
Version
abrdgde
Les mutualismes entre une plante et un insecte pollinisateur dont les larves se developpent au detriment des graines de la plante sont rares et generalement obligatoires: la plante depend entierement de l’insecte pour sa reproduction et reciproquement. En cas de faibles densites de l’insecte mutualiste, la capacite B l’autofecondation ou des strategies visant a attirer des pollinisateurs alternatifs peuvent etre selectionnes. Nous avons Ptudie l’interaction entre le trolle d’Europe ( Trollius europaeur, Ranunculaceae) et six especes de mouches Chiastochetes (genre Chimtocheta, Anthomyiidae) le long d’un gradient altitudinal (six populations a 1 000, 1 600 et 2 200 m) pendant trois ans dans le nord des Alpes francaises. La capacite du trolle a s’autofeconder a ete testee par ensachage des fleurs : 35-45 % d es individus sont incapables de produire des graines et 80-90 % des individus realisent une production de graines inferieure a 20 Yo en autofecondation ce qui permet de caracteriser l’espece comme allogame. Nos releves montrent que 90 % en moyenne des visiteurs du trolle sont des Chiastochetes. Les autres visiteurs observes appartiennent a differents ordres (Dip&es, Coleopteres, Hymenopteres). Ces visiteurs occasionnels presentent gene-
1. Introduction The between
sively genus, opment
to habitat
most extensively studied cases plants and pollinating seed-parasites
fig wasp [l-3], globeflower-globeflower Yucca and Ficus
Several species involved in
yucca-yucca moth 14, 51 and the fly interactions 161. Most of the species and the globeflower are exclu-
been assumed to be obligate: the without its associated pollinator
790
penetrate the globenectar and pollen 191 eggs on the surface of the flower. The larvae fraction of the seeds.
showed that this interaction in Finland: the plant is strictly flies are the exclusive pollinators.
ulations of T. europaeus those found in Finland.
(Ranunculaceae) with Chiasto-
In Europe, the globeflower with eight Chiastocheta
species ISI. Male and female flies shaped flower where they consume and where they mate. Females lay the carpels and passively pollinate of all species develop by eating a [6]
plant and
of its geographical pollinator may not for the plant, as was
of the genus Trollius a mutualistic association
theta flies (Anthomyiidae) [8]. Trollius europaeus is associated
Pellmyr mutualism ible and
mutualism are the fig-
the
vice versa. However, in some parts range, interaction with the associated be as obligate as is generally assumed shown in the case of Yucca [7]. are
of
associated with a single pollinating species or which in return depends on the plant for the develof its larvae. As a consequence, such associations
have frequently cannot reproduce
ralement une faible mobilite d’une fleur a l’autre ou visitent la fleur lorsqu’elle est sur Ie point de finer et ne participcnt done pas significativement a la pollinisation du trolle. Ces resultats suggerent que la production de graines du trolle d’Europe est essentiellement assuree par les Chiastochetes. Les densites en Chiastochttes dans chaque population et chaque an&e ont et& estimees par la moyenne du notnbre d’ceufs pondus par fleur. Cette moyenne fluctue entre 2.,62 et 16,82, ce qui indique une tres grande variabilite de I’activite en Chiastochetes entre an&es et entre populations. D’autrc part, nous avons observe une forte variabilite des conditions mtteorologiques entrainant une forte variabilite de l’activite des Chiastochetes au tours de la periode de floraison. Pourrant les taux de pollinisation sont tres homogPnes et nos experiences d’addition de pollen montrent que la production de graines n’est pas limit&e par les transferts de pollen. Le trolle semble capable d’augmenter sa duree de floraison quand il pleut et la duke de receptivite stigmatique peut etre tres longue (jusqu’a 12-15 j), au moins en cas d’absence des pollinisateurs. Sous des densites particulierement faibles en Chiastochttes, ces deux mecanismes pourraient Ctre dcs facteurs cl& dans le maintien d’un mutualisme obltgatoire entre les deux partenaires.
is an obligate self-incompatHowever, pop-
in the Alps are very different from They are much smaller in size due
patchiness
and
distributed
along
an elevational
gradient ranging from 700 to 2 600 m. This allowed us to study the pollination biology of T europaeus and the characteristics of its interaction with Chiastocheta under various variation
ecological conditions. of weather conditions
Habitat patchiness and the are likely to induce var-
iability in Chiastocheta activity. tion for self-compatibility and/or pollinators when Chiastocheta
This could lead to selecstrategies to attract other provide unpredictable or
inadequate service 171. Studies on other plant species suggest that a strong limitation of reproductive success due to poor and/or variable pollination activity can result in selection tion was pollinator
for self-compatibility [lo, 1 I] and self-pollinareported in T europaeus [I 21. At high elevation, species diversity is likely to be reduced I1 3-l
51
but at an elevation of 1 000-l 500 m, many insects such as bees, wasps, syrphid flies and bumblebee queens are present in globeflower populations and hence are liable to affect slightly
pollination. bowl-shaped
In all other Trollius species, flowers allow access for
flat or many
potential pollinators ]8]. The closed flower T. europaeus is likely to be responsible for exclusivity the interaction by preventing most other potential nators from T. europaeus the association cific
In the present
polli-
entering the flower. However, the globe of can be more or less tight [16] suggesting that with Chiastocheta may not be highly spe-
throughout
interaction is a case
of of
its geographical paper,
between of obligate C. R. Acad.
we examine
range. the possibility
Trollius europaeus mutualism along Sci. Paris, Sciences
that
the
and Chiastocheta an elevational grade
la vie / Life Sciences 1998.321.789-796
Troliius
dient in the Alps by answering two T. europaeus self-compatible? and b) affect pollination of T. europaws! We lination rates and by pollen transfer.
we test for limitation
2. Materials
questions: a) is do other insects also analyse polof seed
production
and methods in the Massif de la Chartreuse and (northern French Alps) in May-July
1995-l 996-l 997. Six populations of T. europaeus were selected in the lower part (Cherlieu, 950 m and Cottaves, 1 050 m), in the middle part (Crolles, 1 550 m and Som, 1 550 m) and in the LX, 2 100 m) of the several weeks
upper part elevational
thousand from May
(G‘tlihier, 2 300 m and range. Each population
individuals and to July depending
flowering on eleva-
Trollius eul-opaeus L. is a hermaphroditic arctic-alpine species (Ranunculaceae). In our populations, it was visited by six Chiastocheta species (Anthomyiidae): C. drntifera, C. inermella, C. maoopyga, C. rotundiventris, C. setifera and C. trollii (described in j 17) and II RI, taxonomy in height composed
of the flies following 11 911. The plant is 0.2-l m usually produces a single yellow flower of 6-l 5 sepals enclosing 1 O-1 5 nectariferous
and
staminodia 7: europaeus We counted number
and the occasionally the number
of
pollen
reproductive produces of stamens
grains
in
organs. However, two or three flowers. on 46 flowers and the
four
anthers
of
14
flowers
using the method described by Atlan et al. 1201 at Cherlieu in 1995. Each year and in each population, we counted the number of carpels and we assessed the number of ovules by randomly selecting five carpels 161 on 38-95 flowers. Individual Results for
flower populations
lifespan and
and years)
anther were
dehiscence estimated
(set by tag-
ging 16-120 flowers per population on their first day of flowering and checking for sepal retention and anther dehiscence each day. Stigmatic receptivity was tested by experimental cross-pollination at Cottaves, Crolles and Galibier in 1997: 122-l 61 flower buds per population were emasculated and enclosed with nylon mesh bags. Ten flowers were hand cross-pollinated on the 1 st day of flowering, ten other flowers on the 2nd day, etc., until 12th or 15th day (depending on the population;t mixture of pollen from S-l 0 donors, and checked set. Seed
production
The breeding production by
indicates
system pollen
stigmatic
and were
potential investigated
with a for seed
receptivity, limitation of seed hy conducting
then own
fllowers pollen
were (hand
pollen flowers
from per
5-10 donors to 1’3-20 population on each day
C. R. Acad. 1998.321,789-796
Sci. Paris,
Sciences
de
la vie
/ Life
Sciences
with their 13-24) or left
naturally pollinated of flowering. Within
each population, all treatments were conducted within a week. Atl flowers were collected and analysed 2-3 weeks after the end of their flowering when viable seeds are easy to distinguish and before numbrr selecting
from non-fertilised predation by larvae.
ot’ seeds per five carpels
ovules C)n
or aborted each flower,
carpel was assessed 161. Throughout the
seed s-t of a flower dividecl by the mean population.
is the number
by present
seeds the
randomly paper,
number of seeds per of ovules per carpel
carpel in the
In e,lch population, we counted Chiastocheta and all other insects penetrating ten flowers during 18-63 periods of 10 min under diverse weather conditions (except rain), times of day (between 0Y:OO and IS:00 hours) and dates n 1995. was estimated (17 = 411-95
In each population, mean number
by the
flowers
Frequencies egg counts
per
were were
Chiastocheta of eggs laid
population!
arcsine square
in 1095-I
per 996--l
square root-transformed root-transformed to
density flower 997. and satisfy
assumptions for analyses of variance. Year, treatment, elevation, population (nested in elevation) and interactions were considered as fixed effects, and type III mean squares were used yses ‘Nere carried (I 090).
in the analyses of variance. out using SAS statistical
All analprograms
3. Results Flowers were 1 O-6!,, n = 909
composed flowers)
of .31.2 containing
* 9.6 carpels 11.6 +- 1.6
(range ovules
each (range 5-18, n = 855 flowers) and 163.9 + 23.2 stamens (range 11 7-247, n = 46 flowersj containing 6 843 + 2 014 pollen grains each (range 2 225-l 1 120, n = 14 flowers). Our estimates ranged from 2 000 to 4 000. f’loVvers effect
of
lasted year 102.7;
from
q
longevity For example,
of
4 to 16 d. There
pollen/ovule was
ratio
a significant
(F,, J,o=. 547.9: P = 0.00011, elevation I’ = 0.0001 1, population (F i, J,. = 16.5;
flower days.
plants. We first to produce seeds
enclosing 40 flower buds were bagged,
from 5-10 donors (hand cross-pollination, n = 40-58). Seed set under natural pollination was assessed by randomly collecting 38-95 flowers per population. Pollen limitation of seed set was tested by adding a mixture of
ments showed
on different was not able
mutualists
self-pollination, n = 8-23). emasculated and bagged, then with a mixture of pollen
(F 2 JIo= P = 0.0001 !, year x elevation and year x population IF, flowtr longevity. In several
performed T europaeus
and Flower
its obligate
either hand-pollinated self-pollination, n =
five treatments (see Results for populations and years): spontaneous self-pollination, hand self-pollination, hand cross-pollination, natural pollination and addition of pollen. Only primary flowers were selected so that treatwere that
and
without pollen by emasculating buds with nylon mesh bags.
untouched (spontaneous Other flower buds were flowers were hand-pollinated
The study took place the Massif du Galibier
contained lasted 3-5 tion.
europaeus
to
(F, 3,,, = 307.4; P = 0.0001 i .rlo = 15.0; P = 0.0001) on populations, we observed
increase with the number of it was much longer at Lac in 1996
rainy than
791
N. Jaeger,
L. DesprGs
in any other populations owing to a l-week period
during of rain.
these
3 years
itable
Seed higher
I)
5.7; Anther dehiscence lasted 6.3 + 0.8 at Som (n = 20), 7.9 9.4 f 1 .I at Cottaves (n = 50) Calibier vations
were hand
Stigmas remained of flowering,
Table
flower
II is the
20 %. Seed set under ranged from 3 to
a decrease from bagged flowers
that
longevity
the 8th to were able
per population
in 1 YYS, 1 YO6 and
able,
than
each
1 YY7:
mc’an
under I. The
oi days
m
Crolles
3.0
f 0.9
Ill = 201
1 600 m 2 200m
SO111
Lat
4.9 4.6
+ 0.7 f 0.6
I/J = 211) (n = 16)
Galihirt
5.0
f 0.6
(n = 1 Y)
Flowers
were
seed
set below
hand effect
self-pollination of treatment
whatever
+ standard
in = 191 111 = 201
checked
for
7.0 7.2 7.1 15.2
+- 0.4 f
0.6
* 0.4 k 2.3
20 %. !F,
was
the year
retention
each
-liIcI = 723.1; liignificant in
(l-tests).
Seed
set
drviation. I907
(/I = 231 f/J = 201
7.3 8.6
(R = LO) (II = 201
6.9 f 1. I !n = 20) 6.6+0.71;,= 1101
~p~\l
any seeds individuals
was, significantly
1096
1 600
of flowersl.
able to produce and among the
cross-pollination
tested
1905 6.0 + 0.8 3.5 + 0.7
hand
population
number
not
80 ‘%, had
set under
higher
Cherlicu Cott
(number
flowers were self-pollination
f3 = 0.0001
m m
m
were
Seed
cross-pollinated at least until Seed set showed dramatic and 15th days.
PolIuldtions
size
seed set helow per population
35 ‘% of the under hand
1 000 1 000
sample
able, 90 % had self-pollination
for 12-l 5 d after the first the absence of pollinators
Elevations
2 200
self-pollina-
receptive at least in
seeds when hand day of flowering. on the 13th, 14th
I. Mean
spontaneous
15 ‘%, (table II) with a significant effect of population P = 0.03) and year x population (F ‘,, LOci= 2.43; 3.65; P = 0.002) but no significant effect of year (Fh 10’) = (FL, Loci = I .5; P = 0.22) (F , l,jcI = 1 .38; P = 0.241, elevation ancl year x elevation (F,, J,,4 = 0.18; P = 0.83~. About
(figure 7). Although there was the 9th days, the emasculated to produce the 12th decrease
set under
ir = 0.73; n = 210; P < 0.01). Anthers during rain and there was a rapid presas soon as weather conditions became
favourable.
day
1). Seed
significantly (F,, LcIcI =
0.901, year x elevation iF,, ,,,) = 0.65; P = 0.421 and year x population (F,, qiI = 0.07; P = 0.78). About 45 “% of the flowers were not able to produce any seeds under spontaneous self-pollination and among the individuals that
among elepopulations
(F,, , 79 = 24.6; P = 0.0001). Pollen presentation was gradual with the outer anthers dehiscing first. Anther dehiscence occurred throughout flower lifespan with a good correlation between the end of anther dehiscence and flower senescence were not dehiscent entation of pollen
P = 0.01
hand self-pollination was spontaneous self-pollination
tion per population ranged from 3 to 7 % (&h/e I/j with no significant effect of year (F,, ,,,) = 0.28; P = O.J9), elevation P = 0.06), population (F,, ‘),, = 0.28; P = (F I 00 -- 3.57;
from 5 to 11 d. It was + 1.5 at Cherlieu rn = 201, and 6.9 + 0.8 (n = 120) at
in 1997 with a significant difference (F,, ,79 = 65.61; P = 0.0001) and
set under than under
8.6 day
from
the
first
day
+ 1.4 In = 201 f 0.5 C/l = SO)
t
1.3 UI = 201
of anthesib
(= first
day
of
flowering).
/Cottaves 1
iCrolles I
80% 70% 60% 50% 40% 30% 20%
Day Figure
1. Determination (0 = 122) in 1997.
oi stigmatic
The duration of stigmatic receptivity 2nd, etc., or 15th day oi flowerlng.
792
receptivity
by experimental
was estimated Seed production
from seed indicatcl\
hand
of flowering (.roi~-l,o/lination
at Cottaves
(n = 1 hl I, Crolles
(17 = 141 I ancl
set oi rmascul,ttc~d and haggrsd flowc,rs that wcsre hand cross-pollin,ltcd stigmatic r(‘c eptivity. Vertical bars are standard deviations.
C R Acad.
Sci. Paris, Sciences
Glibier on the Ist,
de la vie / Me Sciences 1998.321,789-796
europaeus
Trollius Table
II. Mean
seed
set per
population
under
Treatments Spontaneous
self-pollination
Spontaneous
95
self-pollination
96
different
Cottaves
7 f; 1 0 ‘X, Ii,=231 -
7 f 9 ‘%I in = 17)
and
1997:
mean
i standard
Crolles
deviation.
Som
Galihier
4 + 7 ‘!% In = 141
111 = 241
(n = 14)
(f? = 131
111 = 20)
(n = 201
74 * 22 ‘%I In = 54’1
67 + 27 ‘%a i/J = 54)
72 * 13 %
6.i It 20 ?%a
72 * 23 “4,
I/J = ,581
If1 = 401 NO + 12 ‘!U
(n = 501 69 t 18 “%,
pollination
95
8 1 1 1 5 ‘%,
8 I f 19 ‘%>
90 i
Natural
pollination
96
(n = 95j 75 i 19 ‘%,
t/1 = 381 74 i 1 5 ‘%I
(11 = 60) 74 + 16 ‘%,
Natural
pollination
97
Y7
ot flowers). per camel
under hand cross-pollination 63 to 74 % (table //) with
in = 50)
in = 501
80 Yk 1 7 ‘%,
7 1 i 1 Y ‘% I” = 5 5 ‘I
at Cottaves, and 0.19 at
in set
under natural pollination per population ranged from 56 to 90 ‘% (table /I) with a significant effect of year (F,, o,r, = 49.31; P = O.OOOl), elevation iF, c,,,, = 38.9; P = 0.0001) and year x elevation (F, ‘,,r, = 5.7; P = 0.0001) Ibut no sig(F,, ‘,,r, = 1.73; P = 0.16) and 1.36; F’= 0.22). It was high and during these 3 years: it was
higher than SO ‘%, for 80 ‘%I of individuals 70 “io for 50 % of individuals. Seed
set
under
higher than under P = 0.99). The effect
pollen
addition
was
natural pollination of treatment was
and not
higher
8.5 2 15 % (11
on primary of ovules
Among Cherlieu records),
significantly
12 “i,
I/? = 46) 5 6 +- 1 h ‘% In = 50) 72 f 20 ‘5,
(n = 40) 5.3 f 1 9 ‘!% in = 20) -
k 1 5 ‘I/;, II? = 19)
78 + 2 3 ‘%
(n = LO1
LO)
Seed and
set oteach flower was given as a percentage.
calcu-
all visitors, Chiastocheta represented 91 t 16 “XI at (n = 57 records), 85 + 31 % at Cottaves (n = 60 77 + 26 ‘%, at Crolles in = 18 records), 90 + 16 %
at Som (n = 57 records), and 94 + 8 ‘XI at Galibier itant dlffercnce P = 0.10) and (f (, ~~jr, = .67;
93 + 8 ‘%, at Lac in = 60 records) (n = 63 records) with no signif-
among populations P = 0.1 7).
to Iiymenoptera, small Coleoptera
elevations for Other
this visitors
(F,, jIj0 = 2.27; percentage observed
Diptera or Coleoptera. At all (Oedemeridae, Nitidulidae,
Cleridae, Cerambycidae and Staphylinidae) were observed inside the flower. At high elevation, only Diptera and C‘oleoptera were observed to enter into the globe of T. europa~s. At low and intermediate flies were able to enter old flowers became less tight, some vespid wasps sometimes observed to crawl bumblebee queens (5ombu.s visit 7. europaeu5 flowers.
than
(F,, ;rlli = 0.01; not significant in
=
flowers ot ditterent plants. L)er carpel in the population
belonged elevation,,,
also significantly (F,, ,,?s = 2462.9;
I’= 0.0001). The effect of treatment was significant each population tested whatever the year (t-tests). Seed
nificant effect of population year x population (F,, ‘,,r,= reliable in all populations
50)
49
+ 2 1 ‘X, (rl = 201
and populations (F,, lol index (SC1 = seed set set under hand cross-
was
=
!rJ = 17)
64
per population ranged from no significant difference among
pollination self-pollination
(11
10 f
in = 501 f 16 ‘“;I
In = 501
pollination; 121 1) was 0.14 at Cherlieu, 0.17 0.20 at Crolies, 0.0’3 at Som, 0.06 at Galihier Lac in 1995. Seed set under natural higher than under hand
ho
74 t I 6 ‘I/;, (n = 50) 7.1 * 2 ; “,’,I,
Treatments were performed dividrd hy the mean numhcr
elevations (F?, lo-l = 2.51; P = 0.08) = 1.49; P = 0.22). Self-compatibility under hand self-pollination/seed
14 ‘%,
(n=ll1
(n = 50)
in = 181
inumber of seeds
in = 201
110 -t 1 7 ‘!% 111 = 50 I 7’) .+ --_ 3 ‘, “y 0 t32 2 23 “%I (n = 20)
11 is the sample size lated as the number
(iJ = 101 11 *15’io
in = 8)
6 f; I 1 ‘%>
1 6 ‘X,
Natural
addition
3 T!z5 “4,
(II = 19) 8 f 1 3 ‘%
96
Pollen
.3 + 6 “/ (I
(II = 1 51 1 + h ‘%>
In = 241 4 t j ‘%
self-pollination
96
i + 4 ?”
(17 = 17) I 0 t 9 ‘%,
Hand
addition
Lac
!n = 101 4 & .y “‘1,I)
11 i
Pollen
mutualists
2 + 4 “/O
95
95
1996
its obligate
12 + 1 I ‘%I
self-pollination
cross-pollination
in 1995,
Cherlieu
Hand
Hand
treatments
and
5.8 2.8
inside
elevations, when iVespu/a the
soroemsis)
syrphid the globe sp.) were
globe and a few were observed to
During a period of 10 min, ten flowers were visited by + 5.0 Chiastocheta at Cherlieu (n = 57 records), + 1.1 at Cottaves (n = 60 records), 4.4 k 3.8 at Crolles
(n = 18 records), 10.7 13.6 + 7.11 at Calibier
+ 7.7 at Som (n = 63 records)
(n = 57 records), and 20.2 f 9.5
each population tested whatever the year (t-tests). Seed set under pollen addition per population ranged from 49 to 85 ‘% ([ah/r II) with a significant effect of year (F,, ,AJ =
(n = 60 records) at Lac with a significant difference among elevations (F,, ~o~j = 108.1; P = 0.0001) and populations (F-r, (r,‘, = 15.3; P = 0.0001). Mean number of
6.4; P = O.Ol), elevation (f ,I, ,j4 = 3.17: f’ = 0.041, population (F, ,L4 = 7.9; P= 0.06) and year x elevation (F,, ,LJ = 7.87; P = 0.006) hut no significant effect of year x population (F,, ,jd = 1.63; P = 0.20).
Chiastocheta eggs laid per flower showed great variation ranging from 2.62 to 16.82 (tab/t> 111) with a significant effect of year (F, Lj4, = 66.1; P = O.OOOl), elevation P = O.OOOl), population (F,,,,,, = 17.5; iF .!, ‘JJ I -- 81.9; P = 0.0001 i, year x elevation (F, cl1, = 21.6; P = 0.0001) and year x population (F,,, .1,,) = 1.1.9; P = 0.0001). The
Chiastocheta Depending on C. R. Acad. 1998.321,789-796
were the main the population,
SCI. Paris,
Sciences
de
visitors at all elevations. 2-6 species were found. la vie
/ Life
Sciences
N. Jaeger, Table
L. Despres
III. Mean
number
of Cl~ia~toci~eta
Populations
eggs
Crolles
Soni Lac
In 1995,
Galihier
5.20 i- 3.03 4. 18 t 2.98
(I) = 501
4.92
+ 4.22
(17 = .s[)l
.3.96
3. 1.71
l/J = 501
5.36 8.57
* 3.04 i 4.84
3.74
i- 1.89
111 = 501
7.54
i 5.52
f/l = i0) (n = 40) ki = 55)
,Ifter
the end
of their
* 9.00
in = 501 C/~i,~stoch~~& after hatching.
at Crolles,
Som,
eggs
were
Lac and
counted
Gal-
produced by outcrossing. Self-comlow (O.O:-0.2) and consistent with
has a gamctophytic self-incompatibiland Despr&; unpublished data) like Ranunculaceae 1231. However, in all
populations, some under self-pollination. for their germination
individuals were able to produce seeds Further studies are needed to test ability. Under hand or spontaneous 35-45 ‘%, of individuals produced % of the partially self-compatible
had a seed set under 20 % suggesting be considered as a serious alternative to outcrossing in our populations. insects
affect
pollination
no indi-
that selfing reproductive
is an exclua) G&tovisitors were
unlikely to have a significant impact on pollination. First, many insect species were recorded, but very few individuals of each species were actually observed inside flowers. Second, these occasional visitors were unlikely to pollinate T. europaeus. Coleoptera and Diptera were rarely seen to move from one flower to another. Syrphid flies, wasps or bumblebee queens were sometimes observed at low and intermediate elevations inside flowers of T. curopaeus but our observations suggest that they are also unlikely to affect pollination: bumblebee queens
794
of the
or1 cdrpels
4.04 2.62
flowers
weeks
2-3
+ 2.12 f 2.23
(n = 50) (n = 50) h = 78)
a very short time inside each flower, syrphid often not in contact with stigmas and entered
flowering.
flower when it was 5 or 6 d old (after most pollination occurred) and wasps were never seen to move from
had one
to another. This suggests that there is no other sigpollinator of T. eu/-opaeus. The shape of the seems to efficiently prevent visits of other pollina-
the form interesting c ificity
of a bowl results of this
4.3. Why high and
[ 161. Field concerning
flowers to open
of in
studies there should provide the maintenance of the spe-
interaction.
is female reliable?
Pollen-addition
reproductive
never
success
led to higher
of T. europaeus
seed
set than
natural
pollination suggesting that pollen transfer did not limit scecl production 1241. Resource limitation or other factors such as pollen-pistil interference and post-zvgotic abortion could be responsible for the undeveloped seeds [25271. There is no reason to suspect limitation of seed production by pollen in 1995, since seed production was JS high or higher than in 1996 l)opulations, seed production limited
by pollen
transfer
and 1997. appears during
these
Hence, in all our not to have been 3 years.
We observed variation in Chiastocheta activity within flowering season in all our populations due IO great variation in weather conditions. During periods of rain no Chiastocheta flies were observed in the flowers. Moreover, there was a significant decrease in Chiastocheta visitation rates due to cloudiness (Jaeger and Despres,
of T. eoropaeos?
Trollius europaeuslChiastoci,eta interaction sive mutualism in our populations because theta were the main visitors and b) other
spent were
5: 3.08 in = 50) 2 2. I4 in = 501
tors. In some parts of its range (Poland), 71 europaeus (var. transsilvdnicus) are reported
self-compatible?
land. T. europaeus ity system (Jaeger other species of
Do other
-
(I1 = 501
i 1 1 .OY !n = 60) + 5.92 \n = 461
the high value of polleniovule ratio (2 000-4 000) typical of xenogamous species 1221. The low seed production under self-pollination suggests that the plant is selfincompatible, consistent with Pellmyr’s study 161 in Fin-
4.2.
1997
f 4.39
Seed set never exceeded 15 “/u under self-pollination whereas it reached 74 “% under hand cross-pollination and 90 “% under natural pollination suggesting that most
viduals cannot strategy
deviation.
6.92 16.00
4. Discussion
self-pollination, seeds and 80-90
+ standard
1996
flower nificant flower
were was
mean
4.08 1.04
was significant
seeds (if not all) patibility index
1997:
(il = 95) In = 401
10.t1.2
Is T. europaeus
and
+ 1.57 + 2.53
n is the sample size (number of flowers). Empty egg shells remain on carpels even
4.1.
1996
4.12 2.95
7.41
of year (t-tests).
per population
1995
C:herliru Cottnves
effect ibier
Iaid/tlower
flies the
unpublished data). Other studies report no or few insects on rainy days 1281 and show strong effects of weather on visitation ference among
rates 129-31 in the mean years, elevations
difference populations
1. There was also number of eggs and populations
a significant diflaid per flower and a significant
in the fly visitation rates among elevations and reflecting variation in Chiastocheta activity
161. This could be due to variation ,Ind possibly habitat patchiness We showed % europaeus Chiastocheta.
that almost was achieved High pollination
in weather 1321.
conditions
all seed production of by pollination service of levels achieved by Chias-
tocheta, provided that they are common in I europaeus populations, could explain why the plant has not evolved towards self-compatibility or strategies to attract alternaC
R. Acad.
Sci.
Parls.
Sciences
de
la vie / Life Sciences 1998 321, 789-796
iroilius tive pollinators. Moreover, number of Chiastocheta service. This suggests that seed predation for similar variation high and
in Chiastocheta not pollen-limited
populations varied in the eggs for equivalent pollinator some populations suffer higher pollination levels. In spite of activity, seed production was in all populations. Extension
many species should sufficient pollen has populations
europaeus
have been
where
and
its obligate
mutualists
flowers adapted to wait until transferred to the stigmas. In
Chiastocheta
activity
is particularly
low and unpredictable, these two traits for maintenance of obligate mutualism.
could
be critical
of flower longevity under rainy conditions and long stigmatic receptivity in the absence of pollinators could allow T. europaeos to minim&e negative effects of this variability in Chiastocheta activity. Other studies suggest that long
in conclusion, almost all seed production is achieved by pollination service ofChia.stoche~~. Selfing cannot be a serious alternative reproductive strategy to outcrossing and cross-pollen is likely to be exclusively transferred by
flower could
Chiastoch~ta whatever the elevation. In that sense, the association between T. europaeus and Chiastocheta can bc considclred as an obligate mutualism in our popula-
longevity compensate
and
stigmatic receptivity for low or unpredictable
rates 115, 301. Robertson the dehiscence of anthers report increased duration phases, deposition
respectively, are low
in alpine plants pollination
and Lloyd 1331 found delay in in periods of rain. Other studies of staminate and pistillate
when 134-361.
pollen removal and According to Primack
Acknowledgements: We thank Patrice Colcnson, ante. WC thank Irt’ne Till-Bottraud for help with Raymond, Gordon Luikart and John Thompson (Ph.D. fctllowshlp to N.]. and grant AC(CSV71
pollen 1371
D.H..
How
Rrv.
Lcol.
Syst.
10 / I Y~YI 1 1-51.
121 Bronstein J.L.. Seed prrdators as mulualisb: ecology and the fig/pollinator interaction, in: Bernays E (ec1.1, Insect-Plant (Vol. IV). CRC Press, 1992, pp. l-34. 131 Anstett M.C., tars: cvolutlonary 12 I 1996) 94-99. [4J Addicott interaction 494.
J.F., Variation between yuccas
in the costs and and yucca moths.
Iwneflti of mutualism: Occolog~,~ 70 (19861
Linhart glauca Am.
191 Hagerup O., 1956, 1,. 231).
Peterson
Y.B.. Reproductive consequences of (Agavaceae) and ~ege/icu/a yurc-ax//~ J. Bot. 81 (1994) 815-ii25.
V., Botanisk
Atlas,
and Biol.
Munkegaard,
I1 1 i Schoen in C;/yoi~e Evolutlon45
D.J., Brown H.D., Whole arg)wd and C. c-/andcstin.l 119Yll 1651~ 1665.
il 21 Tutin /I. L 10.
T.G.,
Europaw,
Press,
eww
(oadaptaJ. Linnean
and Espletia
self-pollination of autogamy,
Cambridge,
C.
R.
Acad.
1998.321,789-796
Harper K.T.. Booth Am. Mitil. hat. 120
Sci. Purls, Sciences
C.M., 11Y081
Elevational (25-3 IO.
de la vte / Life Sciences
distribution
K.A.. 30.
I I71 ( 01 in J.lI.. da1~1, f’wc. Roya
rainy periods explaining this
Eiiicient
The genus Entomol.
pollinalitrn
ot
activity,
seed Extension
and long result.
Cl?iasfoc-iwr,~ Sot. London
,Ilpine
proof
stigmatic
in Lintiwr ILY-376.
11’11 blichrlwn J.W. Lctic~rstc~llt.
oi the Anthomyiidae 11 11 9i35) 37-65
V., A revision Stcwslrupia
Iplants,
Nature,
iY1
t’okorny !DIpwra: AnthomviiiB: L i 11Y5.1) c15m102.
11 81 t iertmg 1v., Anthomyiidar, arktlschc n Rwion, 1976, pp.
C. :(YI.I, Die
Fliegen
il)lpteral
der
Palar-
descrthcd
by
1201 Atlan A. Couyon P.ti., Fournial T.. Pomente D., Couvet, D., Sex allocation 111 a hermdphrodltic Illant: the case oi gynodioecy in fhymus wlh’dm I ., 1. Evol. Hiol. 5 11992) 183-201. 121 l Lloyd FunI-tional
D.C., Schwn D.I., Self- rmd ( rw-fertilization dimensions, Int. J. Plant S( I. I i $ lOYE I T&369.
IL2 l Cw Icn R.W., Pollen-ovule ing systems in flowcwng plants,
ratios: A c onwrvative Evolution 11 11977)
IL 11 IDoLlglas K.L., Cruden R.\,V, The rcprodu( ccanxicww iRanunculateae:b: breeding system selec-tier, Am J. Bat 131 I1 9941 .I1 4-121.
tlve and
1241 Am
plant
I3ierrychudek P.. Pollinator Nat 117 / 1981, 838-840.
1261 (:harlesworth seeds!. N,lturI~
D,
Why
3
limitation
of
do plants 21-22.
oi
producc~
1271 Scri )ailo < rossed ‘,eed Plant Keprod.
R.W., Barrett S.C.ti., Effects set in trlstyltrus Pomrdcrid 7 il Y041 273-281.
1281 Yurroto nated pl.ints
T., The ecological in an ,Ilpine meadow,
1201 Mc(:all C:., Pnmack weather, timct of day and communities. Am. J. Dot.
lY64.
I1 31 Arroyo M.T.K., Arm&o J.J., Primack R.B., Community studlrs in 1’01~ lination ecology in th(a high temperate Andes of central Chllc. II. Effect of temperatureon visitation rates and pollination possibilities, PI. Syst. Evol. 149 (19851187~203. 1141 Warren S.D., insect pi’llinators,
during help
Chiastocheta not pollen-limited.
in
indicator 32-46. Ih~ology facilitation
plants.
I.
OI brecdof Anemone ot sexual
reproductive
effort.
125; Wit n\ II., Calvin C.L., LZ/~lson CA., Davern C.I., Frank D., Seavcy L.R., Rc~~wrluctive success. spontaneous embryo abortion and genetic load in flovwring plants, Oecoltrgia 7 I 11 9871 501~.5OY.
Copenhagen,
antl wthin-flower and the evolution
University
of 148
interactions tlepidop-
P.E.. Calve R.N., Wind-pollin,ltion, self-incompatibility shifts in pollination systems in the high Andcan genus Am. J. Bot. 76 11989) 1602-I 61-t.
Flor,l
the 486-
J.N., Brown J.M. HarrIson R.C., Evolution in the yucca moth lineage, Am. Nat.
181 Pellmyr 0.. The phylogeny oi a mutualism: evolution bon between Tro///cis ,~nd its seed parasitic pollinators. sot. 47 (19Y21 3 37-+6i.
11 01 Berry albtudina IAstrraccwj,
fig polllnaEcol. Fool.
0.. The cost of mutualism: interacllons between Tro//w\ Its polllnatlng parasites, Oecologia 78 I 1989) 53-5’).
171 Dodd R.J., between Yuccd tera) in Colorado,
0i
evolulion Interactions
Hossaert-McKey M., Kjellberg F., Figs and confllcti in a cocvolvetl mutu,llism, Trends
151 Pellmyr 0.. Thompson poliinatlon and mutu,llism (19961 827-847. 161 Pellmyr paeu~ and
flower longevity receptivity could
11 51 Btngham I I W81 2 18-L
to be a fig!. Annu
of variable high and
Charlottr Fauric>, Mathieu Joron. Pierre-Yves Pinwn and S&wine Souhcyrand for field awststatistics and comments on the manuxript. We also thank Finn Kjellhrrg, Guy iempdric’re, ,\/\ichel for critic al warlint? of this article, T t 1s work was supported hv thcs Frenc II Ministry for Rcwlarch
5. References I1 1 Janzen
tions. In spite duction was
so many
of prior Tdgitfdfd
Imore
w&s
self-pollination (Pontederiaceac!.
polllnatlon syndromes Etol. Res. 1 11986)
of 83-95.
than on outSex.
insect-pollI-
R.B., lnfluente of flower charactctnstlts, season on insect visltatlon rates in thrw plant 79 (1992) 433.-442.
I301 Arrc vo M.T.K.. Primack R., Amwsto J., Community studies in pollination rc ology in the high tempcratc Andes ofcentral Chile. I. Polllnatlon mechanlms and altitudinal van&on, Am. J. Kot. 69 (1982) 82-Y7. I.11 I Tntl,lntl O., Influence drn\ity (,n inwct flower Rewarch 26 , 19941 hh-il.
of climate, timca of day anti visitation in al[)lnc horwav,
season, Arctic
and and
flower Alpine
795
N. Jaeger,
L. Desprbs
1321 Husband B.C, tristylous Eichornia (19921365-371. 13.31 Robertson A.W., in Myosotis c&nsoi,
Barrett S.C.H., Pollinator paniculata in northeastern
in population Oecologia
Lloyd D.C., Rates of pollen deposition Funct. Ecol. 7 (1993) 549-559.
1341 Devlin B., Stephenson the staminate and pistillate 145 (1984) 323-328.
796
visitation Braril,
A.C., phases
Factors that influence of Lohtliia cardInalis
and
of 89
removal
the duration of flowers, Bot. Gaz.
1351 Richardson T.E., Stephenson A.G., Pollen removal and sition affect the duration of the staminate and pistillate Campanda rapunculoides, Am. J. Bot. 76 (1989) 532-538. 1361 Khadari B., Ciberneau M., Anstett McKey M., When figs wait for pollinators: Am. I. Hot. 82 (1995) 992-999.
M.C., the
1371 Primack R.B., Longevity 16 (1985) 15-37.
flowers,
C. R. Acad.
of individual
Sci. Paris,
Sciences
de
pollen depophases in
Kjellberg F., Hossaertlength of fig receptivity, Annu.
Rev. Ecol.
la vie / Life 1998.321,
Sciences 789-796
Syst.
des
Population
sciences
biology
/ Elsevier.
f Biologic
des
Paris populafions
Obligate mutualism between Trollius eurOpaeus and its seed-parasite pollinators Chiastocheta flies in the Alps Mtitudisme obliptoire entre Trollius europaeus et sespollinisateurs pmusites de pines dzns /esAlpes N icolas Jaeger, Laboratoire
de
(Received
18
Laurence
biologie May
des 1998,
Despr&*
populations
accepted
d’altitude, after
revision
CNRS-UMR 21
August
5553,
BP 53,
38041
Grenoble
cedex
1998)
Abstract - Trolhs europaeus (Ranunculaceae) is involved in a mutualistic interaction with several species of Chiastocheta flies (Anthomyiidae) that are both seed predators and pollinators. In the present work, the pollination biology of T. europaeus and its association with Chiastocheta were studied for 3 years in six populations along an elevational gradient in the northern French Alps. We showed that T. europaeus is mainly xenogamous and Chiastocheta represented 90 % of all visitors. We suggest that almost all seed production was achieved by these obligate seed-parasites. Despite high variability in Chiastocheta activity, the pollination service they provided was high and reliable in all populations during this 3-year study and the seed set was not pollenlimited. The ability of T. europaeus to extend flower longevity during rainy periods and a long stigmatic receptivity in the absence of pollinators may help to explain the high female reproductive success observed at all elevations. (10 Acad6mie des sciences / Elsevier, Paris.) Trollius
europaeus
/ Chiastocheta
/ mutualism
/self-incompatibility
/ visitation
rates
/ pollination
R&urn6 - Trolh europaeur (Ranunculaceae) est engage dans une inter.lction mutualiste avec plusieurs esptces de mouches du genre Chiastocheta (Anthomyiidae) qui sent B la fois des pollinisateurs et des parasites de graines. Nous avons &udie la biologie de la pollinisation du trolle d’Europe et son association avec les Chiastochkes pendant 3 ans dans six populations du nord des Alpes frangaises ktagees le long d’un gradient alticudinal. NOLIS avons montrP que le trolle d’Europe est essentiellement allogamc et que les Chiastochktes reprksentent 90 % des visites de la fleur. Nous suggkons que la production de graines est essentiellement assuree par ces parasites de graines spCcifiques. Bien que I’activite des Chiastochktes soit t&s variable, les taux de pollinisation sont klev& dans toutes les populations pendant ies trois an&es d’ktude et la production de graines n’est jamais 1imitPe par le transfert de pollen. La capacitk du trolle j allonger sa duke de floraison pendant les Cpisodes pluvieux et la longue rkceptivitt stigmatique en cas d’absence des pollinisaleurs pourraient contribuer g expliquer le bon succ~s reproducteur femelle du trolle. (0 Acadtmie des sciences / Elsevier, Paris.) Tr0Uk.s
Note
europaew
communicated
*Correspondence E-mail:
/ Chiastochez~
by Claude and
/ mutualisme
I auto-incompatibih2
Combes
reprints
[email protected]
C. R. Acad. Sci. Paris. 1998 321,789-796
Sciences
de
la vie
/ Life
Sciences
/ faux
de visite
/ pollinisation
09,
France
N. Jaeger,
L. Despres
Version
abrdgde
Les mutualismes entre une plante et un insecte pollinisateur dont les larves se developpent au detriment des graines de la plante sont rares et generalement obligatoires: la plante depend entierement de l’insecte pour sa reproduction et reciproquement. En cas de faibles densites de l’insecte mutualiste, la capacite B l’autofecondation ou des strategies visant a attirer des pollinisateurs alternatifs peuvent etre selectionnes. Nous avons Ptudie l’interaction entre le trolle d’Europe ( Trollius europaeur, Ranunculaceae) et six especes de mouches Chiastochetes (genre Chimtocheta, Anthomyiidae) le long d’un gradient altitudinal (six populations a 1 000, 1 600 et 2 200 m) pendant trois ans dans le nord des Alpes francaises. La capacite du trolle a s’autofeconder a ete testee par ensachage des fleurs : 35-45 % d es individus sont incapables de produire des graines et 80-90 % des individus realisent une production de graines inferieure a 20 Yo en autofecondation ce qui permet de caracteriser l’espece comme allogame. Nos releves montrent que 90 % en moyenne des visiteurs du trolle sont des Chiastochetes. Les autres visiteurs observes appartiennent a differents ordres (Dip&es, Coleopteres, Hymenopteres). Ces visiteurs occasionnels presentent gene-
1. Introduction The between
sively genus, opment
to habitat
most extensively studied cases plants and pollinating seed-parasites
fig wasp [l-3], globeflower-globeflower Yucca and Ficus
Several species involved in
yucca-yucca moth 14, 51 and the fly interactions 161. Most of the species and the globeflower are exclu-
been assumed to be obligate: the without its associated pollinator
790
penetrate the globenectar and pollen 191 eggs on the surface of the flower. The larvae fraction of the seeds.
showed that this interaction in Finland: the plant is strictly flies are the exclusive pollinators.
ulations of T. europaeus those found in Finland.
(Ranunculaceae) with Chiasto-
In Europe, the globeflower with eight Chiastocheta
species ISI. Male and female flies shaped flower where they consume and where they mate. Females lay the carpels and passively pollinate of all species develop by eating a [6]
plant and
of its geographical pollinator may not for the plant, as was
of the genus Trollius a mutualistic association
theta flies (Anthomyiidae) [8]. Trollius europaeus is associated
Pellmyr mutualism ible and
mutualism are the fig-
the
vice versa. However, in some parts range, interaction with the associated be as obligate as is generally assumed shown in the case of Yucca [7]. are
of
associated with a single pollinating species or which in return depends on the plant for the develof its larvae. As a consequence, such associations
have frequently cannot reproduce
ralement une faible mobilite d’une fleur a l’autre ou visitent la fleur lorsqu’elle est sur Ie point de finer et ne participcnt done pas significativement a la pollinisation du trolle. Ces resultats suggerent que la production de graines du trolle d’Europe est essentiellement assuree par les Chiastochetes. Les densites en Chiastochttes dans chaque population et chaque an&e ont et& estimees par la moyenne du notnbre d’ceufs pondus par fleur. Cette moyenne fluctue entre 2.,62 et 16,82, ce qui indique une tres grande variabilite de I’activite en Chiastochetes entre an&es et entre populations. D’autrc part, nous avons observe une forte variabilite des conditions mtteorologiques entrainant une forte variabilite de l’activite des Chiastochetes au tours de la periode de floraison. Pourrant les taux de pollinisation sont tres homogPnes et nos experiences d’addition de pollen montrent que la production de graines n’est pas limit&e par les transferts de pollen. Le trolle semble capable d’augmenter sa duree de floraison quand il pleut et la duke de receptivite stigmatique peut etre tres longue (jusqu’a 12-15 j), au moins en cas d’absence des pollinisateurs. Sous des densites particulierement faibles en Chiastochttes, ces deux mecanismes pourraient Ctre dcs facteurs cl& dans le maintien d’un mutualisme obltgatoire entre les deux partenaires.
is an obligate self-incompatHowever, pop-
in the Alps are very different from They are much smaller in size due
patchiness
and
distributed
along
an elevational
gradient ranging from 700 to 2 600 m. This allowed us to study the pollination biology of T europaeus and the characteristics of its interaction with Chiastocheta under various variation
ecological conditions. of weather conditions
Habitat patchiness and the are likely to induce var-
iability in Chiastocheta activity. tion for self-compatibility and/or pollinators when Chiastocheta
This could lead to selecstrategies to attract other provide unpredictable or
inadequate service 171. Studies on other plant species suggest that a strong limitation of reproductive success due to poor and/or variable pollination activity can result in selection tion was pollinator
for self-compatibility [lo, 1 I] and self-pollinareported in T europaeus [I 21. At high elevation, species diversity is likely to be reduced I1 3-l
51
but at an elevation of 1 000-l 500 m, many insects such as bees, wasps, syrphid flies and bumblebee queens are present in globeflower populations and hence are liable to affect slightly
pollination. bowl-shaped
In all other Trollius species, flowers allow access for
flat or many
potential pollinators ]8]. The closed flower T. europaeus is likely to be responsible for exclusivity the interaction by preventing most other potential nators from T. europaeus the association cific
In the present
polli-
entering the flower. However, the globe of can be more or less tight [16] suggesting that with Chiastocheta may not be highly spe-
throughout
interaction is a case
of of
its geographical paper,
between of obligate C. R. Acad.
we examine
range. the possibility
Trollius europaeus mutualism along Sci. Paris, Sciences
that
the
and Chiastocheta an elevational grade
la vie / Life Sciences 1998.321.789-796
Troliius
dient in the Alps by answering two T. europaeus self-compatible? and b) affect pollination of T. europaws! We lination rates and by pollen transfer.
we test for limitation
2. Materials
questions: a) is do other insects also analyse polof seed
production
and methods in the Massif de la Chartreuse and (northern French Alps) in May-July
1995-l 996-l 997. Six populations of T. europaeus were selected in the lower part (Cherlieu, 950 m and Cottaves, 1 050 m), in the middle part (Crolles, 1 550 m and Som, 1 550 m) and in the LX, 2 100 m) of the several weeks
upper part elevational
thousand from May
(G‘tlihier, 2 300 m and range. Each population
individuals and to July depending
flowering on eleva-
Trollius eul-opaeus L. is a hermaphroditic arctic-alpine species (Ranunculaceae). In our populations, it was visited by six Chiastocheta species (Anthomyiidae): C. drntifera, C. inermella, C. maoopyga, C. rotundiventris, C. setifera and C. trollii (described in j 17) and II RI, taxonomy in height composed
of the flies following 11 911. The plant is 0.2-l m usually produces a single yellow flower of 6-l 5 sepals enclosing 1 O-1 5 nectariferous
and
staminodia 7: europaeus We counted number
and the occasionally the number
of
pollen
reproductive produces of stamens
grains
in
organs. However, two or three flowers. on 46 flowers and the
four
anthers
of
14
flowers
using the method described by Atlan et al. 1201 at Cherlieu in 1995. Each year and in each population, we counted the number of carpels and we assessed the number of ovules by randomly selecting five carpels 161 on 38-95 flowers. Individual Results for
flower populations
lifespan and
and years)
anther were
dehiscence estimated
(set by tag-
ging 16-120 flowers per population on their first day of flowering and checking for sepal retention and anther dehiscence each day. Stigmatic receptivity was tested by experimental cross-pollination at Cottaves, Crolles and Galibier in 1997: 122-l 61 flower buds per population were emasculated and enclosed with nylon mesh bags. Ten flowers were hand cross-pollinated on the 1 st day of flowering, ten other flowers on the 2nd day, etc., until 12th or 15th day (depending on the population;t mixture of pollen from S-l 0 donors, and checked set. Seed
production
The breeding production by
indicates
system pollen
stigmatic
and were
potential investigated
with a for seed
receptivity, limitation of seed hy conducting
then own
fllowers pollen
were (hand
pollen flowers
from per
5-10 donors to 1’3-20 population on each day
C. R. Acad. 1998.321,789-796
Sci. Paris,
Sciences
de
la vie
/ Life
Sciences
with their 13-24) or left
naturally pollinated of flowering. Within
each population, all treatments were conducted within a week. Atl flowers were collected and analysed 2-3 weeks after the end of their flowering when viable seeds are easy to distinguish and before numbrr selecting
from non-fertilised predation by larvae.
ot’ seeds per five carpels
ovules C)n
or aborted each flower,
carpel was assessed 161. Throughout the
seed s-t of a flower dividecl by the mean population.
is the number
by present
seeds the
randomly paper,
number of seeds per of ovules per carpel
carpel in the
In e,lch population, we counted Chiastocheta and all other insects penetrating ten flowers during 18-63 periods of 10 min under diverse weather conditions (except rain), times of day (between 0Y:OO and IS:00 hours) and dates n 1995. was estimated (17 = 411-95
In each population, mean number
by the
flowers
Frequencies egg counts
per
were were
Chiastocheta of eggs laid
population!
arcsine square
in 1095-I
per 996--l
square root-transformed root-transformed to
density flower 997. and satisfy
assumptions for analyses of variance. Year, treatment, elevation, population (nested in elevation) and interactions were considered as fixed effects, and type III mean squares were used yses ‘Nere carried (I 090).
in the analyses of variance. out using SAS statistical
All analprograms
3. Results Flowers were 1 O-6!,, n = 909
composed flowers)
of .31.2 containing
* 9.6 carpels 11.6 +- 1.6
(range ovules
each (range 5-18, n = 855 flowers) and 163.9 + 23.2 stamens (range 11 7-247, n = 46 flowersj containing 6 843 + 2 014 pollen grains each (range 2 225-l 1 120, n = 14 flowers). Our estimates ranged from 2 000 to 4 000. f’loVvers effect
of
lasted year 102.7;
from
q
longevity For example,
of
4 to 16 d. There
pollen/ovule was
ratio
a significant
(F,, J,o=. 547.9: P = 0.00011, elevation I’ = 0.0001 1, population (F i, J,. = 16.5;
flower days.
plants. We first to produce seeds
enclosing 40 flower buds were bagged,
from 5-10 donors (hand cross-pollination, n = 40-58). Seed set under natural pollination was assessed by randomly collecting 38-95 flowers per population. Pollen limitation of seed set was tested by adding a mixture of
ments showed
on different was not able
mutualists
self-pollination, n = 8-23). emasculated and bagged, then with a mixture of pollen
(F 2 JIo= P = 0.0001 !, year x elevation and year x population IF, flowtr longevity. In several
performed T europaeus
and Flower
its obligate
either hand-pollinated self-pollination, n =
five treatments (see Results for populations and years): spontaneous self-pollination, hand self-pollination, hand cross-pollination, natural pollination and addition of pollen. Only primary flowers were selected so that treatwere that
and
without pollen by emasculating buds with nylon mesh bags.
untouched (spontaneous Other flower buds were flowers were hand-pollinated
The study took place the Massif du Galibier
contained lasted 3-5 tion.
europaeus
to
(F, 3,,, = 307.4; P = 0.0001 i .rlo = 15.0; P = 0.0001) on populations, we observed
increase with the number of it was much longer at Lac in 1996
rainy than
791
N. Jaeger,
L. DesprGs
in any other populations owing to a l-week period
during of rain.
these
3 years
itable
Seed higher
I)
5.7; Anther dehiscence lasted 6.3 + 0.8 at Som (n = 20), 7.9 9.4 f 1 .I at Cottaves (n = 50) Calibier vations
were hand
Stigmas remained of flowering,
Table
flower
II is the
20 %. Seed set under ranged from 3 to
a decrease from bagged flowers
that
longevity
the 8th to were able
per population
in 1 YYS, 1 YO6 and
able,
than
each
1 YY7:
mc’an
under I. The
oi days
m
Crolles
3.0
f 0.9
Ill = 201
1 600 m 2 200m
SO111
Lat
4.9 4.6
+ 0.7 f 0.6
I/J = 211) (n = 16)
Galihirt
5.0
f 0.6
(n = 1 Y)
Flowers
were
seed
set below
hand effect
self-pollination of treatment
whatever
+ standard
in = 191 111 = 201
checked
for
7.0 7.2 7.1 15.2
+- 0.4 f
0.6
* 0.4 k 2.3
20 %. !F,
was
the year
retention
each
-liIcI = 723.1; liignificant in
(l-tests).
Seed
set
drviation. I907
(/I = 231 f/J = 201
7.3 8.6
(R = LO) (II = 201
6.9 f 1. I !n = 20) 6.6+0.71;,= 1101
~p~\l
any seeds individuals
was, significantly
1096
1 600
of flowersl.
able to produce and among the
cross-pollination
tested
1905 6.0 + 0.8 3.5 + 0.7
hand
population
number
not
80 ‘%, had
set under
higher
Cherlicu Cott
(number
flowers were self-pollination
f3 = 0.0001
m m
m
were
Seed
cross-pollinated at least until Seed set showed dramatic and 15th days.
PolIuldtions
size
seed set helow per population
35 ‘% of the under hand
1 000 1 000
sample
able, 90 % had self-pollination
for 12-l 5 d after the first the absence of pollinators
Elevations
2 200
self-pollina-
receptive at least in
seeds when hand day of flowering. on the 13th, 14th
I. Mean
spontaneous
15 ‘%, (table II) with a significant effect of population P = 0.03) and year x population (F ‘,, LOci= 2.43; 3.65; P = 0.002) but no significant effect of year (Fh 10’) = (FL, Loci = I .5; P = 0.22) (F , l,jcI = 1 .38; P = 0.241, elevation ancl year x elevation (F,, J,,4 = 0.18; P = 0.83~. About
(figure 7). Although there was the 9th days, the emasculated to produce the 12th decrease
set under
ir = 0.73; n = 210; P < 0.01). Anthers during rain and there was a rapid presas soon as weather conditions became
favourable.
day
1). Seed
significantly (F,, LcIcI =
0.901, year x elevation iF,, ,,,) = 0.65; P = 0.421 and year x population (F,, qiI = 0.07; P = 0.78). About 45 “% of the flowers were not able to produce any seeds under spontaneous self-pollination and among the individuals that
among elepopulations
(F,, , 79 = 24.6; P = 0.0001). Pollen presentation was gradual with the outer anthers dehiscing first. Anther dehiscence occurred throughout flower lifespan with a good correlation between the end of anther dehiscence and flower senescence were not dehiscent entation of pollen
P = 0.01
hand self-pollination was spontaneous self-pollination
tion per population ranged from 3 to 7 % (&h/e I/j with no significant effect of year (F,, ,,,) = 0.28; P = O.J9), elevation P = 0.06), population (F,, ‘),, = 0.28; P = (F I 00 -- 3.57;
from 5 to 11 d. It was + 1.5 at Cherlieu rn = 201, and 6.9 + 0.8 (n = 120) at
in 1997 with a significant difference (F,, ,79 = 65.61; P = 0.0001) and
set under than under
8.6 day
from
the
first
day
+ 1.4 In = 201 f 0.5 C/l = SO)
t
1.3 UI = 201
of anthesib
(= first
day
of
flowering).
/Cottaves 1
iCrolles I
80% 70% 60% 50% 40% 30% 20%
Day Figure
1. Determination (0 = 122) in 1997.
oi stigmatic
The duration of stigmatic receptivity 2nd, etc., or 15th day oi flowerlng.
792
receptivity
by experimental
was estimated Seed production
from seed indicatcl\
hand
of flowering (.roi~-l,o/lination
at Cottaves
(n = 1 hl I, Crolles
(17 = 141 I ancl
set oi rmascul,ttc~d and haggrsd flowc,rs that wcsre hand cross-pollin,ltcd stigmatic r(‘c eptivity. Vertical bars are standard deviations.
C R Acad.
Sci. Paris, Sciences
Glibier on the Ist,
de la vie / Me Sciences 1998.321,789-796
europaeus
Trollius Table
II. Mean
seed
set per
population
under
Treatments Spontaneous
self-pollination
Spontaneous
95
self-pollination
96
different
Cottaves
7 f; 1 0 ‘X, Ii,=231 -
7 f 9 ‘%I in = 17)
and
1997:
mean
i standard
Crolles
deviation.
Som
Galihier
4 + 7 ‘!% In = 141
111 = 241
(n = 14)
(f? = 131
111 = 20)
(n = 201
74 * 22 ‘%I In = 54’1
67 + 27 ‘%a i/J = 54)
72 * 13 %
6.i It 20 ?%a
72 * 23 “4,
I/J = ,581
If1 = 401 NO + 12 ‘!U
(n = 501 69 t 18 “%,
pollination
95
8 1 1 1 5 ‘%,
8 I f 19 ‘%>
90 i
Natural
pollination
96
(n = 95j 75 i 19 ‘%,
t/1 = 381 74 i 1 5 ‘%I
(11 = 60) 74 + 16 ‘%,
Natural
pollination
97
Y7
ot flowers). per camel
under hand cross-pollination 63 to 74 % (table //) with
in = 50)
in = 501
80 Yk 1 7 ‘%,
7 1 i 1 Y ‘% I” = 5 5 ‘I
at Cottaves, and 0.19 at
in set
under natural pollination per population ranged from 56 to 90 ‘% (table /I) with a significant effect of year (F,, o,r, = 49.31; P = O.OOOl), elevation iF, c,,,, = 38.9; P = 0.0001) and year x elevation (F, ‘,,r, = 5.7; P = 0.0001) Ibut no sig(F,, ‘,,r, = 1.73; P = 0.16) and 1.36; F’= 0.22). It was high and during these 3 years: it was
higher than SO ‘%, for 80 ‘%I of individuals 70 “io for 50 % of individuals. Seed
set
under
higher than under P = 0.99). The effect
pollen
addition
was
natural pollination of treatment was
and not
higher
8.5 2 15 % (11
on primary of ovules
Among Cherlieu records),
significantly
12 “i,
I/? = 46) 5 6 +- 1 h ‘% In = 50) 72 f 20 ‘5,
(n = 40) 5.3 f 1 9 ‘!% in = 20) -
k 1 5 ‘I/;, II? = 19)
78 + 2 3 ‘%
(n = LO1
LO)
Seed and
set oteach flower was given as a percentage.
calcu-
all visitors, Chiastocheta represented 91 t 16 “XI at (n = 57 records), 85 + 31 % at Cottaves (n = 60 77 + 26 ‘%, at Crolles in = 18 records), 90 + 16 %
at Som (n = 57 records), and 94 + 8 ‘XI at Galibier itant dlffercnce P = 0.10) and (f (, ~~jr, = .67;
93 + 8 ‘%, at Lac in = 60 records) (n = 63 records) with no signif-
among populations P = 0.1 7).
to Iiymenoptera, small Coleoptera
elevations for Other
this visitors
(F,, jIj0 = 2.27; percentage observed
Diptera or Coleoptera. At all (Oedemeridae, Nitidulidae,
Cleridae, Cerambycidae and Staphylinidae) were observed inside the flower. At high elevation, only Diptera and C‘oleoptera were observed to enter into the globe of T. europa~s. At low and intermediate flies were able to enter old flowers became less tight, some vespid wasps sometimes observed to crawl bumblebee queens (5ombu.s visit 7. europaeu5 flowers.
than
(F,, ;rlli = 0.01; not significant in
=
flowers ot ditterent plants. L)er carpel in the population
belonged elevation,,,
also significantly (F,, ,,?s = 2462.9;
I’= 0.0001). The effect of treatment was significant each population tested whatever the year (t-tests). Seed
nificant effect of population year x population (F,, ‘,,r,= reliable in all populations
50)
49
+ 2 1 ‘X, (rl = 201
and populations (F,, lol index (SC1 = seed set set under hand cross-
was
=
!rJ = 17)
64
per population ranged from no significant difference among
pollination self-pollination
(11
10 f
in = 501 f 16 ‘“;I
In = 501
pollination; 121 1) was 0.14 at Cherlieu, 0.17 0.20 at Crolies, 0.0’3 at Som, 0.06 at Galihier Lac in 1995. Seed set under natural higher than under hand
ho
74 t I 6 ‘I/;, (n = 50) 7.1 * 2 ; “,’,I,
Treatments were performed dividrd hy the mean numhcr
elevations (F?, lo-l = 2.51; P = 0.08) = 1.49; P = 0.22). Self-compatibility under hand self-pollination/seed
14 ‘%,
(n=ll1
(n = 50)
in = 181
inumber of seeds
in = 201
110 -t 1 7 ‘!% 111 = 50 I 7’) .+ --_ 3 ‘, “y 0 t32 2 23 “%I (n = 20)
11 is the sample size lated as the number
(iJ = 101 11 *15’io
in = 8)
6 f; I 1 ‘%>
1 6 ‘X,
Natural
addition
3 T!z5 “4,
(II = 19) 8 f 1 3 ‘%
96
Pollen
.3 + 6 “/ (I
(II = 1 51 1 + h ‘%>
In = 241 4 t j ‘%
self-pollination
96
i + 4 ?”
(17 = 17) I 0 t 9 ‘%,
Hand
addition
Lac
!n = 101 4 & .y “‘1,I)
11 i
Pollen
mutualists
2 + 4 “/O
95
95
1996
its obligate
12 + 1 I ‘%I
self-pollination
cross-pollination
in 1995,
Cherlieu
Hand
Hand
treatments
and
5.8 2.8
inside
elevations, when iVespu/a the
soroemsis)
syrphid the globe sp.) were
globe and a few were observed to
During a period of 10 min, ten flowers were visited by + 5.0 Chiastocheta at Cherlieu (n = 57 records), + 1.1 at Cottaves (n = 60 records), 4.4 k 3.8 at Crolles
(n = 18 records), 10.7 13.6 + 7.11 at Calibier
+ 7.7 at Som (n = 63 records)
(n = 57 records), and 20.2 f 9.5
each population tested whatever the year (t-tests). Seed set under pollen addition per population ranged from 49 to 85 ‘% ([ah/r II) with a significant effect of year (F,, ,AJ =
(n = 60 records) at Lac with a significant difference among elevations (F,, ~o~j = 108.1; P = 0.0001) and populations (F-r, (r,‘, = 15.3; P = 0.0001). Mean number of
6.4; P = O.Ol), elevation (f ,I, ,j4 = 3.17: f’ = 0.041, population (F, ,L4 = 7.9; P= 0.06) and year x elevation (F,, ,LJ = 7.87; P = 0.006) hut no significant effect of year x population (F,, ,jd = 1.63; P = 0.20).
Chiastocheta eggs laid per flower showed great variation ranging from 2.62 to 16.82 (tab/t> 111) with a significant effect of year (F, Lj4, = 66.1; P = O.OOOl), elevation P = O.OOOl), population (F,,,,,, = 17.5; iF .!, ‘JJ I -- 81.9; P = 0.0001 i, year x elevation (F, cl1, = 21.6; P = 0.0001) and year x population (F,,, .1,,) = 1.1.9; P = 0.0001). The
Chiastocheta Depending on C. R. Acad. 1998.321,789-796
were the main the population,
SCI. Paris,
Sciences
de
visitors at all elevations. 2-6 species were found. la vie
/ Life
Sciences
N. Jaeger, Table
L. Despres
III. Mean
number
of Cl~ia~toci~eta
Populations
eggs
Crolles
Soni Lac
In 1995,
Galihier
5.20 i- 3.03 4. 18 t 2.98
(I) = 501
4.92
+ 4.22
(17 = .s[)l
.3.96
3. 1.71
l/J = 501
5.36 8.57
* 3.04 i 4.84
3.74
i- 1.89
111 = 501
7.54
i 5.52
f/l = i0) (n = 40) ki = 55)
,Ifter
the end
of their
* 9.00
in = 501 C/~i,~stoch~~& after hatching.
at Crolles,
Som,
eggs
were
Lac and
counted
Gal-
produced by outcrossing. Self-comlow (O.O:-0.2) and consistent with
has a gamctophytic self-incompatibiland Despr&; unpublished data) like Ranunculaceae 1231. However, in all
populations, some under self-pollination. for their germination
individuals were able to produce seeds Further studies are needed to test ability. Under hand or spontaneous 35-45 ‘%, of individuals produced % of the partially self-compatible
had a seed set under 20 % suggesting be considered as a serious alternative to outcrossing in our populations. insects
affect
pollination
no indi-
that selfing reproductive
is an exclua) G&tovisitors were
unlikely to have a significant impact on pollination. First, many insect species were recorded, but very few individuals of each species were actually observed inside flowers. Second, these occasional visitors were unlikely to pollinate T. europaeus. Coleoptera and Diptera were rarely seen to move from one flower to another. Syrphid flies, wasps or bumblebee queens were sometimes observed at low and intermediate elevations inside flowers of T. curopaeus but our observations suggest that they are also unlikely to affect pollination: bumblebee queens
794
of the
or1 cdrpels
4.04 2.62
flowers
weeks
2-3
+ 2.12 f 2.23
(n = 50) (n = 50) h = 78)
a very short time inside each flower, syrphid often not in contact with stigmas and entered
flowering.
flower when it was 5 or 6 d old (after most pollination occurred) and wasps were never seen to move from
had one
to another. This suggests that there is no other sigpollinator of T. eu/-opaeus. The shape of the seems to efficiently prevent visits of other pollina-
the form interesting c ificity
of a bowl results of this
4.3. Why high and
[ 161. Field concerning
flowers to open
of in
studies there should provide the maintenance of the spe-
interaction.
is female reliable?
Pollen-addition
reproductive
never
success
led to higher
of T. europaeus
seed
set than
natural
pollination suggesting that pollen transfer did not limit scecl production 1241. Resource limitation or other factors such as pollen-pistil interference and post-zvgotic abortion could be responsible for the undeveloped seeds [25271. There is no reason to suspect limitation of seed production by pollen in 1995, since seed production was JS high or higher than in 1996 l)opulations, seed production limited
by pollen
transfer
and 1997. appears during
these
Hence, in all our not to have been 3 years.
We observed variation in Chiastocheta activity within flowering season in all our populations due IO great variation in weather conditions. During periods of rain no Chiastocheta flies were observed in the flowers. Moreover, there was a significant decrease in Chiastocheta visitation rates due to cloudiness (Jaeger and Despres,
of T. eoropaeos?
Trollius europaeuslChiastoci,eta interaction sive mutualism in our populations because theta were the main visitors and b) other
spent were
5: 3.08 in = 50) 2 2. I4 in = 501
tors. In some parts of its range (Poland), 71 europaeus (var. transsilvdnicus) are reported
self-compatible?
land. T. europaeus ity system (Jaeger other species of
Do other
-
(I1 = 501
i 1 1 .OY !n = 60) + 5.92 \n = 461
the high value of polleniovule ratio (2 000-4 000) typical of xenogamous species 1221. The low seed production under self-pollination suggests that the plant is selfincompatible, consistent with Pellmyr’s study 161 in Fin-
4.2.
1997
f 4.39
Seed set never exceeded 15 “/u under self-pollination whereas it reached 74 “% under hand cross-pollination and 90 “% under natural pollination suggesting that most
viduals cannot strategy
deviation.
6.92 16.00
4. Discussion
self-pollination, seeds and 80-90
+ standard
1996
flower nificant flower
were was
mean
4.08 1.04
was significant
seeds (if not all) patibility index
1997:
(il = 95) In = 401
10.t1.2
Is T. europaeus
and
+ 1.57 + 2.53
n is the sample size (number of flowers). Empty egg shells remain on carpels even
4.1.
1996
4.12 2.95
7.41
of year (t-tests).
per population
1995
C:herliru Cottnves
effect ibier
Iaid/tlower
flies the
unpublished data). Other studies report no or few insects on rainy days 1281 and show strong effects of weather on visitation ference among
rates 129-31 in the mean years, elevations
difference populations
1. There was also number of eggs and populations
a significant diflaid per flower and a significant
in the fly visitation rates among elevations and reflecting variation in Chiastocheta activity
161. This could be due to variation ,Ind possibly habitat patchiness We showed % europaeus Chiastocheta.
that almost was achieved High pollination
in weather 1321.
conditions
all seed production of by pollination service of levels achieved by Chias-
tocheta, provided that they are common in I europaeus populations, could explain why the plant has not evolved towards self-compatibility or strategies to attract alternaC
R. Acad.
Sci.
Parls.
Sciences
de
la vie / Life Sciences 1998 321, 789-796
iroilius tive pollinators. Moreover, number of Chiastocheta service. This suggests that seed predation for similar variation high and
in Chiastocheta not pollen-limited
populations varied in the eggs for equivalent pollinator some populations suffer higher pollination levels. In spite of activity, seed production was in all populations. Extension
many species should sufficient pollen has populations
europaeus
have been
where
and
its obligate
mutualists
flowers adapted to wait until transferred to the stigmas. In
Chiastocheta
activity
is particularly
low and unpredictable, these two traits for maintenance of obligate mutualism.
could
be critical
of flower longevity under rainy conditions and long stigmatic receptivity in the absence of pollinators could allow T. europaeos to minim&e negative effects of this variability in Chiastocheta activity. Other studies suggest that long
in conclusion, almost all seed production is achieved by pollination service ofChia.stoche~~. Selfing cannot be a serious alternative reproductive strategy to outcrossing and cross-pollen is likely to be exclusively transferred by
flower could
Chiastoch~ta whatever the elevation. In that sense, the association between T. europaeus and Chiastocheta can bc considclred as an obligate mutualism in our popula-
longevity compensate
and
stigmatic receptivity for low or unpredictable
rates 115, 301. Robertson the dehiscence of anthers report increased duration phases, deposition
respectively, are low
in alpine plants pollination
and Lloyd 1331 found delay in in periods of rain. Other studies of staminate and pistillate
when 134-361.
pollen removal and According to Primack
Acknowledgements: We thank Patrice Colcnson, ante. WC thank Irt’ne Till-Bottraud for help with Raymond, Gordon Luikart and John Thompson (Ph.D. fctllowshlp to N.]. and grant AC(CSV71
pollen 1371
D.H..
How
Rrv.
Lcol.
Syst.
10 / I Y~YI 1 1-51.
121 Bronstein J.L.. Seed prrdators as mulualisb: ecology and the fig/pollinator interaction, in: Bernays E (ec1.1, Insect-Plant (Vol. IV). CRC Press, 1992, pp. l-34. 131 Anstett M.C., tars: cvolutlonary 12 I 1996) 94-99. [4J Addicott interaction 494.
J.F., Variation between yuccas
in the costs and and yucca moths.
Iwneflti of mutualism: Occolog~,~ 70 (19861
Linhart glauca Am.
191 Hagerup O., 1956, 1,. 231).
Peterson
Y.B.. Reproductive consequences of (Agavaceae) and ~ege/icu/a yurc-ax//~ J. Bot. 81 (1994) 815-ii25.
V., Botanisk
Atlas,
and Biol.
Munkegaard,
I1 1 i Schoen in C;/yoi~e Evolutlon45
D.J., Brown H.D., Whole arg)wd and C. c-/andcstin.l 119Yll 1651~ 1665.
il 21 Tutin /I. L 10.
T.G.,
Europaw,
Press,
eww
(oadaptaJ. Linnean
and Espletia
self-pollination of autogamy,
Cambridge,
C.
R.
Acad.
1998.321,789-796
Harper K.T.. Booth Am. Mitil. hat. 120
Sci. Purls, Sciences
C.M., 11Y081
Elevational (25-3 IO.
de la vte / Life Sciences
distribution
K.A.. 30.
I I71 ( 01 in J.lI.. da1~1, f’wc. Roya
rainy periods explaining this
Eiiicient
The genus Entomol.
pollinalitrn
ot
activity,
seed Extension
and long result.
Cl?iasfoc-iwr,~ Sot. London
,Ilpine
proof
stigmatic
in Lintiwr ILY-376.
11’11 blichrlwn J.W. Lctic~rstc~llt.
oi the Anthomyiidae 11 11 9i35) 37-65
V., A revision Stcwslrupia
Iplants,
Nature,
iY1
t’okorny !DIpwra: AnthomviiiB: L i 11Y5.1) c15m102.
11 81 t iertmg 1v., Anthomyiidar, arktlschc n Rwion, 1976, pp.
C. :(YI.I, Die
Fliegen
il)lpteral
der
Palar-
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