Plant Syst. Evol. 232: 63–71 (2002)
Self-pollination in Euphrasia willkommii Freyn (Scrophulariaceae),
an endemic species from the alpine of the Sierra Nevada (Spain)
J. M. Gómez
Departamento de Biologı́a Animal y Ecologı́a, Facultad de Ciencias, Universidad de Granada,
Granada, Spain
Received May 2, 2001
Accepted December 6, 2001
Abstract. The reproductive ecology of Euphrasia
willkommii (Scrophulariaceae), an endemic species
from the Mediterranean alpine environments of
the SE Spain, has been experimentally studied
during two reproductive seasons. The flowers of
this plant species were visited by very few insects
belonging only to two generalist taxa, thrips and
ants. Nevertheless, reproduction is not pollen
limited in E. willkommii. Hand-pollinations demonstrated that this plant species is capable of
selfing, reproductive success being similar in autogamous and allogamous crosses. Moreover, pollinator-exclusion experiments also showed that,
under natural conditions, this plant relies predominantly on selfing, seed production being similar in
presence or absence of pollinators. Selfing in
E. willkommii is presumably an ecological mechanism to ensure successful reproduction in a harsh
environment where pollinator availability is
extremely low.
Key words: Euphrasia willkommii, Scrophulariaceae,
Mediterranean high-mountains, pollinator abundance, reproductive assurance, self-fertilization.
Introduction
Self-pollination is a common trend in angiosperm evolution (Holsinger 1992, Schoen et al.
1997, Barrett 1998). In some plant species,
selfing has evolved to allow reproduction when
conditions for outcrossing are unfavourable,
this phenomenon known as reproductive
assurance (Barrett 1998, Holsinger 2000, Aarssen 2000). According to the reproductive
assurance hypothesis, the fitness advantage of
selfing comes from increased success with
respect to outcrossing (Aarssen 2000). A main
ecological factor that can decrease outcrossing
advantage and thereby promote selfing in many
plant species is the shortage of pollinators
(Erhardt and Jäggi 1995, Kampny 1995,
Navarro and Guitián 2001, Fausto et al. 2001).
In Scrophulariaceae, many species have a
mixed mating system in which selfing is
assumed to provide a reproductive assurance
when pollinators are scarce (Dole 1990, 1992;
Ortega Olivencia and Devesa 1993a; Kalisz
et al. 1999). For example, long-tubed flowers
of Ourisia spp. (Scrophulariaceae) self spontaneously when pollinators are unavailable
(Arroyo and Peñazola 1990). Similarly,
delayed selfing occurs in Collinsia verna when
there is a limitation of pollinators (Kalisz et al.
1999). The type of environment in which the
plant inhabits, by determining predictability
and abundance of pollinators, can indirectly
affect the frequency of selfing. In fact, several
alpine and subalpine Scrophulariaceae, where
64
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
pollinators are scarce, are predominantly autogamous (Kampny 1995).
Euphrasia willkommii Freyn (Scrophulariaceae) is an alpine species endemic to the Sierra
Nevada high-mountains (Spain). Here, as in
most alpine environments, conditions are especially harsh for plant life, the vegetative
period being very short, since the area is
covered by snow many months of the year.
In addition, because the zone also has a
Mediterranean climate, strong summer
droughts constrain the growth and reproduction period of the plants while limiting the
diversity and abundance of the floral visitors
(Gómez and Zamora 1992, 1996). In this
study, I experimentally explore the reproductive ecology of E. willkommii in this severe
environment. Specifically, I (1) quantify the
abundance and composition of the floral
visitor assemblage, (2) experimentally determine the breeding system of the plant, (3) test
whether pollinators are necessary for seed
production, and (4) test whether reproduction
in this plant is pollen-limited.
Methods
The plant species and the study site. E. willkommii is
a tiny (up to 6 cm high) perennial herb inhabiting
wet as well as dry high-mountain meadows (above
2500 m a.s.l., Molero Mesa et al. 1992). It flowers
during the summer, between June and July in the
study area. Flowers are pink-purple with some
yellow spots in the bottom petals. The corolla tube
is short and the flower is open with lobes spreading
weakly actinomorphically (Fig. 1). Fruits are capsules containing from 4 to 10 seeds.
The study was performed during 1995 and
1996 in a 2-ha plot located at 2600 m a.s.l. in the
Sierra Nevada National Park (Granada, SE Spain).
The study area is a dry Mediterranean alpine
habitat inhabited by scattered stunted shrubs and
cushion plants belonging to the species Thymus
serpylloides Bory, Hormathophylla spinosa Küpfer,
Alyssum purpureum Lag. & Rodr. or Arenaria
tetraquetra L., and by many species of perennial
herbs, notably, Mucizonia sedoides (DC.) D.A.
Webb, Dianthus subacaulis Vill, Sempervivum minutum (Kunze ex Willk.) Nyman ex Pau in Bol.,
Fig. 1. Schematic view of a flower of Euphrasia
willkommii Freyn. a corolla width, b central petal
length, c lateral petal length, d corolla depth
Sedum anglicum Hudson subsp. melanantherum
(DC.) Maire, and Lotus glareosus Boiss. & Reuter.
In this habitat, E. willkommii is very abundant,
forming populations with hundreds of individuals
growing very closely.
Reproductive traits. The reproductive traits of
E. willkommii were studied by tagging 20 plants in
each of the two years of study, and recording the
number of flowers, fruits and seeds produced by
each plant. The parameters used to estimate
reproductive success were number of fruits produced per plant (fruits/plant), percentage of flowers
ripening to fruit (fruit set), percentage of ovules
ripening to seeds in each ripe fruit (SO ratio), and
overall number of seeds produced per plant (seeds/
plant).
The floral morphology was quantified from 60
arbitrarily selected individuals in 1996. Measurements (in mm), taken in one flower of each plant,
were corolla width (from the apex of the two outer
lateral petals), length of the central petal, length of
one lateral petal and depth of the corolla (from the
tip of the upper petals to the calyx, see Fig. 1). To
quantify nectar production, I covered all the
flowers produced by 30 plants in 1995 and 40
plants in 1996 (350 flowers in total), and tried to
extract the nectar with capillary micropipettes.
Floral visitor censuses. I determined the composition and abundance of the floral visitor assemblage during 1995 and 1996 by counting all insects
visiting flowers of E. willkommii individuals arbitrarily chosen in the study plot during 1-min
periods. I made a total of 5385 1-min censuses
(aprox. 90 hours of observations) evenly distributed from sunrise to sunset, with 85% of the censuses
made during the diurnal period (before 20.00 pm
GMT) and the remaining 15% made during the
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
nocturnal period (between 20.00 pm and 01.00 am
GMT) using moon nights to avoid the use of lights,
which could attract insects and thus alter the results
of the censuses. During the censuses, I stayed about
1 m from the flowering plant, to monitor all the
floral visitors but not disturb their foraging behaviour. Any insect seen on the flowers that could
make contact with the anthers and/or stigma was
sampled. Pollinator abundance is expressed as the
number of insects per plant and per 10 min. I
visually determined the type of food collected by
the floral visitors (pollen vs. nectar).
Experimental study of the breeding system. In
1996 60 plants were tagged and then covered with
mosquito netting which was attached to the soil
surface using Tanglefoot to impede both winged
and wingless insect access to the flowers. All the
flowers produced by 20 plants randomly selected
were pollinated once using pollen from the same
flower (obligate autogamy). The flowers from
another 20 randomly-selected plants were emasculated and hand-pollinated once using pollen from
another individuals growing at least 2 m from the
recipient plant (xenogamy). Finally, the remaining
20 plants were left netted and not hand-pollinated
(spontaneous autogamy). Flowers were pollinated
only once to decrease the number of manipulations
which might affect to the effectiveness of pollinator
exclusions. The experiment was checked every day
until flower senescence to ensure that the exclusions
successfully eliminated insect visits.
At the beginning of the experiments, I counted
the number of flowers per plant, which was
statistically
similar
between
treatments
(F2,57 ¼ 0.72, P ¼ 0.49, being 3.8 ± 0.5 for plants
with spontaneous autogamy, 4.6 ± 0.3 in obligated autogamy and 3.8 ± 0.7 in xenogamy), and at
the end of ripening I counted the proportion of
these that set fruits, in order to calculate the
fruiting success for each treatment. For each
treatment, all fruits from each plant were collected
at the end of the ripening period before seed
dispersal, and a laboratory count was made of the
number of mature seeds, aborted seeds and unfertilized ovules within each fruit.
Role of pollinators in plant reproductive success. I studied the role of pollinators of
E. willkommii by selectively excluding flowers from
ants and winged insects. The basic design of the
experiments had four treatments: (1) ‘‘Control
treatment’’, in which flowers were left to open
65
pollination (N ¼ 15 plants). (2) ‘‘Only Ants treatment’’, in which flowers were excluded from all
visitors but ants (n ¼ 15 plants). To achieve this, I
loosely covered plants with mosquito netting that
screened out all winged insects while allowing ants
to crawl up the stems. In this treatment, the
development of the inflorescences revealed no
abnormalities. (3) ‘‘Only Winged treatment’’, in
which flowers were visited only by winged insects
(n ¼ 15 plants). Ants were excluded by the application of glue (Tanglefoot) surrounding the plants
(see Gómez et al. 1996 for a detailed description of
the methodology). (4) ‘‘No Pollinator treatment’’ in
which flowers were not visited by insects (n ¼ 15
plants). Total exclusion of all flower visitors was
ensured by using the two previous techniques
simultaneously. The plants used in the exclusion
experiments were not the same that those used in
the censuses of floral visitors. The initial number of
flowers produced per plant did not vary among
treatments (F3,56 ¼ 0.002, P ¼ 0.96).
The experiments were checked every two-three
days until flower senescence to ensure that the
exclusions did not affect the normal foraging of
flower visitors. I recorded no wingless insects
visiting the flowers of the ‘‘Only Winged’’ or ‘‘No
Pollinators’’ treatments. During fruiting period,
fruits were counted and collected to quantify
reproductive estimate as above mentioned.
Experimental determination of pollen limitation. In 1996 I tagged 40 plants, leaving 20
randomly selected plants exposed to the natural
level of pollination as the control group. The other
20 plants were also exposed to natural pollinators,
but I supplemented the number of pollen grains
arriving to the stigmas by hand-pollinating all
flowers of each plant with pollen from at least 5
donor plants (Pollen-supplementation treatment).
Artificial pollination was repeated in each flower at
least twice to ensure successful pollination. The
initial number of flowers per plant did not vary
between treatments (F1,38=0.002, P=0.96), being
5.8±0.9 for control plants and 5.7±0.6 for pollensupplemented plants. During the fruiting period,
fruits were counted and collected to quantify
reproductive estimate as mentioned above.
Statistical analysis. All experiments were analysed by one-way ANOVAs (GLM procedure, SAS
1997), introducing each estimate of the plant
reproductive success as a dependent variable, the
treatments as fixed factors and the plant as the
66
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
individual units. When departure from normality, I
arcsin-transformed ratios and log-transformed the
remaining variables. Since I repeated the same
model for each reproductive success estimate, I
used the sequential Bonferroni correction to avoid
experiment-wise type I error, adjusting the p values
of the statistical test to a<0.05.
Results
Plants reproductive traits and flower morphology. On average, plants in the study site
produced 6.4±0.6 flowers [range: 1–21, n ¼ 40]
per year. Fruit set and the SO ratio of
successful fruit (both in percentage) were
75.5±5.0 [0–100] and 79.5±2.1 [10–100],
respectively. Consequently, the average
number of seeds produced per plant every
year was 37.7±6.2 [0–210]. The only reproductive parameter varying between years was
fruit set, which was significantly higher in 1996
than in 1995 (Table 1).
The flower of E. willkommii had a wide
corolla, 4.79±0.14 mm in width and
3.49±0.09 mm in length of the central petal,
with a very short corolla tube, since corolla
depth was just 4.32±0.2 mm (Table 2). As
shown in Table 2, there was a strong correlation between most floral traits (p<0.0001 all
pairwise Pearson correlations, after Bonferroni
correlation), the only trait not correlating with
the others being the depth of the corolla.
Although observations suggest that the flowers
produce nectar, the quantities produced are so
small that they cannot be realiably measured.
Pollinators. The abundance of the insects
visiting the flowers of E. willkommii was
extremely low. During the diurnal period, no
insect was observed at all visiting the flowers of
E. willkommii during 1995. In 1996 I observed
only two species of flower visitors, an ant
species (Proformica longiseta, Formicidae),
and an unknown thrip species (Thysanoptera),
with only 3 and 1 plant visited, respectively. In
addition, no insect at all was observed visiting
the flowers of E. willkommii during the
nocturnal censuses. For this reason, only 3%
of the 128 plants I monitored received an insect
visit during the study period.
Table 1. Between-years comparisons of reproductive parameters of Euphrasia willkommii
1995
Flowers/plant
Fruits/plant
Seeds/plant
Fruit set (%)
SO ratio (%)
7.3
3.9
25.3
58.4
79.9
1996
±
±
±
±
±
0.8
0.4
2.7
5.9
3.4
5.8
5.3
46.9
88.4
79.5
F#
±
±
±
±
±
0.9
0.8
10.3
6.2
2.5
1.34 ns
1.54 ns
3.16 11.71***
0.01 ns
# df = 1, 38, ns = non-significant, p = 0.08, *** p < 0.002. All p-values adjusted to a = 0.05 after
Bonferroni correction
Table 2. Descriptive statistics of each floral trait considered. Also shown is the variance-covariance matrix
among floral traits. Figures above diagonal are covariances, in diagonal are variances, and below diagonal
are correlations. Correlations statistically significants after Bonferroni correction appear in bold face
Floral traits
Corolla width
Central petal length
Lateral petal length
Corolla depth
Mean ± 1
SE (mm)
4.8±0.1
3.5±0.1
2.5±0.1
4.3±0.2
Range
2.1–6.6
1.3–4.8
1.1–3.8
3.5–6.2
Variance-covariance matrix
Corolla
width
Central petal Lateral petal
length
length
Corolla
depth
1.115
0.860
0.803
)0.021
0.665
0.537
0.799
)0.142
)0.080
)0.552
)0.359
0.574
0.593
0.410
0.490
)0.126
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
Both species of flower visitors apparently
visited the flower for nectar. The thrip spent
considerable time visiting the same flower
(about five minutes), whereas the ants usually
spent little time at each flower (less than 30 s),
visiting only one or two flowers per plant.
Nevertheless, the ants observed were apparently visiting E. willkommii flowers only
incidentally, since they spent much more time
visiting flowers of co-occurring plant species
as Sedum anglicum, Thymus serpylloides, Hormathophylla spinosa, Alyssum purpureum or
Arenaria tetraquetra, the flowers of which
were aboundantly visited by these apterous
insects.
By using magnifying glasses, I searched for
E. willkommii pollen grains on the body of the
ants. However, due to the low number of
flower visitor specimens collected, I could not
determine whether they actually are a pollen
vector of E. willkommii. Nevertheless, I
observed ants touching the anthers and stigma
of the flowers during foraging bouts. I could
not gather information on thrips.
Experimental study of the breeding
system. No difference was found between
treatments in any of the components of
reproductive success examined, such as fruit
set (F2,57=1.43, P=0.25), SO ratio (F2,37=
0.08, P=0.92), fruits/plant (F2,57=0.58,
67
P=0.56) and seeds/plants (F2,57=0.15,
P=0.86, see Fig. 2).
Role of pollinators in plant reproductive
success. Whereas fruit set was statistically
similar among treatments, SO ratio was
significantly lower in plants excluded from
winged insects (Table 3). Furthermore, the
number of seeds produced per plant was
similar in plants excluded from winged insects,
wingless insects or from all pollinators than in
flowers left open to all pollinators (Table 3).
Experimental determination of pollen limitation. The experiment showed that the plants
are not pollen limited, since there were no
differences between control and pollen-supplemented plants in fruit set (F1,38=2.18, P=
0.15), SO ratio (F1,38=0.58, P=0.41), fruits/
plant (F1,38=0.084, P=0.77) and seeds/plants
(F1,38=0.001, P=0.98, see Fig. 3).
Discussion
The several experiments conducted during
1995 and 1996 strongly imply that
E. willkommii has the capacity for a high
degree of autofertility and relies mainly on
selfing, since the fruit set and seed set were
similar between autogamously- and allogamously hand-pollinated plants, and spontaneously selfed flowers produced the same amount
Fig. 2. Differences between treatments in reproductive parameters of
Euphrasia willkommii; SA Spontaneous Autogamy, OA Obligated Autogamy, and X Xenogamy
68
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
Table 3. Results of the experimental exclusion of floral visitors. Within a column, values with different
superscripts differ significantly after Bonferroni correction
Treatments
Control
Only ants
Only winged
No pollinator
F-value#
Fruit set (%)
58.4
49.8
53.7
47.6
0.88
±
±
±
±
ns
05.9
11.3
05.5
07.9
SO ratio (%)
79.9 ±
55.7 ±
71.8 ±
71.0 ±
4.53**
a
3.4
3.8b
5.4a,b
6.8a,b
Seeds/plant
18.1
10.4
15.0
17.5
3.53
±
±
±
±
ns
1.7
0.8
2.1
2.8
# df = 3, 56, ns = non significant, ** p < 0.01. All p-values adjusted to a ¼ 0:05 after Bonferroni correction
Fig. 3. Effect of experimental pollen
supplementation on the reproductive
success of Euphrasia willkommii
of fruits and seeds as did hand-pollinated
flowers and open-pollinated flowers. Several
additional traits of E. willkommii suggest that
this plant species is primarily autogamous.
Thus, nectar production is extremely low, if
not absent in most flowers. In addition, its
flowers are very small, only 5 mm in width and
4 mm in length. A decrease in flower size has
been repeatedly associated with the evolution
toward selfing (e.g. Herrera 1992). Indeed,
Ortega Olivencia and Devesa (1993a) have
shown that the autogamous species of iberian
Scrophularia have flowers significantly smaller
than the outcrossers. Unfortunately, there is
no other Euphrasia species, whether outcrossers or selfers, in the alpine of the Sierra
Nevada to make accurate flower-size compar-
isons. Nevertheless, this species bears flowers
significantly smaller that those borne by other
co-occurring Scrophulariaceae, as Digitalis
purpurea L. Linaria glacialis Boiss. or Chaenorrhinum glareosum (Boiss.) Willk. (Molero
Mesa et al. 1992).
Selfing in Euphrasia species has long been
reported (see e.g. Müller 1883). No information
exists about the mechanisms promoting selfing
in E. willkommii. A main mechanism favouring
selfing in many Euphrasia species, like in other
Scrophulariaceae (Dole 1990, 1992; Donnelly
et al. 1998; Kalisz et al. 1999), is delayed selfpollination. Selfing is prevented during the first
day of the flower life by a pronounced herkogamy, when the stigma projects beyond the tip
of the corolla. However, the corolla later
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
elongates, moving the adnate stamens, whereas
the style does not increase in length. Consequently, during the last days of the lifetime of a
flower, anthers and stigma become closer,
leading to self-pollination (Faegri and van der
Pijl 1979). Delayed self-pollination occurs if
flowers have not previously been pollinated
(Dole 1990, Navarro 1997, Kalisz et al. 1999).
Nevertheless, Leclerc-Potvin and Ritland
(1994) did not found delayed selfing in Mimulus
guttatus. For this reason, it is necessary to
study whether selfing in E. willkommii is
promoted by delayed self-pollination or by
any other mechanism, as for example incomplete dichogamy or close proximity of anthers
and stigmas during dehiscence.
The ecological scenario where E. willkommii
inhabits, the Mediterranean high-mountains of
SE Spain, presumably favour the evolution of
selfing, since stressful abiotic conditions usually
make pollinators a limiting resource – either
scarce and unpredictable or lacking synchrony
between insect life cycles and flowering (Gómez
and Zamora 1996). Indeed, the pollinator
censuses during two reproductive seasons,
with almost 90 hours of observations, have
shown that, in fact, the abundance of insects at
E. willkommii flowers is quite low in these alpine
environments. I observed many flowers wilted
without receiving a single insect visit. In addition, the species of insects visiting the flowers of
E. willkommii, ants and thrips, were tiny and
considered as generalist and low-efficient pollinators. This observation contrasts with the
abundant literature on the pollination ecology
of many other species of plants belonging to the
Scrophulariaceae, which have shown that the
floral visitors are usually efficient pollinators,
such as hummingbirds, moths, butterflies, bumblebees, long-tongued bees, etc. (e.g. Dieringer
1992, Vickery 1992, Ortega Olivencia and
Devesa 1993b, Sutherland and Vickery 1993,
Kampny 1995, Kampny and Dengler 1997,
Jones and Reithel 2001). Ants, and other generalist floral visitors such as mosquitoes or
Muscid flies, are important pollinators of other
plant species in the Sierra Nevada high mountains (Gómez and Zamora 1992, 1999; Gómez
69
et al. 1996). The limitation of pollinators is so
extreme in these habitats that some typical
entomophilous plant species (for example, the
crucifer Hormathophylla spinosa) have even
evolved the ability of using wind as a pollen
vector in their highest populations (Gómez and
Zamora 1996). The presence of the few ants and
thrips found in the flowers of E. willkommii is
made possible by the fact that the small and lowreward flowers are wide, short and tubular,
allowing access to almost any type of insect. In
addition, since the entire plant is very low (<5
cm in height), the flowers are normally very close
to the ground, discouraging discovery by and
accessibility for large flying insects and thus
favouring access by non-flying insects such as
ants.
Selfing may explain why, despite the
absence of floral visitors, E. willkommii proved
not to be pollen-limited in natural conditions.
This contrasts with many other alpine plants,
in which reproduction is highly limited by
pollen availability (Galen 1985, Berry and
Calvo 1991, Campbell 1991, Stentröm and
Molau 1992). Furthermore, selfing could also
explain why the percentage of flowers ripening
to fruit and the percentage of ovules ripening
to seed is very high in E. willkommii (>80% for
both parameters). Empirical and theoretical
studies have shown that these two ratiooriented estimates of the reproductive success
are usually low in allogamous but high in
autogamous plant species (e.g. Lee 1988). All
of these data suggest the benefit that selfing
can confer on E. willkommii reproduction,
although it may be necessary to explore the
effect of selfing on other, postdispersal stages
of the recruitment process, as for example seed
germination or seedling survival.
In brief, according to the data of this study,
E. willkommii is predominantly autogamous.
In this case, selfing appears to be an ecological
mechanism to ensure successful reproduction
in a harsh environment where pollinator
availability and predictability is extremely low.
Adela González Megı́as helped during the field
work. I thank very much the comments of Dr. Luı́s
70
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
Navarro which have substancially improved an
early version of the manuscript. David Nesbitt
improved the English. This work was partially
supported by DGICYT grants PB900852 y
AMB95-0479.
References
Aarssen L. W. (2000) Why are most selfers annuals? A new hypothesis for the fitness benefit of
selfing. Oikos 89: 606–612.
Arroyo M. K. T., Peñazola A. (1990) Genetic selfincompatibility in a South American species of
Ourisia (Scrophulariaceae). New Zeal. J. Bot. 28:
467–476.
Barrett S. C. H. (1998) The evolution of mating
strategies in flowering plants. Trends in Plant
Science 3: 335–341.
Berry P. E., Calvo R. N. (1991) Pollinator limitation and position dependent fruit set in the high
Andean orchid Myrosmodes cochlerare (Orchidaceae). Plant Syst. Evol. 174: 93–101.
Campbell D. R. (1991) Effects of floral traits on
sequential components of fitness in Ipomopsis
aggregata. Amer. Nat. 137: 713–737.
Dieringer G. (1992) Pollinator effectiveness and
seed set in populations of Agalinis strictifolia
(Scrophulariaceae). Amer. J. Bot. 79: 1018–1023.
Dole J. A. (1990) Role of corolla abscission in
delayed self-pollination of Mimulus guttatus
(Scrophulariaceae). Amer. J. Bot. 77: 1505–1507.
Dole J. A. (1992) Reproductive assurance mechanisms in three taxa of the Mimulus guttatus
complex (Scrophulariaceae). Amer. J. Bot. 79:
650—659.
Donnelly S. E., Lortie C. J., Aarssen L. W. (1998)
Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Amer. J. Bot.
85: 1618–1625.
Erhardt A., Jaggi B. (1995) From pollination by
Lepidoptera to selfing: the case of Dianthus
glacialis (Caryophyllaceae). Plant Syst. Evol.
195: 67–76.
Faegri K., van der Pijl L. (1979) The principles of
pollination ecology, 3rd edn. Pergamon Press.
Fausto J. A., Eckhart V. M., Geber M. A. (2001)
Reproductive assurance and the evolutionary
ecology of self-pollination in Clarkia xantiana
(Onagraceae). Amer. J. Bot. 88: 1794–1800.
Galen C. (1985) Regulation of seed-set in Polemonium viscosum: floral scents, pollination, and
resource. Ecology 66: 792–797.
Gómez J. M., Zamora R. (1992) Pollination by
ants: consequences of the quantitative effects on
a mutualistic system. Oecologia 91: 410–418.
Gómez J. M., Zamora R. (1996) Wind pollination
in high-mountain populations of Hormathophylla spinosa (Cruciferae). Amer. J. Bot. 83: 580–
585.
Gómez J. M., Zamora R. (1999) Generalization vs.
specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecology 80:
796–805.
Gómez J. M., Zamora R., Hódar J. A., Garcı́a D.
(1996) Experimental determination of pollination by ants in Mediterranean high mountain
and arid habitats. Oecologia 105: 236–242.
Herrera J. (1992) Flower variation and breeding
system in the Cistaceae. Plant Syst. Evol. 179:
245–255.
Holsinger K. E. (1992) Ecological models of plant
mating systems and the evolutionary stability of
mixed mating systems. In: Wyatt R. (ed.) Ecology and evolution of plant reproduction. Chapman and Hall, New York, NY, pp. 169–191.
Holsinger K. E. (2000) Reproductive systems and
evolution in vascular plants. Proc. Natl. Acad.
Sci. 97: 7037–7042.
Jones K. N., Reithel J. S. (2001) Pollinator-mediated selection on a flower color polymorphism in
experimental populations of Antirrhinum
(Scrophulariaceae). Amer. J. Bot. 88: 447–454.
Kalisz S., Vogler D., Fails B., Finer M., Shepard
E., Herman T., Gonzales R. (1999) The mechanism of delayed selfing in Collinsia verna
(Scrophulariaceae). Amer. J. Bot. 86: 1239–1247.
Kampny C. M. (1995) Pollination and flower
diversity in Scrophulariaceae. The Botanical
Review 61: 350–366.
Kampny C. M., Dengler N. G. (1997) Evolution of
flower shape in Veroniceae (Scrophulariaceae).
Plant Syst. Evol. 205: 1–25.
Lee T. D. (1988) Patterns of fruit and seed
production. In: Lovett Doust J., Lovett Doust
L. (eds.) Plant reproductive ecology, patterns
and strategies. Oxford University Press, New
York, USA, pp. 179–202.
Leclerc-Potvin C., Ritland K. (1994) Modes of
self-fertilization in Mimulus guttatus (Scrophu-
J. M. Gómez: Self-pollination as reproductive assurance in an alpine Scrophulariaceae
lariaceae): a field experiment. Amer. J. Bot. 81:
199–205.
Molero Mesa J., Perez Raya F., Valle F. (1992)
Parque Natural de Sierra Nevada: Paisaje,
fauna, flora, itinerarios. Editorial Rueda, Alcorcón, Madrid, Spain.
Müller H. (1883) The fertilization of flowers.
Macmillan and Co, London, UK.
Navarro L. (1997) Is the dichogamy of Salvia
verbenaca (Lamiaceae) an effective barrier to
self-fertilization? Plant Syst. Evol. 207: 111–117.
Navarro L., Guitian J. (2001) The role of floral
biology and breeding system on the reproductive
success of the narrow endemic Petrocoptis viscosa Rothm. (Caryophyllaceae). Biol. Conserv.
103: 125–132.
Ortega Olivencia A., Devesa J. A. (1993a) Sexual
reproduction in some Scrophularia species
(Scrophulariaceae) from the Iberian Peninsula
and the Balearic Islands. Plant Syst. Evol. 184:
159–174.
Ortega Olivencia A., Devesa J. A. (1993b) Floral
rewards in some Scrophularia species (Scrophulariaceae) from the Iberian Peninsula and the
Balearic Islands. Plant Syst. Evol. 184: 139–158.
71
Schoen D. J., Morgan M. T., Bataillon T. (1997)
How does self-pollination evolve? Inferences
from floral ecology and molecular genetic variation. In: Silvertown J., Franco M., Harper J. L.
(eds.) Plant life history. Cambridge University
Press, Cambridge, UK, pp. 77–101.
Stenström M., Molau U. (1992) Reproductive
ecology of Saxifraga oppositifolia: Phenology,
mating system, and reproductive success. Artic
and Alpine Research 24: 337–343.
Sutherland S. D., Vickery R. K. (1993) On the
relative importance of floral color, shape, and
nectar reward in attracting pollinators to Mimulus. Great Basin Naturalist 53: 107–117.
Vickery R. K. (1992) Pollinator preferences for
yellow, orange, and red flowers of Mimulus
verbenaceous and M. cardinalis. Great Basin
Naturalist 52: 145–148.
Address of the author: José M. Gómez,
Departamento de Biologı́a Animal y Ecologı́a,
Fac. de Ciencias, Universidad de Granada,
E-18071 Granada, Spain (e-mail: [email protected]).