Plant Plant Species Species Biology Biology(2016) (2015)31, ••,288–295 ••–••
10.1111/1442-1984.12114 doi: 10.1111/1442-1984.12114
Better common than rare? Effects of low reproductive success, scarce pollinator visits and interspecific gene flow in threatened and common species of Tibouchina (Melastomataceae) XAVIER ROJAS RUILOVA* and ISABEL MARQUES*† *Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja, Loja, Ecuador; and †Department of Agricultural and Environmental Sciences, High Polytechnic School of Huesca, University of Zaragoza, Huesca, Spain
Abstract The reasons for plant rarity have been the focus of many studies, especially because rare species are more prone to extinction than common species. Under the same habitat conditions, rare plants are expected to attract fewer flower visitors and to show some limitation in their reproductive success. Here, using one of the most emblematic Neotropical plant genus (Tibouchina) we tested whether narrow endemic and threatened species in Ecuador have a lower reproductive success or are visited by fewer pollinators than common species, in 13 populations monitored from 2011 to 2013. We also assessed whether interspecific gene flow could be considered a threat to the rare species. However, contrary to expectations, we found that few pollinators visited the flowers, independently of species rarity. Natural outcross pollinations were always very low in all small-size populations, leading to high levels of pollen limitation. Interspecific crossing experiments also revealed weak reproductive barriers in some species. This study reveals that both narrow and common species of Tibouchina have similar reproductive and pollinator patterns in Ecuador and, therefore, other causes of the rarity of these species should be considered. Keywords: conservation, Ecuador, IUCN, rain forest, rarity, reproductive success. Received 26 March 2015; revision received 17 August 2015; accepted 20 September 2015
Introduction Understanding why some species are rare while others are quite common is one of the most important questions in ecological studies (Burne et al. 2003; Carrió et al. 2009). Ultimately, a species is considered to be rare because it lives in a narrow habitat, which may be a consequence of intrinsic processes related to the biology of the species or because its habitat has been disturbed, fragmented or destroyed (Rabinowitz 1981; Bevill & Louda 1999; Storkey et al. 2011). Rare species might also be considered threatened because species with small population sizes are more prone to local extinction through demographic and environmental stochasticity (Keller & Waller 2002; Blomqvist et al. 2010). A species is also more likely to be over-collected because of its rarity (Courchamp et al. 2006; Correspondence: Isabel Marques Email:
[email protected] © 2015 2015 The The Society Society for for the the Study Study of of Species Species Biology Biology ©
Hall et al. 2008), as occurs with many orchids (Subedi et al. 2013), sometimes leading to species extinction (Fuller 1999). In plants, the scarcity of individuals might also affect pollination visits because rare plants usually attract fewer insects than common species (Rymer et al. 2005), which leads to low levels of fruit set, unless the flowers are autogamous (Lavergne et al. 2004). Rare species might also be more prone to generalist pollinators, which may enhance the risk of pollen waste or even interspecific gene flow (Muchhala et al. 2009). In the absence of strong reproductive barriers, hybridization of rare species with widespread relatives might also lead to the extinction of the rare one through genetic assimilation or demographic swamping (Levin et al. 1996; Rhymer & Simberloff 1996). Tibouchina, a neotropical genus of woody shrubs and small trees of Melastomataceae, has 300–350 species distributed throughout the rain forests of Mexico, the
I TEN 2 X . R . R U I L O VA A N D I . M A R QF U SESS OF NARROW AND COMMON TIBOUCHINA 289 Caribbean and South America (Wurdack 1962; Guimarães & Martins 1997). Self-incompatibility and apomixis are common in the family, but not in this genus, which relies on pollinators (especially bees) to develop fruits (Campos et al. 2009; Brito & Sazima 2012; Rodrigo da Maia et al. 2013). Several species are considered to be rare and in Ecuador four species (from a total of 14 described species) are also described as threatened according to IUCN guidelines: T. anderssonii (Endangered B1ab), T. campii (Vulnerable B1ab), T. gleasoniana (Vulnerable B1+2c) and T. oroensis (Vulnerable B1ab) (World Conservation Monitoring Centre 1998; Cotton & Pitman 2004a,b,c). Nevertheless, in the Red List of Ecuadorian plant species only T. andersonii and T. oroensis were included (León-Yánez et al. 2011). In this study, we used a comparative approach to understand whether the rare Ecuadorian species of Tibouchina are indeed more threatened than the common ones. Specifically, we studied how reproductive success affects the degree of persistence of the rare and threatened T. oroensis and T. campii in comparison with two common species (T. laxa and T. longifolia). If the rate of reproductive success is connected to the degree of rarity or threat, we expect to find a greater level of success in the common species than in the rare ones. Likewise, we expect rare species to be more limited by pollination or receive fewer visits than common species. The occurrence of interspecific gene flow might also be a cause of concern because hybridization between these species has been postulated due to the existence of individuals with intermediate morphological traits in some populations. Thus, specifically, we aimed to determine: (i) if the level of reproductive success is limited by pollination, (ii) if the rare Tibouchina species are visited by fewer pollinators than the common ones and (iii) if hybridization might be considered a threat to rare species of Tibouchina.
Material and methods
Study species and sites The four species of Tibouchina studied here are showy shrubs (less than 3 m) with leaf blades usually narrowly elliptic, acute to gradually acuminate at the apex and membranaceous. The flowers are hermaphrodite, heteranthous, herkogamous and usually pentamerous, except for T. campii, which sometimes have tetramerous flowers in the same shrub. The flowers are magenta in T. laxa, purple-blue in T. oroensis and white in T. campii and T. longifolia. The petals are always glabrous except for the cilia although the style is also glabrous. Stamens are dimorphic in T. campii, T. laxa and T. longifolia and near isomorphic in T. oroensis. The fruit is capsular and each fruit can produce more than 1000 seeds. Seed dispersal is © 2015 The Society Study of Species Biology Plant Species Biologyfor 31, the 288–295
expected to be limited because seeds are not adapted to wind dispersal and simply fall to the ground around the mother plant. Tibouchina andersonii was not included in this study because it was not found in its only known locality despite multiple searches. It was last recorded in 1974 (León-Yánez et al. 2011). This study was conducted during three flowering seasons from 2011 to 2013. Experiments were carried out in 13 populations located in the south of Ecuador with population sizes ranging from five to 25 individuals in the case of rare species and from 33 to 98 individuals in the case of common species (Table 1). All populations occur in fragmented Neotropical forests, except populations YAN (Loja. Yangana–Cerro Toledo) and VAL (Zamora. Zumba– Valladolid), which occur 5 m away from the main provincial road.
Reproductive success and pollen limitation To investigate whether the breeding system and the reproductive success differ between Tibouchina species, plants received one of the following treatments: (i) flowers were emasculated and bagged (apomitic); (ii) flowers were left intact and bagged (autonomous selfpollination), (iii) flowers were emasculated, hand selfpollinated and bagged (hand self-pollination), (iv) flowers were emasculated, cross-pollinated using pollen from other flowers of the same individual plant and bagged (geitonogamous), (v) flowers were emasculated, crosspollinated and bagged (cross-pollination) and (vi) flowers were left unbagged for natural pollinations to occur (control). A total of 50 individual plants were used in each treatment. Flower buds were previously selected and bagged with 1-mm mesh nylon bags to prevent insect visits. In the supplementary pollination experiment, crosspollinations were performed using flowers of the same population. Mean fruit set and mean seed number per capsule were recorded for each treatment. All mature fruits were collected and seeds were subsequently placed in a 1% solution of triphenyl tetrazolium chloride and stored for 24 h at 30°C to evaluate seed viability. A total of 250 seeds per fruit were observed under an optical microscope (100× magnification) and the percentage of viable seeds (recorded as seeds stained) was calculated. Fruit set and seed viability were log- and square-root-transformed, respectively. The effects of treatments in rare and common species were tested with a Generalized Linear Model (GLM), with pollination treatment and populations as fixed factors and years as a random-effect factor. For each species, pollen limitation (PL; Larson and Barrett (2000) was based on fruit set (Pl) and calculated per year, as PL = 1 − (FS of control flowers/FS of cross-pollinated flowers). Reproductive assurance (RA; Eckert et al. 1996) Plant Biology ••,Biology ••–•• © 2015 The Society for the Species Study of Species
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Table 1 Geographic position, population size and type of population for the six common and rare Tibouchina species studied Type of species Rare
Rare
Common
Common
Species T. campii
T. oroensis
T. laxa
T. longifolia
Latitude
Longitude
Label
Population
Population size
−3.02
−78.47
BOM
25
Allopatric
−3.87
−78.85
CHA
15
Allopatric
−3.89 −3.75 −4.81
−78.78 −79.67 −79.11
ZAM LOJ VAL
5 12 8
Sympatric with T. longifolia Allopatric Sympatric with T. longifolia
−4.38
−79.13
YAN
11
Sympatric with T. laxa
−4.26 −3.98
−79.22 −79.18
VIL ZAM
98 76
Allopatric Allopatric
−4.38
−79.13
YAN
33
Sympatric with T. oroensis
−2.33
−78.11
MAC
79
Allopatric
−3.53
−78.45
CON
67
Allopatric
−3.89 −4.81
−78.78 −79.11
ZAM VAL
Zamora-Chinchipe. Bombuscaro Zamora-Chinchipe. Chapitza Morona-Santiago. Zambii Loja. NE of San Pablo Zamora. Zumba– Valladolid Loja. Yangana–Cerro Toledo Loja. Vilcabamba Zamora-Chinchipe. Near Zamora Loja. Yangana–Cerro Toledo Morona-Santiago. Road to Macas Zamora. Cordillera del Cóndor Morona-Santiago. Zambii Zamora. Zumba– Valladolid
56 38
Sympatric with T. campii Sympatric with T. oroensis
was estimated for fruit set as 1 − (mean production of emasculated flowers/mean production of intact flowers).
Pollinator observations To test for differences in the activity of pollinators, flower visitors were recorded in all populations during the flowering seasons of 2012 and 2013. A 1-m2 plot was set up in each population and all individual plants inside the plot were monitored during the entire blooming period. Observations were conducted on sunny days in 20-min sessions from 07.00 to 19.00 h Greenwich Mean Time (GMT) for a total of 27 sessions (9 h) per day. For each species and per year, flower visitors were monitored over 10 days for a total of 90 h. Only those flower visitors that touched the reproductive parts of the flower and were seen carrying or depositing pollen were recorded. Thus, all recorded flower visitors were potential pollinators. In each session, we recorded insect identity, the number of visits made within the plot and the time spent at each flower per session. Voucher specimens were deposited in the collection of the Universidad Técnica Particular de Loja (UTPL). To test whether rare species were visited less frequently than common species, we compared the number of visits of each insect and the time spent in each flower per session using a generalized lineal model with the identity link function and using insect identity as the dependent variable. Species, popuPlant Biologyfor ••,the ••–•• © 2015Species The Society Study of Species Biology
Type of population
lation, year and their interaction were included in the model as fixed factors. Within each population, the visits of each insect were pooled together because no significant variation was found between the two plots (P > 0.05). Variables were square-root transformed prior to the analysis due to heteroscedasticity in the untransformed data.
Level of interspecific compatibility The efficiency of reproductive barriers against hybridization was tested by performing interspecific crosses between all species in 2012, in the populations of ZAM (Morona-Santiago. Zambii) and YAN. Flower buds from each species were previously emasculated, bagged to prevent insect visits and crossed with pollen from other species. All possible crossing pollinations were conducted in both directions using 60 plants in each treatment in a total of 480 crossings performed: T. oroensis × T. laxa, T. oroensis × T. longifolia, T. campii × T. laxa and T. campii × T. longifolia. Plants were monitored for fruit set after anthesis. Mean fruit set, mean seed number per capsule and seed viability were recorded as in the first experiment. Data were transformed and analyzed by oneway ANOVA followed by a Scheffé test to evaluate the degree of reproductive isolation between species. All statistical analyses in this study were carried out using SPSS 15.0 (SPSS Inc., Chicago, Illinois, USA). © 2015 The Society Plant for theSpecies StudyBiology of Species Biology 31, 288–295
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I TEN X . R . R U I L O VA A N D I . M A R QF U SESS OF NARROW AND COMMON TIBOUCHINA 291 100.00 c c
80.00
c c
Fruit set (%)
c
60.00 b a
40.00
a
20.00
0.00
LAX
LON
ORO
common
CAM rare
Species
Fig. 1 Fruit set from open intact flowers (grey) and handcrossed-pollinated flowers (white) in two rare (T. campii and T. oroensis) and two common (T. laxa and T. longifolia) species of Tibouchina. LAX, T. laxa; LON, T. longifolia; ORO, T. oroensis; CAM, T. campii. Values indicate mean ± SD. Superscripts indicate comparisons between treatments using Scheffé’s test. Treatments with the same letter do not differ significantly (P > 0.05).
Results
Breeding system and pollen limitation Very few flowers set fruit when self-pollinated (< 1%) or even in geitonogamous crosses (< 3%), indicating that both common and rare species of Tibouchina are mainly self-incompatible. Apomitic treatments also failed to produce fruits. Consequently, these treatments were eliminated from further analyses. The possibility of reproductive assurance was therefore absent in these species. Fruit set varied between 45.75% and 81.60% in the cross-pollinations performed, whereas in open intact flowers fruit set varied between 25.01% and 87.80% (respectively, in the rare T. campii and in the common T. laxa; Fig. 1). There was a significant interaction between pollination treatments and rarity because common species had generally similar levels of fruit set, whereas in rare species fruit set was always lower when flowers were left intact (Fig. 1; Table 2). This result was consistent across years and in all populations of rare species, whereas in the common ones, significant differences were found between populations (Table 2). Fruit set of intact flowers of T. laxa and T. longifolia was significantly lower in the YAN and VAL populations than in the remaining ones (t-test: T. laxa, 51.37%, T = 3.456, d.f. = 23, P < 0.0001; T. longifolia, 32.14%, T = 3.456, d.f. = 23, P < 0.0001). The interaction between years and populations was slightly significant but only for the common species (Table 2). © 2015 The Society Study of Species Biology Plant Species Biologyfor 31, the 288–295
A high degree of pollen limitation (PL) was found in the rare species, across years and across populations (PL, T. oroensis, 0.40; T. campii, 0.45). However, this value was close to zero in the common species (PL, T. laxa, −0.07; T. longifolia, −0.08), except in the populations of YAN (PL, T. laxa, 0.37) and VAL (PL, T. longifolia, 0.52). All species developed similar amounts of seeds (average across species, 827 ± 128 seeds/fruit; GLM, F4,45 = 175.21, P = 0.871), even across years (F3,78 = 84.342, P = 0.983), but this was slightly different between populations of the same species (F4,12 = 5.351, P = 0.045). More than 75% of the seeds found inside each fruit were viable (average across species, 623 ± 98) and no differences were found between species (F4,27 = 95.782, P = 0.935), populations (F4,12 = 172.109, P = 0.918) or years (F2,26 = 89.001, P = 0.903).
Pollinator behavior and abundance Only five species (three Coleoptera and two Hymenoptera) were recording carrying and depositing pollen on flowers of Tibouchina: Otiorhynchus cuneiformis (Coleoptera), Polydrusus (Coleoptera), Diabrotica (Coleoptera), Bombus (Hymenoptera) and Eulaema (Hymenoptera). Overall, insect visits started after 10.00 h, when fog and rain conditions were less intense, and finished around 16.00 h. However, the number of visits per observation session was very low and no significant differences were found between species (GLM, F4,26 = 95.782, P = 0.935; Fig. 2). The pollen beetle, Otiorhynchus cuneiformis, was the most important visitor because 85% of flower visits were performed by this insect (F6,16 = 3.218, P = 0.003) . Similar values were found between populations (F12,78 = 4.231, P = 0.902) and years (F2,8 = 6.650, P = 0.981). The interaction population × year was also not significant (F14,31 = 1.017, P = 0.886). The beetle usually stayed in each flower for an average of 7.8 ± 4.5 min, always touching and leaving pollen on the stigma with the movements within the flower. It was also seen transferring pollen between different plants. No differences in the time spent on each flower were found between populations (F12,25 = 3.458, P = 0.872), years (F2,12 = 4.891, P = 0.783) or the interaction population × year (F14,33 = 1.871, P = 0.893). By contrast, visits by bees were very scarce and each visit lasted an average of 0.43 ± 0.39 sec per flower. Bees usually embraced the anthers, releasing pollen through vibratory movements, although they were only observed touching the stigma on 43% of their visits. The numbers of visits made by bees were similar between populations (F12,78 = 3.561, P = 0.891) and years (F2,8 = 3.791, P = 0.992). The interaction population × year was also not significant (F14,31 = 1.881, P = 0.782). Plant Biology ••,Biology ••–•• © 2015 The Society for the Species Study of Species
292 X . R . R U I L O VA A N D I . M A R Q U F IETSN E S S O F N A R R O W A N D C O M M O N T I B O U C H I N A Table 2 Analysis of variation under a univariate general linear model of fruit set in rare and common Tibouchina species
Type of species Rare
Common
5
Source
Type III SS
d.f.
MS
F
Treatment Population Year Treatment × Population Treatment × Year Population × Year Error Treatment Population Year Treatment × Population Treatment × Year Population × Year Error
51.00 533.21 953.48 163.19 56.451 141.62 167.21 234.01 142.52 563.10 782.10 45.83 78.231 89.32
1 5 2 1 2 9 18 1 6 2 1 2 11 24
51.00 106.6 476.74 163.19 28.22 15.73 9.28 234.01 23.75 281.55 782.10 22.91 7.11 3.72
5.49*** 11.47 51.32 17.56 3.03 1.69 62.87 6.38** 75.65 210.14 6.15* 1.91
Significant values are indicated in bold type (*** P < 0.0001; ** P < 0.005; * P < 0.05).
5
rare (64.83 ± 0.75) T. oroensis
(81.60 ± 0.89)l T. laxa
60.81 ± 0.83 h
.2
5
0.
05
a
.2 0
. 11
b
± 0.
25
c
08
0.
f
05
±
1
a
b
33
±
44
7.99 ± 0.54
05
0.
2.89 ± 0.88
8
.2
49
±
1.99 ± 0.93
a
a
2
0
common
f
e
a
3
45.75 ± 2.62
g
a
5.01 ± 0.87
Number of insects/ 20 min
4
i
LAX
LON
ORO
common
CAM rare
Species
Fig. 2 Number of pollinators recorded per 20-min observation sessions. LAX, T. laxa; LON, T. longifolia; ORO, T. oroensis; CAM, T. campii. Values indicate mean ± SD. Superscripts indicate comparisons between treatments using Scheffé’s test and have the same letter because they do not differ significantly (P > 0.05).
T. campii f (45.75 ± 2.62)
72.05 ± 0.50 k 24.50 ± 0.89 d
T. longifolia i (65.89 ± 1.10)
Fig. 3 Reproductive isolation between rare (T. campii and T. oroensis) and common (T. laxa and T. longifolia) species of Tibouchina based on fruit set (mean ± SD). The direction of the arrows indicates the maternal progenitor in the interspecific cross performed. Thickness is proportional to breeding compatibility between species. Values in parentheses indicate fruit set from intraspecific crossings. Superscripts indicate comparisons between treatments using Scheffé’s test and have the same letter because they do not differ significantly (P > 0.05).
Level of interspecific compatibility Breeding compatibility varied considerably between the four species of Tibouchina (F3,19 = 495.544; Fig. 3). Fruit set was minimal when interspecific crosses were performed between the two rare species (T. oroensis × T. campii, < 8%) or between the two common species (T. laxa × T. longifolia, < 3%). However, interspecific crosses between a common and a rare species generally led to a high formation of fruits when the rare species acted as the mother progenitor, although a significant reduction was found in the opposite crosses (Fig. 3). Two interspecific crosses perPlant Biologyfor ••,the ••–•• © 2015Species The Society Study of Species Biology
formed on the flowers of T. campii resulted in a higher amount of fruit set than the intraspecific cross (T. campii × T. longifolia and T. campii × T. laxa). All crossing experiments produced similar amounts of seeds per fruit, with the exception of the treatments between the two common and the two rare species, where a significant reduction was found (808 ± 115 vs. 127 ± 84 seeds/fruit; GLM, F15,74 = 3734.251, P = 0.0001). Seed viability was similar between crossing experiments (F15,71 = 1.710, P = 0.679). © 2015 The Society Plant for theSpecies StudyBiology of Species Biology 31, 288–295
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Discussion
Reproductive success and visitation rates are not linked to rarity Contrary to our expectations, both common and rare species of Tibouchina were found to be primarily selfincompatible and consequently, reproductive assurance was inexistent. Although species of Tibouchina are usually reported as self-compatible (Campos et al. 2009; Franco et al. 2011; Brito & Sazima 2012; dos Santos et al. 2013), the species studied here are self-incompatible, like T. aegopogon (Almeda 1977). Selfing can be an advantage because it allows reproduction even when few mates are available (Marques & Draper 2012), while obligate or mainly outcrossing species maintain high levels of genetic diversity only if there is continuous exchange of genes with other populations (Honnay & Jacquemyn 2006; Ellstrand 2014). However, in our study, reproductive success (fruit set, seed number and seed viability) was not higher in the common species of Tibouchina than in the rare or threatened ones and a high rate of pollen limitation was found. Likewise, contrary to expectations, the amount of insect visits to flowers of Tibouchina was very low, independently of whether they were rare or common species. Despite being showy bushes with a high density of flowers and an extended flowering period, flowers were visited by few insects. Bees, which are usually recorded as main pollinators in Tibouchina (Brito & Sazima 2012; Rodrigo da Maia et al. 2013; Brito et al. 2015), were scarcely seen in our populations and the main pollinator was the pollen beetle Otiorhynchus cuneiformis. Although pollination by beetles assumes an important role in environments with low pollination activity like the ones reported here (Sakai et al. 1999), it might also lead to high levels of pollen robbery (Hargreaves et al. 2009). In our populations we have not seen any holes in flowers or other signs of damage that might be caused if beetles were only acting as pollen thieves. Our observations also recorded the transfer of pollen between flowers, thereby confirming the role of these beetles as pollinators. However, it is still necessary to further evaluate the efficiency of this insect as a pollinator and the impact of pollen consumption on the reproductive success of Tibouchina.
Causes of low insect activity A possible explanation for the low pollination activity comes from the unfavorable abiotic conditions in our study locations because there was always a high degree of humidity coupled with frequent rainfall and foggy weather, which seems to affect visitation rates in other species in the same area (Vega et al. 2013; Vega & Marques © 2015 The Society Study of Species Biology Plant Species Biologyfor 31, the 288–295
2015). Studies performed on other species of Tibouchina reported an increase in the frequency of insect visits when humidity was lower and temperature higher, favoring pollen extraction (Franco et al. 2011; Brito & Sazima 2012). If cross-breeding is low, as expected from the low number of visits, then populations are more vulnerable to habitat destruction and fragmentation because the exchange of genes becomes less likely (Lopez et al. 2009). Also, small populations become too isolated to attract pollinators, which explains the high levels of pollen limitation found in the rare species, and without the possibility of reproductive assurance, population numbers might become critically low (Becker et al. 2011; Geslin et al. 2013).
Is there a potential role for hybridization in Tibouchina? The formation or the survival of hybrid plants is thought to be quite infrequent in Tibouchina because only one study pinpoints hybridization as the origin of one endemic Brazilian species of Tibouchina (Wu et al. 2009). Nonetheless, evidence from our study suggests that hybridization might be more common than previously suspected in Tibouchina, at least in these species. First, flowering asynchrony was very low because all sympatric species have similar flowering phenologies and there was always a high percentage of flowering plants from co-occurring species throughout the flowering period. Second, all species of Tibouchina were visited by the same pollinators and there is no evidence of a specialized plant– pollinator relationship. Although it is true that more detailed studies should be conducted in order to assess pollinator preference and efficiency in these species of Tibouchina, results so far do not indicate that pollinators are a strong barrier to interspecific gene flow. Finally, the high values obtained in some interspecific crosses suggest that hybridization might be a matter of concern in sympatric populations. Without molecular support, these results do not necessary imply that hybridization is occurring in natural populations because both pre- and post-zygotic barriers might be acting to constrain natural interspecific gene flow (Marques et al. 2014; Pinheiro et al. 2015). Nevertheless, an ongoing molecular study confirms the presence of hybrids in some populations (Marques et al., unpublished data), highlighting the need for future studies focusing on discovering the degree of hybridization in these natural populations and the factors that maintain species isolation in Tibouchina. If introgression and backcrossed hybrids are present, future projects for recovery of the threatened species would also have to implement measures that avoid the genetic swamping of species. Plant Biology ••,Biology ••–•• © 2015 The Society for the Species Study of Species
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Acknowledgments This study was funded by UTPL and performed as the final project by JRR for the signature of reproductive biology in tropical plants. We are grateful for the comments made by an anonymous reviewer on a previous version of this manuscript.
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