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Gayana Bot. 69(2), 2012
286
Pollination and breeding system in Adesmia bijuga Phil. (Fabaceae), a
critically endangered species in Central Chile
Polinización y sistema reproductivo en Adesmia bijuga Phil. (Fabaceae), una especie en
peligro crítico en Chile central
PERSY GÓMEZ P.1, DIANA LILLO2 & ALEJANDRA V. GONZÁLEZ2*
1Jardín Botánico de la Universidad de Talca, P.O. Box 747, Talca, Chile.
2Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, P.O. Box 653, Santiago, Chile.
*apgonzalez@uchile.cl
ABSTRACT
Adesmia bijuga Phil. is an endemic shrub in central Chile, classified as a critically endangered species of plant. After
more than 100 years since its original description by R. A. Philippi (1884), the species was rediscovered exclusively in
two locations of the Maule Region. One of them, Fundo San Pedro-Las Cañas, is close to extinction with a low number of
shrubs, occurring in a disturbed habitat due to plantations of Pinus radiata. This study examined the pollination biology
and breeding system of A. bijuga in order to explain their small number of shrubs. We estimated composition of pollinator
species attracted to flowers and visitation rates. In order to describe its breeding system in A. bijuga we used manipulated
treatments to estimate autonomous self-pollination, level of reproductive assurance and pollen limitation. The results of this
study indicate that only pollinators from the order Hymenoptera visit A. bijuga. The pollinator assemblage did not show
temporary variation during the flowering season, with Bombus dahlbomii as its most frequent visitor. A. bijuga showed a
mixed mating system that involves both cross- and self- pollination. The fruit set ranges from 20% to 60% in the absence or
presence of pollinators, respectively. This selfing ability would provide reproductive assurance when pollinators fail. The
taxon showed ability of asexual formation of seeds without the occurrence of fertilization by agamospermy. Supplemental
outcross pollen did not increase female reproductive success, suggesting that the species is not pollen limited. All these
factors may help to explain how this species has been able to survive over time in a small and isolated population. Finally,
this work discusses how the results of our study can be applied to future A. bijuga conservation measures.
KEYWORDS: Critically endangered species, Adesmia bijuga, pollination, breeding system, visitation rate.
RESUMEN
Adesmia bijuga Phil. es una especie arbustiva endémica de Chile central, clasificada como especie en peligro crítico. Después
de más de 100 años desde su descripción original por R.A. Philippi (1884), la especie fue redescubierta exclusivamente en
dos localidades de la Región del Maule. Una de ellas, en el Fundo San Pedro-Las Cañas, se encuentra cercana a la extinción,
en un hábitat perturbado debido a plantaciones de Pinus radiata. Este estudio examinó la biología de la polinización y
el sistema reproductivo de A.bijuga, que podrían explicar su restringido número de plantas. Se estimó la composición
de polinizadores atraídos por las flores y la tasa de visita. Con el objetivo de caracterizar el sistema reproductivo en A.
bijuga se realizaron tratamientos manipulativos para cuantificar la capacidad de autofertilización, el nivel de aseguramiento
reproductivo y la limitación de polen. Los resultados de este estudio indican que A. bijuga es visitada solamente por
polinizadores que pertenecen al orden himenóptera. El ensamble de polinizadores no varió temporalmente durante el periodo
de floración, siendo Bombus dahlbomii el visitador más frecuente. A. bijuga presentó un sistema reproductivo mixto, con
polinización cruzada y autopolinización. El rango de fructificación varió entre 20% a 60% en ausencia y presencia de
polinizadores, respectivamente. Esta capacidad de autopolinización podría proveer de aseguramiento reproductivo cuando
los polinizadores fallan. Tratamientos con suplemento de polen no incrementaron el éxito reproductivo, sugiriendo que la
especie no se encuentra limitada de polen. El taxon mostró capacidad de formar semillas asexualmente sin la ocurrencia de
fertilización (agamospermia). Todos estos factores podrían ayudar a explicar cómo esta especie es capaz de persistir en el
tiempo en una población pequeña y aislada. Finalmente, este trabajo discute cómo los resultados de este estudio pueden ser
aplicados en futuras medidas para la conservación de A. bijuga.
PALABRAS CLAVE: Especie en peligro crítico, Adesmia bijuga, polinización, sistema reproductivo, tasa de visita.
Gayana Bot. 69(2): 286-295, 2012 ISSN 0016-5301
287
Pollination and breeding system in Adesmia bijuga: GÓMEZ, P. ET AL.
INTRODUCTION
Understanding the ecology of critically endangered species
is crucial both in comprehending the causes of their
conservation status as well as formulating appropriate
management measures. Nevertheless, insufficient
appreciation of the ecology of a particular species is
repeatedly cited as a shortcoming in the management of
threatened and endangered plants (Schemske et al. 1994, Tear
et al. 1995). Critically endangered species are at the sharp
end of today’s global extinction crisis. These are species
judged most likely to become extinct in the immediate
future unless conservation efforts are made (Rossetto et
al. 1997). Causes of rarity and critical endangerment are
diverse, ranging from direct human destruction of wild
ecosystems to processes such as recent evolutionary origin
or reproductive failure of relict species under changed
environmental circumstances (Fiedler & Ahouse 1992, Pate
& Hopper 1993). For example, several comparisons of rare-
common species pairs have demonstrated that reproduction
and recruitment are often particularly low in rare species
(Münzbergová 2005, Young et al. 2007). The need to gather
information on the basic biology of rare species is vital to
both species- and community-level conservation efforts
(Saunders & Sedonia 2006).
Pollination is a fundamental aspect of plant reproduction,
and pollination by animals is largely considered a co-
adaptive process in which plants evolve traits to attract
certain pollinators, whereby pollinators then evolve traits
to better exploit floral resources of particular plants, with
the occurring natural selection mediated by that pollinator
(Faegri & Van der Pijl 1980, Heinrich 1983). For natural
selection to occur, the pollinator must first benefit from the
plants fitness, increasing for example their reproductive
success (Gómez & Zamora 2006). Plant reproductive
success often depends on pollination biology (including
the frequency and identity of floral visitors), capability
of autonomous self-pollination, and/or the magnitude of
pollen limitation (Banks 1980, Mehrhoff 1983, Burd 1994,
Gaston & Kunin 1997, Knight et al. 2005, Lavergne et al.
2005, Rymer et al. 2005, Aizen & Harder 2007). Autogamy
provides reproductive assurance and can benefit alien as well
as narrowly distributed plants. It is easier for autogamous,
introduced plant species to invade new territories than those
that require cross-pollination through animal pollinators
(Baker 1955, Richardson et al. 2000, Van Kleunen &
Johnson 2007). Likewise, autogamous, plant species with
reduced habitat distribution are less likely to experience
failed or low reproductive output when they occur at
low densities (Banks 1980, Clampitt 1987, Kaye 1999).
Numerous studies have recognized that mating strategies
play a critical role in the survival of small plant populations
(Gargano et al. 2009).
Adesmia bijuga is a perennial plant forming a shrub
(reaching 2 m in height) with hermaphrodite flowers (Hahn
& Gómez 2008). After more than 100 years since the
original description by R. A. Philippi (1884), the species was
rediscovered in two localities of the Maule Region, Chile:
Fundo San Pedro-Las Cañas (Constitución) and Huelón
(Curepto) (Figs. 1a-1b), both populations which are separated
by approximately 55 km. The population in Fundo San
Pedro-Las Cañas (Fig. 1c) is in a disturbed habitat, growing
mainly underneath Pinus radiata D.Don plantations, and
sclerophyllous vegetation such as Baccharis rhomboidalis
J.Remy subsp. truncata (Phil.) F.H.Hellw., Adesmia elegans
Clos, Ugni molinae Turcz., Ribes punctatum Ruiz et Pav. and
Escallonia pulverulenta Pers. (Hahn & Gómez 2008). Based
on demographic characteristics, A. bijuga was classified as
a critically endangered plant (Gómez et al. 2009). Studies
in pollination biology and breeding systems of A. bijuga are
unknown, even less so given that the pollination ecology
may be contributing to their small habitat distribution. Since
plant mating systems affect population genetic diversity
(Hamrick & Godt 1989) and potentially population
survival, developing an effective management plan for
plants with reduced habitat distribution, should be the first
step to understanding the reproductive biology of the taxon
(Hamrick et al. 1991). Indeed, the lack of data on species
biology is repeatedly cited as a shortcoming of threatened
and endangered species recovery plans (Schemske et al.
1994, Clark et al. 2002). In this context, we examined the
natural history of the pollination biology and breeding
systems of A. bijuga (Fabaceae). We used observational and
experimental approaches to address three main questions:
(i) Is Adesmia bijuga visited by pollinators?, (ii) Is A. bijuga
capable of autonomous selfing?, and (iii) Does selfing
provide reproductive assurance when pollinators fail?
METHODS
STUDY SITE AND NATURAL HISTORY
The study was conducted from December 2010 to January
2011 at the Fundo San Pedro (Maule Region; lat. 35°29’31”S,
long.72°22’47”W), located about 20 km southeast of
Constitution, Chile (Fig. 1). In this area, the climate is of
a Mediterranean type with rainfall concentrated in the
winter season (Di Castri & Hajek 1976). The population
of A. bijuga grows primarily underneath sclerophyllous
vegetation. However, about 20 years ago, this habitat was
disturbed by Pinus radiata. After that, A. bijuga grows in
clearings between two Pinus plantations (Fig. 2a). This
population is composed by approximately 300 shrubs
(juveniles and adults) with only 33 (11%) being observed
as flowering shrubs. The hermaphrodite flowers are yellow
with brownish lines, composed by five petals with butterfly-
shaped papilonaceus (Fig. 2b). Flowers are 1.48-1± 0.03
( SE) cm long with 10 staminoids. The indehiscent fruit
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Gayana Bot. 69(2), 2012
(legumes) are 0.5-1.4 cm long, covered with numerous
hairs and with 1-4 seeds per legume (Fig. 2c). The
flowering season is from December through January, while
fructification is from January through February. At the study
site, 40.9 % of the A. bijuga flowers presented some level of
herbivory by larvae (9 out of 22 flowers), due to the absence
of reproductive structures (ovary, pistil and staminoids).
POLLINATOR VISITATION
We recorded the identity and visitation rate of diurnal
insects in 33 flowering shrubs. On each focal flower, we
observed pollinator visits during 30 min, recording the
species and number of visits. We defined a visit as the
contact between a pollinator and the sexual structure of
the flower. The observations of pollinator activity were
performed between 1100 and 1700 h by two trained
observers. We spent a total of 14,400 min of observation
during a total period of 4 days, once a week from December
to January. Only during the first-day of observation
were unknown pollinators captured and identified in the
laboratory. Visitation rates were calculated as the number
of visits per open flower per hour. Probability of visits
were estimated as Pv= 1- 1/ex, where x is the visitation rate
for each plant (Cavieres et al. 1998). To evaluate temporal
variation during the flowering season, we statistically
compared visitation rates between weeks using repeated
measures ANOVA. Additionally, we calculated pollinator
diversity using the Shannon–Wiener H’ index. In order to
accomplish this, we estimated 95% confidence intervals
for each index by randomizing samples in 500 bootstrap
replications in EstimateS (Colwell 2009). We compared
pollinator diversity between weeks using the t-test with
Bonferroni’s adjustments (Sokal & Rohlf 1995).
FIGURE 1. Geographic location of Adesmia bijuga populations. (a) Map of Chile characterizing the Maule Region. (b) Close-up of the Maule
Region with two locations of A. bijuga, 1) Population Fundo San Pedro-Las Cañas, Constitucion and 2) Population Huelón, Curepto. (c)
Close-up to the exact location of the study population (Fundo San Pedro-Las Cañas).
FIGURA 1. Ubicación geográfica de las poblaciones donde se encuentra Adesmia bijuga. (a) Mapa de Chile caracterizando la VII Región del
Maule. (b) Acercamiento de la VII Región del Maule con las dos únicas localidades en que se ha encontrado A. bijuga, 1) Población del
Fundo San Pedro-Las Cañas, Constitución and 2) Población de Huelón, Curepto. (c) Acercamiento para mostrar con exactitud la ubicación
geográfica de la población en estudio (Fundo San Pedro-Las Cañas).
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Pollination and breeding system in Adesmia bijuga: GÓMEZ, P. ET AL.
FIGURE 2. Adesmia bijuga from Fundo San Pedro (Maule Region). (a) A. bijuga grows mainly underneath sclerophyllous vegetation that
includes Pinus radiata plantation and sclerophyllous shrubs; scale bar= 1 m. (b) Yellow hermaphrodite flowers, composed of five petals;
scale bar= 1 cm. (c) The indehiscent fruit (legumes) with 1-4 seeds per legume; scale bar= 1 cm.
FIGURA 2. Adesmia bijuga del Fundo San Pedro (región del Maule). (a) A. bijuga creciendo bajo la vegetación que incluye plantación Pinus
radiata y arbustos esclerófilos, escala =1 m. (b) Flores amarillas hermafroditas compuestas por cinco pétalos; escala = 1 cm. (c) El fruto
indehiscente (lomento) con 1-4 semillas por lomento; escala = 1 cm.
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Gayana Bot. 69(2), 2012
BREEDING SYSTEM
In order to evaluate the dependence upon pollinator agents
for effective fertilization, we evaluated the breeding system
of A. bijuga at the study site. For this, we tagged 20 plants
and set up five treatments on each one, and they were tested
for: (1) Autogamy, estimating the capacity for automatic
self-pollination, in which buds were bagged throughout their
flowering period without emasculation; (2) Geitonogamy,
estimating genetic self-incompatibility by hand self-
pollination. One bud per plant was immediately bagged after
emasculation, during anthesis the flowers were pollinated
with pollen from the same individual previously isolated
in the bud stage. The pollinated flower was re-bagged until
fruit formation; (3) Agamospermy, estimating the capacity
of asexual formation of seeds without the occurrence of
fertilization, in which buds were immediately bagged after
emasculation; (4) Manual cross-pollination (Xenogamy),
in which emasculated flowers in anthesis were pollinated
with pollen from another plant at least 10 m away and then
bagged; and (5) open-pollinated flowers (Control), in which
flowers were exposed to the natural agents of pollination.
All emasculation treatments were conducted before anther
dehiscence and the stigma was rubbed with a brush as well
as the control treatment. From a total of 100 flowers, we
quantified the percentage of flowers that set fruit four weeks
after anthesis. Fruit sets were estimated as mature fruits
per flower (legume formation). Additionally, we estimated
fruit size (legume length), and number of seeds per fruit
(N° of seed per legume) for each treatment. We compared
fruit set among treatments using G-test with Bonferroni’s
adjustments (Sokal & Rohlf 1995). Comparisons of fruit
size and number of seeds per fruit were made using one-way
ANOVA with a posteriori Tukey-HSD test (Sokal & Rohlf
1995). We examined whether the levels of fruit set exhibited
a relationship to fruit size and seeds per fruit, to do this we
used Spearman correlation analyses. All statistical analyses
were performed using STATISTICA (data analysis software
system) version 7 (StatSoft, Inc. 2004, www.statsoft.com).
In addition, we estimated an index of self-incompatibility
(ISI) using the formula: ISI = N° seed geitonogamy/ N° seed
xenogamy (Ruiz & Arroyo 1978). An index of automatic
self-pollination (IAS) was obtained using the formula: IAS=
% fruit set by autogamy / % fruit set by geitonogamy (Ruiz
& Arroyo 1978).
RESULTS
POLLINATOR VISITATION
We recorded a total of 688 visits to 33 focal plants of A.
bijuga. The assemblage of diurnal visitors consisted of
five taxa (Table I), all of them hymenopterans species
from the Apidae family. In terms of frequency, the most
important visitor was the endemic Bombus dahlbomii
(88.2%), visiting A. bijuga plants between 8 to 46 times
more often than other species (Table I). Most of the
visitors (10.7%) were introduced species including
Bombus terrestris (4.6%), Bombus ruderatus (4.4%), and
Apis mellifera (0.7%). The remaining 2% of visits were
made by the native species, Manuelia gayatina. During the
study period visitation rates and pollinator diversity did
not differ between weeks of observation (ANOVA F=0.05,
P=0.98; Table II), indicating no temporal variation in
diurnal visitor assemblages during their flowering season
(December to January). This result suggests that A. bijuga
attracted a variety of potential pollinators that probably
play an important role on the dispersion and amount of
pollen deposited on the stigmas.
TABLE I. Pollinator visitation rate (visits fl ower-1 h-1) mean ± SE and probability of visits of pollinator on Adesmia bijuga during their
fl owering season (December to January).
TABLA I. Tasa de visita de los polinizadores (visita fl or -1 h-1) promedio ± EE y probabilidad de visita de los polinizadores en Adesmia bijuga
durante su periodo de fl oración (diciembre a enero).
POLLINATOR SPECIES VISITATION RATE
(Visits flower-1 h-1)
PROBABILITY OF VISITS
(Pv)
Apis mellifera 0.02 ± 0.03 0.02
Manuelia gayatina 0.05 ± 0.09 0.05
Bombus ruderatus 0.12 ± 0.09 0.11
Bombus terrestris 0.12 ± 0.04 0.11
Bombus dahlbomii 2.31 ± 0.49 0.90
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Pollination and breeding system in Adesmia bijuga: GÓMEZ, P. ET AL.
BREEDING SYSTEM
A. bijuga Fundo San Pedro showed a mixed mating system
that involves both cross- and self-pollination. The fruit
set ranges from 20% to 60% in the absence or presence
of pollinators, respectively (Table II). In addition, plants
were self-compatible (ISI=1.13) and partially autogamous
(IAS=0.55).
Fruit-set among treatments was statistically different (G
= 10.04, df = 4, P = 0.04; Table III). Paired comparisons
showed significant differences in the percentage of fruit sets
between Control flowers and the other treatments, reaching
60% of fructification in untreated flowers. Treatments
with flowers excluded from the pollinators set showed
no statistical differences between them; autogamously
treatments showed capability for automatic self-pollination
in 25% of the sampled flowers, while geitonogamously
selfed flowers showed genetic self-compatibility in 45%
of the sampled flowers. Additionally, the capability of
the asexual seed formation without the occurrence of
fertilization (agamospermy) was found in only 20% of the
sampled flowers, and there were no statistical differences
when compared to flowers from which pollinators had been
excluded (autogamy and geitonogamy, Table III).Conversely,
supplemental outcross pollen treatment (xenogamy) did
not significantly increase female reproductive success in
A. bijuga compared to the Control flowers, this treatment
reached only 25% of the sampled flowers, and did not differ
from other treatments excluded from pollinators (Table III).
Overall, these results indicate that A. bijuga showed a mixed
mating system, however pollinators play an important role
as inter- and intra-plant pollen vectors increasing fruit set
percentages of sampled flowers.
TABLE II. Comparisons of pollinator visitation during studied period (four weeks) on Adesmia bijuga. Visitation rate (visits fl ower-1 h-1)
mean ± SE, and diversity (H’ mean ± SD).
TABLA II. Comparación de la visita de polinizadores durante el periodo de estudio (cuatro semanas) en Adesmia bijuga. Tasa de visita de los
polinizadores (visita fl or -1 h-1) promedio ± EE y diversidad (H’ promedio ± DS).
PERIOD OF POLLINATORS
OBSERVATIONS
VISITATION RATE (visits
flower-1 h-1)
POLLINATOR DIVERSITY
(H’ mean ± SD)
1st week 0.6 ± 0.53a 0.43 ± 0.14a
2nd week 0.6 ± 0.47a0.46 ± 0.10a
3rd week 0.5 ± 0.44a 0.48 ± 0.05a
4th week 0.5 ± 0.45a 0.48 ± 0.00a
Different letters show significant differences (P < 0.001). / Letras diferentes indican diferencias significativas (P < 0,001).
TABLE III. Fruit-set, legume length and number of seed from different treatment of breeding system on Adesmia bijuga (mean ± SE).
TABLA III. Fructifi cación, tamaño del lomento y número de semillas de los diferentes tratamientos del sistema reproductivo en Adesmia
bijuga (promedio ± EE).
TREATMENT N° OF PLANTS
PER TREATMENT
FRUIT-SET (%) LEGUME
LENGTH (cm)
N° OF SEED PER
LEGUME
Autogamy 20 25a0.8±0.2ab 1.6±0.1ab
Geitonogamy 20 45ab 0.8±0.3ab 1.8±0.1ab
Agamospermy 20 20a1.2 ±0.1a2.8±0.1a
Xenogamy 20 25a0.8±0.2ab 1.6±0.1ab
Control 20 60b0.7±0.2 b1.5±0.1b
Different letters show significant differences (P < 0.001). / Letras diferentes indican diferencias significativas (P < 0,001).
292
Gayana Bot. 69(2), 2012
The fruit size (legume length) and number of seeds per
legume differed among treatments (F=3.50, df = 4, P=0.018
and F=2.72, df = 4, P=0.047, respectively). In both cases,
A posteriori comparisons revealed significant differences
between Control flowers and agamospermy treatment (Table
III). We found a positive correlation between legume length
and number of seeds per legume (r = 0.98, P = 0.002). By
contrast, non- significant associations were found between
fruit set percentage and legume length (r = -0.64, P = 0.242),
and between fruit set percentage and number of seeds by
legume (r = -0.51, P = 0.382). These results suggest that
longer legumes produce a higher number of seed in A.
bijuga from Fundo San Pedro.
DISCUSSION
Results from this study indicate that the critically
endangered species, A. bijuga, from Fundo San Pedro, is
visited by pollinators from the order hymenopterans. The
pollinator assemblage did not show temporal variation
during the flowering season, with Bombus dahlbomii being
the most important visitor. A. bijuga has a mixed mating
system that involves both cross- and self-pollination. Cross
pollination was characterized due to a higher visitation
rate from Bombus dahlbomii; whereas self-pollination was
observed in their capacity for being self-compatible and
being relatively autogamous. This selfing ability would
provide reproductive assurance when the pollinator fails to
visit the flower. In this population the species showed ability
for asexual formation of seeds, without the occurrence of
fertilization by agamospermy. Supplemental outcross pollen
did not increase female reproductive success, indicating that
female reproductive success is not pollen limited. All these
factors may help to explain how this species has been able to
survive over time in a small and isolated population.
Under natural conditions the A. bijuga populations exist
in an already fragmented system, and the introduced bees
Apis mellifera, Bombus ruderatus and Bombus terrestris
were among the main flower visitors. However, the endemic
Bombus dahlbomii was 9 times more likely to visit A. bijuga
than introduced species. Fragmentation and introduced
pollinators are known threats to the successful pollination of
native plants (Goulson 2003, Tscharntke & Brandl 2004). In
principle, habitat fragmentation is expected to affect plant
population genetic diversity due to endogamy and genetic
drift, both reducing the adaptive capability of the species to
environmental changes (Aguilar et al. 2009). Nevertheless,
habitat fragmentation influences plant-pollinator
interactions by reducing the richness of pollinators, or by
decreasing efficient pollinator abundance (e.g. Aizen &
Feinsinger 1994, Rathcke & Jules 1993, Steffan-Dewenter
& Tscharntke 1999, Cane 2001, Aguilar 2005). In both
cases, the plants populations experience reduced fitness due
to unsuccessful pollination, with lower fructification and
seed formation (e.g. Aguilar & Galetto 2004). Even though
it is difficult to speculate on the possible impact of either
of these processes on the examined A. bijuga populations
without prior knowledge of the pollination conditions upon
their establishment, it is likely that hymenopterans are the
visitors with the greatest ability for affecting pollination in
A. bijuga, with the native Bombus dahlbomii as one of the
most important visitors. Moreover, pollinator introduction
can displace native species (Morales et al. 2009), especially
when the new pollinator is more of a generalist than its
native counterpart. For example, Apis mellifera and Bombus
terrestris are the most commonly introduced species due
to human activities, and both are considered generalist
pollinators that can reach higher abundance (see Morales
et al. 2009 for a review). With A. bijuga, introduced species
showed lower frequency of visits than Bombus dahlbomii,
but future studies should address the effect of pollinator
abundance, efficiency, and their consequences on A. bijuga
reproductive success.
The species A. bijuga has several characteristics
suggesting a mixed mating system of outbreeding and self-
fertilization. Versatility in mode of reproduction has been
described for other Adesmia legume species (Tedesco et al.
2000), and probably explains their maintenance over time.
For example, in very variable pollination environments,
such as the Atacama Desert, the mixed mating system
keeps the population of A. argyrophylla alive (González
& Pérez 2010). Numerous studies demonstrated a mixed
mating system in species with reduced habitat which
probably helps to explain how the species are able to
survive over time in small and isolated populations (Hill
et al. 2008, Gargano et al. 2009, Shi et al. 2010, Powell et
al. 2011). In this context, selfing ability and autogamous
capacity provide reproductive assurance, producing enable
seed production when pollinators or mates are scarce or
unavailable, and outcross pollen is insufficient for full
fertilization of ovules. In our studied population, selfing
occurred by automatic self-pollination (autogamy, 25%
of fructification), and between flowers of the same plant
(geitonogamy 45% of fructification). In this scenario,
only autogamy would provide reproductive assurance, the
geitonogamy which can be due to common bee movement
within-inflorescence of A. bijuga or lower flowers display
for pollination is not expected to provide reproductive
assurance because it involves both pollen and seed
discounting (Lloyd 1992, Lloyd & Schoen 1992, Herlihy &
Eckert 2002). Geitonogamy will result in greater inbreeding
depression (Holsinger & Thomson 1994, Harder & Barrett
1995), with lower seed set and fitness when compared to
populations receiving large amounts of outcross pollen
(Jennersten 1988, Lamont et al. 1993, Agren 1996, Fischer
& Matthies 1998). Inbreeding depression may, in turn,
have serious negative consequences for population survival
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Pollination and breeding system in Adesmia bijuga: GÓMEZ, P. ET AL.
(Oostermeijer 2000), as reduction in genetic diversity and
fitness over time (Ellstrand & Elam 1993). Numerous
studies have suggested that geitonogamy reduces female
reproductive success due to post-fertilization abortion
(Finner & Morgan 2003). Due to its widespread and largely
deleterious nature, geitonogamy has been hypothesized as a
major selective force in plant reproductive ecology (Wyatt
& Broyles 1994). Even though we found a higher rate of
geitonogamy in A. bijuga, future studies about inbreeding
depression by loss of genetic variability and fitness are
needed in order to be able to explore the data on seed
quality/viability and early developmental phases, which
are critical in estimating successful seedling establishment
population.
The lack of pollen limitation may be attributed to three
different factors. First, the application of a low-diversity
pollen grains, as we found low number of flowering A.
bijuga shrubs (11%) in the studied population, the number
of pollen donors was limited, second, a high probability
of flowers of visitation by Bombus dahlbomii (0.9) under
natural condition suggests that supplemental pollination
should not increase female reproductive output. Third, the
ability of A. bijuga to self-fertilize probably affects pollen
limitation. Burd (1994) detected a correlation between plant
mating systems and pollen limitation, showing that self-
compatible species are not pollen-limited, whereas self-
incompatible species are commonly pollen limited.
Finally, flower herbivory is another factor which probably
affects A. bijuga populations. We found large numbers of
floral buds with destroyed reproductive structures (ovary,
pistil and staminoids), due to the presence of insect
larvae. Numerous studies have demonstrated that flower
herbivory can have a direct and immediate impact on plant
attractiveness when florivores destroy primary reproductive
tissues such as anthers, pistils, or ovaries (Kirk 1987, Maron
et al. 2002, Wise & Cummins 2002, Althoff et al. 2005).
Future studies should evaluate the impact of florivory on A.
bijuga female reproductive success.
Overall, our work provides initial insight into the
pollination biology and breeding system of the critically
endangered species A. bijuga, helping to identify possible
biological reasons for the limited number of plants of
this species. Nevertheless, this is only a first step towards
conserving the remaining population of A. bijuga. Their
continuous habitat fragmentation and the introduction
of alien species implies the need for futures studies to
obtain information about pollinators (diversity, abundance,
and efficiency), and their consequences on reproductive
success. Furthermore, A. bijuga conservation probably
involves studies in seed dispersion, herbivory, successful
seedling establishment, species reintroduction and habitat
management.
ACKNOWLEDGEMENTS
We thank M. Murúa, S. Cuartas and A. Conley for help
and comments. Financial support was obtained from the
following grants: DI from Universidad de Talca, PSD-66,
and VID I 09/07-2. The authors also thank two anonymous
reviewers for suggestions and criticisms that greatly
improved the manuscript.
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Recibido: 11.11.11
Aceptado: 20.04.12
