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Population Biology |
2Musée national d'histoire naturelle, 25 rue Munster, L-2160 Luxembourg; 3Institut für Umweltwissenschaften, Universität Zürich, CH-8057 Zürich, Switzerland; 4Pflanzenökologie, Fachbereich Biologie, Philipps-Universität Marburg, D-35032 Marburg, Germany
Received for publication September 12, 2003. Accepted for publication June 1, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Asteraceae • breeding system • geitonogamy • offspring fitness • pollen limitation • pollen quality • pollen quantity • Scorzonera humilis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Holsinger, 2000
). In small, isolated populations genetic diversity decreases due to random genetic drift (e.g., Fischer and Matthies, 1998a
; Paschke et al., 2002
), and the probability of crossings between closely related individuals increases, resulting in inbreeding. Inbreeding can strongly reduce both individual and population viability (Keller and Waller, 2002
), and negative effects of small population size on offspring fitness have been found in many species (Fischer and Matthies, 1998b
; Morgan, 1999
; Kéry et al., 2001
).
To increase the vigor of plants in fragmented populations, increasing the gene flow between populations to enhance levels of heterozygosity has been suggested (Oostermeijer et al., 1995
). Several experimental studies have found that between-population crosses increase offspring vigor in comparison to within-population crosses (Oostermeijer et al., 1995
; Byers, 1998
; Sheridan and Karowe, 2000
). However, interpopulation outcrossing may also result in reduced performance of the offspring (outbreeding depression) if the parental plants are adapted to local conditions or if coadapted gene complexes become disrupted (Waser and Price, 1989
; Fischer and Matthies, 1997
; Montalvo and Ellstrand, 2001
). If both inbreeding and outbreeding depression occur there may be an optimal outcrossing distance (Waser and Price, 1989
).
Many plants rely on animal pollinators for the transfer of pollen onto their stigmas for ovule fertilization. However, in fragmented populations plant–pollinator interactions may become disrupted and reproduction may be reduced because of insufficient pollination (pollen limitation) (Kearns et al., 1998
; Moody-Weis and Heywood, 2001
). Plants in small populations are often less attractive to pollinators and may be visited less frequently (Rathcke and Jules, 1993
). Moreover, in small populations, the local density of plants is often reduced and there is less pollen transfer between individuals (Kunin, 1997
; Roll et al., 1997
). Nearly all studies of the effects of density on plant reproduction have found that both pollination and reproductive success decrease in sparse populations (Kunin, 1997
; Roll et al., 1997
; Bosch and Waser, 2001
).
The sensitivity of the reproduction of plants to fragmentation depends on their mating system. Self-incompatible species are more likely to be affected by pollen limitation than self-compatible species, because they cannot compensate for reduced pollinator services by selfing (DeMauro, 1993
; Byers, 1995
). Moreover, in small and isolated populations the diversity of pollen genotypes is reduced and it is more likely that flowers will receive incompatible pollen (Byers and Meagher, 1992
; Byers, 1995
). For example, in a very small population of Hymenoxys acaulis (Pursh) K. L. Parker (Asteraceae), all plants possessed the same self-incompatibility type (DeMauro, 1993
), and in the distylous Primula veris L. (Primulaceae) a single mating type became increasingly dominant with decreasing population size (Kéry et al., 2003
).
Pollen limitation may not only reduce seed set but also progeny vigor by reducing the selectivity among gametes (i.e., pollen competition) before and during fertilization (Palmer and Zimmerman, 1994
; Winsor et al., 2000
). For example, the progeny from fruits receiving high pollen loads outperformed the progeny from fruits receiving low pollen loads for several traits in Campanula americana L. (Campanulaceae) (Richardson and Stephenson, 1992
), and in Cucurbita foetidissima Kunth progeny produced by multiple pollinator visits were more vigorous than those produced by single visits (Winsor et al., 2000
). However, there are hardly any studies of the effects of pollen limitation on progeny fitness in natural populations (Brown and Kephart, 1999
).
We studied reproduction and offspring fitness of the rare, long-lived plant Scorzonera humilis L. (Asteraceae) in relation to pollen quality and quantity and the effect of interpopulation gene flow. Populations of S. humilis have become increasingly fragmented in recent decades (Colling et al., 2002
). Moreover, due to the eutrophication of sites, mean plant size has increased in many populations, which could affect reproductive success because with increasing plant size the probability of within-plant pollen transfer (geitonogamy) may increase (De Jong et al., 1992
).
To study the effects of cross proximity on reproductive success, we excluded natural pollinators and performed hand-pollinations with pollen from the same plant, from other plants in the same population, and from plants in other populations. We grew the offspring in a common garden and analyzed the effects of cross-proximity on various fitness-related traits. We studied in several populations whether reproduction was pollen limited by supplementing natural pollination with hand-pollination of flowers and analyzed the effect of pollen quantity on offspring performance. In addition, effects of plant size and density on the reproduction of S. humilis were studied in one large population.
We addressed the following questions: (1) Is S. humilis self-compatible and does seed set depend on pollinators? (2) Does plant size and density affect reproduction? (3) Is reproduction pollen limited? (4) Does pollen quantity and cross proximity influence offspring fitness?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Korneck et al., 1996
). The main reasons for its decline are the use of fertilizers, drainage of habitats, and land reclamation. Many populations are now very small and isolated due to intense fragmentation of the remaining habitats.
A single plant (genet) of S. humilis may consist of 1–100 rosettes in a dense cluster that are connected to a large tap root (Colling et al., 2002
). Each rosette can produce 1–3 inflorescences in May–June. The flowering period of an individual plant is in general short and does not exceed 1 wk (Schwabe and Kratochwil, 1986
). The flowers are pollinated by apoid Hymenoptera, Lepidoptera, Diptera, and Coleoptera (Schwabe and Kratochwil, 1986
). A single inflorescence can produce 26–76 achenes (hereafter called seeds), which have a pappus and are wind-dispersed. However, the seeds are large (ca. 2.6 mg), and dispersal distance is very limited. Seeds of S. humilis germinate after rainfalls in late summer or in the following spring and the seedlings grow into small rosettes during their first year. The flower heads are frequently parasitized by larvae of the seed fly Heterostylodes macrurus (Schnabl in Schnabl and Dziedzicki, 1911) (Diptera, Anthomyidae), which destroy the developing seeds in the center of the flower heads.
Experiment 1: effect of pollinator exclusion and interparental distance
In mid-May 1998, we randomly selected 33 plants of S. humilis that had at least five unopened flower heads in the largest population in Luxembourg (>5000 plants) at Werwelslach (WERWEL), ca. 10 km west of the city of Luxembourg. At this time, most of the plants in the population were already flowering. We determined the maximum length and width of each plant and calculated the plant area (length times width) as a measure of plant size.
On each individual plant five different pollination treatments were carried out, each on a single randomly selected flower head on a separate inflorescence: (1) One flower head was marked with a plastic ring but otherwise left untouched to investigate the reproductive success of open-pollinated inflorescences ("open pollination"). After the flower heads had withered, they were bagged with fine nylon mesh to prevent dispersal of the seeds. For the other four treatments, flower heads were caged at the start of the experiment with bags made of fine nylon mesh (mesh size ca. 0.8 mm) to prevent insects from visiting. (2) One of the caged flower heads was left untouched to investigate the possibility of autonomous self-pollination ("caged"). (3) One flower head was hand-pollinated with pollen from the same flower head ("selfed"). (4) Another flower head was hand-pollinated with pollen from three randomly collected flower heads of three other plants from the same population that were located at least 10 m and but not more than 30 m from the recipient plant (within-population crosses [WPC]). (5) Another flower head was hand-pollinated with pollen from three randomly collected flower heads of three plants from two large populations (each >4000 plants) about 10 km away (between-population crosses [BPC]).
All hand-pollination treatments were carried out twice. At the first pollination, the florets at the edge of the flower heads were receptive, and at the second pollination 3 d later the florets at the center were receptive. We carried out the hand pollinations by gently transferring pollen from the anthers to the receptive stigmata with small paintbrushes. For each pollinated flower head a new brush was used. Complete flower heads were transported between populations individually in small plastic bags and all pollinations were carried out within 3 h after collection. All fruiting flower heads were collected in mid-June 1998 before mowing of the sites, and the number of developed seeds and the number of seeds destroyed by the seed fly H. macrurus were counted per flower head. Aborted seeds and seeds destroyed by the fly can be easily distinguished, because the larvae only attack developing seeds, which are much larger than aborted seeds. Seed predation occurred only in open-pollinated flower heads because hand-pollinated flower heads were protected by the mesh bags. The healthy seeds were dried at room temperature for 2 mo, weighed individually, and stored individually in plastic bags at 6°C until the start of the germination tests.
On 14 January 1999 the 359 seeds were placed on wet filter paper in petri dishes and each seed was assigned a number, allowing the fate of individual seeds to be followed. A maximum of five seeds of the same pollination treatment, but from different plants, were placed in each petri dish. To break dormancy, the seeds were stratified at 4°C in darkness for 6 wk, after which they were kept at 20°C under a light regime of 12 h day/12 h night.
We checked the seeds every second day for germination (development of a radicle). Seedlings that had developed green cotyledons were transplanted into soaked peat pellets (Jiffy pots) when the cotyledons had reached a length of 2 cm. All seedlings were transplanted within 1 wk. The seedlings were randomly placed into trays and received light from fluorescent tubes (Sylvania GRO-LUX, Germany) for 16 h/d. We re-randomized the position of the seedlings every 2 wk.
After 28 d of growth the sum of the lengths of all leaves (cumulative leaf length) was determined for each surviving plant. After 56 d of growth the young plants were transplanted into pots 12 cm in diameter that contained low-nutrient soil (0.5 g/L of fertilizer, N : P : K 15 : 10 : 20) and transferred to a common garden. Plants were watered regularly when necessary. After 95 d the cumulative leaf length was determined a second time. Finally, in mid-May 2000, after 420 d (60 wk) of growth, the total number of leaves was determined for each surviving plant.
To study the effects of the experimental treatments on offspring performance, several multiplicative fitness functions were calculated. The number of seedlings per flower head was calculated as the product of the number of seeds per flower head and the proportion of germinated seeds. The number of seedlings per flower head at various times (see Table 1) was calculated as (number of seeds per flower head) x (proportion of germinated seeds) x (proportion of plants surviving). To calculate the cumulative leaf length per flower head and the number of leaves per flower head, the number of seedlings per flower head was multiplied by the mean cumulative leaf length of the plants or the mean number of leaves of the plants, respectively. To allow comparisons between the fitness of open-pollinated plants, whose seeds were destroyed by the fly H. macrurus, with that of caged plants, which were not, additional fitness functions excluding the effect of the predators were calculated.
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Experiment 2: pollen limitation and the effects of supplementary hand pollination
To investigate whether the reproduction of S. humilis was pollen limited, we carried out supplementary hand pollinations in four populations located less than 30 km from the city of Luxembourg. Two of the populations, WERWEL and Schiltzenheck (SCHIL), were large (> 4000 plants) and two of them, Capellen (CAPEL) and Oberpallen (OBER), were of medium size (>190 plants).
On 28 May 1998, between 15 and 31 flowering plants were randomly chosen and marked in each population and subjected to one of three treatments. Differences in the number of treated plants were due to the small number of flowering individuals in the smaller populations at the time of the experiment. Only one flower head per plant was used in the study. Each flower head was either left untouched and was only pollinated by insects or was hand-pollinated in addition. For supplementary pollination the plants received pollen from three other plants, either from the same population or from a population at Bitchenheck. The pollen donors for the within-population crosses were at least 10 m and not more than 30 m from the recipient plants and the pollen donor population was at least 10 km from each study population.
Hand pollinations were carried out in the same way as described for Experiment 1, but flower heads were pollinated only once when the florets at the edge were receptive. After the flower heads had withered, we bagged them to prevent dispersal of the seeds. The flower heads were collected in mid-June 1998 before the sites were mown. Seeds at the edge and in the center of the flower head were separated and counted. The number of seeds counted included those seeds in the center that had been destroyed by the seed fly H. macrurus. Because only florets at the edge of each flower head had been hand-pollinated, only their seeds were used for further studies. These seeds were dried at room temperature, weighed individually, and stored at 6°C (see Experiment 1).
On 26 May 1999 all the seeds were placed in petri dishes for germination tests, and the seedlings were later transplanted into peat pellets. We used 124– 200 seeds per treatment and 97–275 seeds per population. Procedures were the same as described for Experiment 1, except that eight seeds from the same population (but not necessarily from the same treatment) were placed in each petri dish. After 84 d of growth the cumulative leaf length of surviving plants was determined and multiplicative fitness functions were calculated as for Experiment 1.
In Experiment 2 we considered population as a fixed effect, because we studied only four selected populations. The factor population was crossed in a two-factorial design with the factor pollination treatment (three levels). We partitioned the effect of pollination treatment into two orthogonal contrasts: (1) open pollination vs. additional hand pollination and (2) additional pollination with pollen from the same population vs. additional pollination from a different population. The interactions between population and pollination treatment were partitioned in an analogous way. All effects were tested against the residual variation among plants. Data were transformed if necessary prior to analysis to achieve normally distributed residuals and homogeneity of variances. All analyses were carried out with SPSS for Windows 11.0 (SPSS, 2001
).
Effects of plant size, plant density, and position of flower heads
To study the effects of geitonogamy and the availability of potential pollen donors we randomly selected 35 plants of different size in areas of different plant density in the population WERWEL at the end of May 2002. Within each plant we randomly selected one flower head that had not yet opened and marked it with a colored string. Two days later, when the marked flower heads were flowering, we counted for each plant the number of flower heads with open florets. At the same time we also counted the number of flowering plants within radii of 1, 2, and 4 m distance to the target plant. These data were used to calculate the number of flowering plants in concentric rings (0–1, 1–2, and 2–4 m distance) around the target plants.
At the time of seed ripening in mid-June we collected the marked flower heads and counted the number of florets and seeds. Two types of seeds were distinguished: healthy seeds, which are hard and black or green, and seeds destroyed by the larvae of the fly H. macrurus. A flower head was considered parasitized if at least one seed had been destroyed by H. macrurus. Seeds attacked by H. macrurus were counted as developed for the calculation of the potential (gross) seed set because the larvae feed only on developing seeds. Potential seed set was calculated as the ratio between the number of developed seeds and the total number of florets per flower head. Realized (net) seed set was calculated as the ratio between the number of healthy seeds and the number of florets per flower head.
If geitonogamy is frequent, flowers at the edge of a plant may be more likely to receive cross pollen than flowers in the center of a plant. To study the effect of the position of a flower head within a plant on seed production, we randomly selected 15 large plants with at least 20 open flower heads in the population WERWEL at the end of May 2002. For each plant, we randomly selected two flower heads from the edge and two flower heads from the center and marked them with a colored string. At the time of seed ripening in mid-June we collected the marked flower heads. In each flower head the number of florets and seeds was counted and the potential seed set and realized seed set were calculated as described above.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The germination of seeds resulting from open pollination was higher than that of seeds from flowers subjected to the other treatments, but this effect was not significant. In contrast, the number of seedlings per flower head, a multiplicative fitness measure at the germination stage, was much higher for between-population crosses than for selfing.
Treatments consistently influenced multiplicative fitness measures at later dates. At the end of the experiment, multiplicative fitness could be ranked from low to high as selfed < open pollination < within-population crosses < between-population crosses, but only differences between selfed and interpopulation crosses were significant (Table 1). However, without seed predation, all multiplicative fitness measures for open pollination would have been similar to those of within-population crosses by hand.
Most of the measures of plant performance differed significantly between the descendents of the different individual plants (Table 1), and these differences persisted to the end of the experiment. The mean number of seeds per flower head for different plants ranged from 0 to 34, mean seed mass from 1.2 to 4.3 mg, and the mean number of surviving offspring per flower head from 0 to 3.5 individuals. However, the performance of offspring measured as cumulative leaf length after 95 d was not related to the size of the maternal plant (P > 0.3), because plant size explained only a small part of the differences between plants (r2 = 0.03).
Pollen limitation and effects of pollen source
Supplementary hand pollination resulted in a significant increase of ca. 44% in the number of seeds per flower head in all four studied populations, indicating that seed set was pollen limited (Fig. 1a, Table 2). The source of the supplementary pollen (from the same or a different population) had no effect. Mean seed mass was not affected by the treatments but varied between the studied populations. Seeds were significantly larger in the populations OBER (3.4 mg) and CAPEL (3.1 mg) than in SCHIL (2.6 mg) and WERWEL (2.5 mg) (Table 2). The following traits could only be determined for three of the populations because none of the seeds collected in WERWEL germinated. Germination of seeds from SCHIL (17%) was much lower than that of seeds from OBER (97%) and CAPEL (83%). The effect of hand pollination varied between populations. While in SCHIL hand pollination increased the germination of seeds compared with open pollination, it had no effect in the other two populations (Fig. 1b).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Richards, 1997
). In this system, the behavior of the pollen is determined by the genotype of its parent (Heslop-Harrison, 1975
).
However, the self-incompatibility system in S. humilis is not perfect because 12% of the plants produced seeds after self-pollination by hand. Interestingly, the performance of offspring from self-pollination was not lower than that of offspring from outcrossing. A partial breakdown of the self-incompatibility system has been found in other plants, e.g., in Aster furcatus Burgess (Asteraceae) (Reinartz and Les, 1994
), Eupatorium perfoliatum L. (Asteraceae) (Byers, 1995
), Arnica montana L. (Asteraceae) (Luijten et al., 1996
), and Campanula rapunculoides L. (Campanulaceae) (Stephenson et al., 2000
).
Supplementary hand pollination consistently increased seed production in S. humilis, indicating that reproduction was pollen limited even in the two large populations (>3000 plants). Similarly, in Experiment 1, experimental cross pollinations resulted in higher seed set than open pollinations. There is increasing evidence that seed set in natural populations of plants is frequently pollen limited (Bierzychudek, 1981
; Burd, 1994
), in particular in self-incompatible plants (Larson and Barrett, 2000
; Ramsey and Vaughton, 2000
). Possible causes of pollen limitation include low activity of pollinators that result in insufficient numbers of pollen on stigmas to fertilize all ovules and compatibility type of pollen. The sporophytic self-incompatibility system of Asteraceae not only prevents self-fertilization but also crossing between closely related individuals (Richards, 1997
). In plant populations neighboring individuals are commonly more closely related because seed dispersal and pollen exchange is limited (Levin, 1984
). Because pollinators often move only short distances between plants, pollen may frequently be transferred between related incompatible individuals (Waser and Price, 1991
). A large number of S-alleles is necessary for maintaining a high level of cross-compatibility in populations of self-incompatible species like S. humilis (Byers and Meagher, 1992
). Self-compatible genotypes will be at a selective advantage in populations that lack a sufficient number of S-alleles to produce compatible crosses (Reinartz and Les, 1994
), and fragmentation might therefore be expected to favor the evolution of self-compatibility in S. humilis. However, fragmented populations have a high risk of extinction, because of their sensitivity to environmental stochasticity (Matthies et al., 2004
).
Seed set of S. humilis increased with the number of flowering conspecifics in the immediate vicinity (within 1 m) of a plant. Including conspecifics at greater distances (1–4 m) did not improve the proportion of variation explained. This suggests that processes operating at a small scale influenced seed set most. Similarly, the number of conspecifics within only 1 m distance most strongly influenced the reproduction of the desert plant Lesquerella fendleri (Gray) S. Watts (Brassicaceae) (Roll et al., 1997
). High-density patches are often more attractive for pollinators (Roll et al., 1997
; Bosch and Waser, 2001
), resulting in increased pollination. The intensity of pollen limitation in S. humilis may therefore depend on local density and may vary within populations. Moreover, the mean intensity of pollen limitation in a population will depend on its spatial structure.
Reproduction of S. humilis was also influenced by individual plant size. The number of developing seeds per flower head was lower in large plants with many flower heads than in small plants. This is probably a consequence of more geitonogamy in large plants. Because pollinators tend to move between neighboring flowers, the probability of pollen transfer between flower heads of the same plant increases with plant size (De Jong et al., 1992
; Rademaker and De Jong, 1998
). As a consequence, less xenogamous pollen is available to fertilize ovules. Moreover, large amounts of self-pollen may clog the stigma surface and may strongly reduce subsequent germination of compatible pollen (Galen et al., 1989; Waser and Price, 1991
). This explanation for the reduced seed set in large plants of S. humilis is supported by the higher seed set of flower heads at the edge of individual plants. Because pollinators first visit flower heads at the edge of a plant, these will be more likely to receive xenogamous pollen than flower heads in the center of a plant.
For plants increased geitonogamy is thought to be an unavoidable cost of increased flower numbers (Charlesworth and Charlesworth, 1987
; Ramsey and Vaughton, 2000
). However, it has been suggested that the deleterious effects of geitonogamy on female fecundity in large plants may be compensated by other factors such as size-related fruit or seed abortion (De Jong et al., 1992
). Our results show that reduced seed parasitism is a mechanism that may mask the negative effects of increased geitonogamy in large plants. Because in S. humilis the probability of predation of the developing seeds by the seed parasite H. macrurus decreased with plant size, realized seed set was not related to plant size.
In S. humilis supplementary hand pollination not only increased the number but also the quality of seeds produced. The survival of offspring from flowers that received supplementary pollen was nearly twice that of offspring from flowers that were only naturally pollinated. These effects persisted to the end of the experiment after 12 wk of growth. Moreover, in one of the studied populations, germination of seeds was also increased by pollen supplementation. There are two nonmutually exclusive explanations for the increased fitness of progeny of flowers that received supplementary pollen. First, if most of the pollen deposited by pollinators originated from plants in the immediate vicinity, which are commonly closely related, supplementary pollen from plants at least 10 m away may have reduced the mean level of inbreeding and thus reduced inbreeding depression in the progeny. Second, the higher pollen load due to supplementary pollination could have increased selectivity among gametes before and during fertilization by increased pollen competition or female choice (Winsor et al., 2000
; Kalla and Ashman, 2002
). When many more pollen grains are present at a stigma than ovules are available, the fastest growing pollen tubes will likely achieve fertilization (Winsor et al., 1987
). Because there is often a positive relationship between pollen vigor and progeny fitness (e.g., Winsor et al., 1987
; Mitchell, 1997
; but see Walsh and Charlesworth, 1992
), pollen competition can substantially increase offspring fitness. Selection on gametophytes is thought to be an efficient means of removing deleterious alleles at loci important for both the gametophytic and sporophytic stages of the life cycle (Charlesworth and Charlesworth, 1992
).
Self-incompatibility systems are thought to be advantageous because they help to avoid the deleterious effects of inbreeding and simultaneously preserve the opportunity for cross-fertilization (Winsor et al., 1987
). However, our results suggest that in the study populations of S. humilis there was either inbreeding depression in spite of the incompatibility system or offspring fitness was lower because pollen competition was reduced due to pollen limitation. Because pollen limitation is more frequent in self-incompatible species (Ramsey and Vaughton, 2000
), such an indirect reduction of offspring fitness via reduced pollen competition could be a frequently neglected effect of self-incompatibility. However, there are few other studies that have simultaneously demonstrated pollen limitation of reproduction in natural populations and analyzed possible effects of pollen limitation on progeny fitness (Brown and Kephart, 1999
).
We found that S. humilis is likely to be sensitive to habitat fragmentation. Because of its self-incompatibility system, pollen limitation is likely in small and isolated populations, in particular as local plant density tends to be lower in small populations (Colling and Matthies, 2004
) and seed set is reduced at low densities. The increased pollen transfer between closely related individuals due to fragmentation will also reduce progeny vigor, because S. humilis appears to be sensitive to inbreeding. At the individual level, the effects of plant size, pollinator behavior and herbivore behavior on reproduction may interact in a complex way with the effects of population size and density.
To prevent loss of genetic diversity and inbreeding depression in fragmented populations, occasional artificial enhancement of interpopulation gene flow has been suggested as a management tool (Van Treuren et al., 1993
). However, caution is necessary because interpopulation crosses may result in outbreeding depression (Waser and Price, 1989
; Fischer and Matthies, 1997
). In S. humilis we found inbreeding depression generally to be a greater problem than F1 outbreeding depression for the spatial scale examined (10–30 km). However, outbreeding depression could be more pronounced in later generations or if the distance between crossed populations were larger (Fenster and Galloway, 2000
; Hufford and Mazer, 2003
). In Experiment 1, seed production, seed mass, and seed germination following between-population crosses were consistently higher than following within-population crosses, although these differences were not significant. In Experiment 2, the effects of the source of the supplementary pollen varied between populations. There were indications of slight outbreeding depression following addition of far pollen in one population and no differences between pollen sources in the second population. In contrast, in the third population progeny resulting from open crosses and from flowers supplemented with pollen from the same population did not survive, while survival of progeny following supplemental pollination with pollen from a different population was high, indicating strong inbreeding depression. Management measures to enhance gene flow among fragmented populations of S. humilis may therefore increase offspring vigor, at least when the distances between the populations are not large.
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FOOTNOTES |
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5 Reprint requests: Musée national d'histoire naturelle, 25 rue Munster L-2160 Luxembourg (E-mail: guy.colling{at}mnhn.lu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bosch M. N. M. Waser 2001 Experimental manipulation of plant density and its effects on pollination and reproduction of two confamilial montane herbs. Oecologia 126: 76-83[CrossRef][ISI]
Brown E. S. Kephart 1999 Variability in pollen load: implications for reproduction and seedling vigor in a rare plant, Silene douglasii var. oraria. International Journal of Plant Sciences 160: 1145-1152[CrossRef][ISI][Medline]
Burd M. 1994 Bateman's principle and plant reproduction—the role of pollen limitation in fruit and seed set. Botanical Review 60: 83-139[CrossRef][ISI]
Byers D. L. 1995 Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae). American Journal of Botany 82: 1000-1006[CrossRef][ISI]
Byers D. L. 1998 Effects of cross proximity on progeny fitness in a rare and a common species of Eupatorium (Asteraceae). American Journal of Botany 85: 644-653[Abstract]
Byers D. L. T. R. Meagher 1992 Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68: 353-359[ISI]
Charlesworth D. B. Charlesworth 1987 Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268[CrossRef][ISI]
Charlesworth D. B. Charlesworth 1992 The effects of selection in the gametophyte stage on mutational load. Evolution 46: 703-720[CrossRef][ISI]
Colling G. D. Matthies 2004 The effects of plant population size on the interactions between the endangered plant Scorzonera humilis, a specialised herbivore, and a phytopathogenic fungus. Oikos 105: 71-78[CrossRef][ISI]
Colling G. D. Matthies C. Reckinger 2002 Population structure and establishment of the threatened long-lived perennial Scorzonera humilis in relation to environment. Journal of Applied Ecology 39: 310-320[CrossRef][ISI]
De Jong T. J. N. M. Waser M. V. Price R. M. Ring 1992 Plant size, geitonogamy and seed set in Ipomopsis aggregata. Oecologia 89: 310-315[ISI]
De Mauro M. 1993 Relationship of breeding system to rarity in the lakeside daisy (Hymenoxys acaulis var. glabra). Conservation Biology 7: 542-550[CrossRef][ISI]
Fenster C. B. L. F. Galloway 2000 Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conservation Biology 14: 1406-1412[CrossRef][ISI]
Fischer M. D. Matthies 1997 Mating structure, inbreeding and outbreeding depression in the rare plant Gentianella germanica. American Journal of Botany 84: 1685-1692[Abstract]
Fischer M. D. Matthies 1998a RAPD variation in relation to population size and plant fitness in the rare Gentianella germanica (Gentianaceae). American Journal of Botany 85: 811-819[Abstract]
Fischer M. D. Matthies 1998b The effect of population size on performance in the rare plant Gentianella germanica. Journal of Ecology 86: 195-204[CrossRef][ISI]
Galen C. T. Gregory L. F. Galloway 1989 Costs of self-pollination in a self-compatible plant, Polemonium viscosum. American Journal of Botany 76: 1675-1680[CrossRef][ISI]
Heslop-Harrison J. 1975 Incompatibility and the pollen–stigma interaction. Annual Review of Plant Physiology 26: 403-425[ISI]
Holsinger K. E. 2000 Demography and extinction in small populations. In A. G. Young and G. M. Clarke [eds.], Genetics, demography and viability of fragmented populations, 55–74. Cambridge University Press, Cambridge, UK
Hufford K. M. S. J. Mazer 2003 Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends in Ecology and Evolution 18: 147-155[CrossRef]
Kalla S. E. T.-L. Ashman 2002 The effects of pollen competition on progeny vigor in Fragaria virginiana (Rosaceae) depend on progeny growth environment. International Journal of Plant Sciences 163: 335-340[CrossRef]
Kearns C. A. D. W. Inouye N. M. Waser 1998 Endangered mutualisms: the conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics 29: 83-112[CrossRef][ISI]
Keller L. F. D. M. Waller 2002 Inbreeding effects in wild populations. Trends in Ecology and Evolution 17: 230-241[CrossRef]
Kéry M. D. Matthies M. Fischer 2001 Interactions between the rare plant Gentiana cruciata and the specialized herbivore Maculinea rebeli. Journal of Ecology 89: 418-427[CrossRef]
Kéry M. D. Matthies B. Schmid 2003 Demographic stochasticity in small remnant populations of the distylous plant Primula veris. Basic and Applied Ecology 4: 197-206[CrossRef][ISI]
Korneck D. M. Schnittler I. Vollmer 1996 Rote Liste der Farn- und Blütenpflanzen (Pteridophyta et Spermatophyta) Deutschlands. Schriftenreihe für Vegetationskunde 28: 21-187
Kunin W. E. 1997 Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology 85: 225-234[CrossRef]
Lambinon J. J.-E. De Langhe L. Delvosalle J. Duvigneaud 1992 Nouvelle Flore de la Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des Régions voisines (Ptéridophytes et Spermatophytes). Editions du Patrimoine du Jardin botanique national de Belgique, Meise, Belgium
Larson B. M. H. S. C. H. Barrett 2000 A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69: 503-520[CrossRef]
Levin D. A. 1984 Inbreeding depression and proximity dependent crossing success in Phlox drummondii. Evolution 38: 116-127[CrossRef][ISI]
Luijten S. H. J. G. B. Oostermeijer N. C. Van Leeuwen H. C. M. Den Nijs 1996 Reproductive success and clonal genetic structure of the rare Arnica montana (Compositae) in the Netherlands. Plant Systematics and Evolution 201: 15-30[CrossRef][ISI]
Matthies D. I. Bräuer W. Maibom T. Tscharntke 2004 Population size and the risk of local extinction: empirical evidence from rare plants. Oikos 105: 481-488[CrossRef][ISI]
Menges E. S. 1998 Evaluating extinction risks in plant populations. In P. L. Fiedler and P. M. Kareiva [eds.], Conservation biology for the coming decade, 49–65. Chapman and Hall, New York, New York, USA
Mitchell R. J. 1997 Effects of pollen quantity on progeny vigor: evidence from the desert mustard Lesquerella fendleri. Evolution 51: 1679-1684[CrossRef][ISI]
Montalvo A. M. N. C. Ellstrand 2001 Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). American Journal of Botany 88: 258-269
Moody-Weis J. M. J. S. Heywood 2001 Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). American Journal of Botany 88: 1615-1622
Morgan J. W. 1999 Effects of population size on seed production and germinability in an endangered, fragmented grassland plant. Conservation Biology 13: 266-273[CrossRef][ISI]
Oostermeijer J. G. B. R. G. M. Altenburg H. C. M. Den Nijs 1995 Effects of outcrossing distance and selfing on fitness components in the rare Gentiana pneumonanthe (Gentianaceae). Acta Botanica Neerlandica 44: 257-268
Palmer T. M. M. Zimmerman 1994 Pollen competition and sporophyte fitness in Brassica campestris—does intense pollen competition result in individuals with better pollen?. Oikos 69: 80-86[CrossRef][ISI]
Paschke M. C. Abs B. Schmid 2002 Relationship between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica. Conservation Genetics 3: 131-144[CrossRef][ISI]
Rademaker M. C. J. T. J. De Jong 1998 Effects of flower number on estimated pollen transfer in natural populations of three hermaphroditic species: an experiment with fluorescent dye. Journal of Evolutionary Biology 11: 623-641[CrossRef][ISI]
Ramsey M. G. Vaughton 2000 Pollen quality limits seed set in Burchardia umbellata (Colchicaceae). American Journal of Botany 87: 845-852
Rathcke B. J. E. S. Jules 1993 Habitat fragmentation and plant-pollinator interactions. Current Science 65: 273-277[ISI]
Reinartz J. A. D. H. Les 1994 Bottleneck-induced dissolution of self-incompatibility and breeding system consequences in Aster furcatus (Asteraceae). American Journal of Botany 81: 446-455[CrossRef][ISI]
Richards A. J. 1997 Plant breeding systems, 2nd ed. Chapmann & Hall, London, UK
Richardson T. E. A. G. Stephenson 1992 Effects of parentage and size of the pollen load on progeny performance in Campanula Americana. Evolution 46: 1731-1739[CrossRef][ISI]
Roll J. R. J. Mitchell R. J. Cabin C. R. Marshall 1997 Reproductive success increases with local density of conspecifics in a desert mustard (Lesquerella fendleri). Conservation Biology 11: 738-746[CrossRef][ISI]
Schwabe A. A. Kratochwil 1986 Schwarzwurzel-(Scorzonera humilis-) und Bachkratzdistel-(Cirsium rivulare-) reiche Vegetationstypen im Schwarzwald: ein Beitrag zur Erhaltung selten werdender Feuchtwiesen-Typen. Veröffentlichungen Naturschutz und Landschaftspflege Baden-Württemberg 61: 277-333
Sheridan P. M. D. N. Karowe 2000 Inbreeding, outbreeding, and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae), in Virginia. American Journal of Botany 87: 1628-1633
SPSS. 2001 SPSS 11.0 for Windows and Smart-ViewerTM. SPSS, Chicago, Illinois, USA
Stephenson A. G. S. V. Good D. W. Vogler 2000 Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the breeding system of Campanula rapunculoides L. (Campanulaceae). Annals of Botany 85: 211-219
Van Treuren R. R. Bijlsma N. J. Ouborg W. Van Delden 1993 The significance of genetic erosion in the process of extinction. 4. Inbreeding depression and heterosis effects caused by selfing and outcrossing in Scabiosa columbaria. Evolution 47: 1669-1680[CrossRef][ISI]
Walsh N. E. D. Charlesworth 1992 Evolutionary interpretations of differences in pollen tube growth rates. Quarterly Review in Biology 67: 19-37[CrossRef]
Waser N. M. M. V. Price 1989 Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43: 1097-1109[CrossRef][ISI]
Waser N. M. M. V. Price 1991 Outcrossing distance effects in Delphinium nelsonii. Pollen loads, pollen tubes, and seed set. Ecology 72: 171-179[CrossRef][ISI]
Winsor J. A. L. E. Davis A. G. Stephenson 1987 The relationship between pollen load and fruit maturation and its effects on offspring vigor in Cucurbita pepo. American Naturalist 129: 643-656[CrossRef][ISI]
Winsor J. A. S. Peretz A. G. Stephenson 2000 Pollen competition in a natural population of Cucurbita foetidissima (Cucurbitaceae). American Journal of Botany 87: 527-532
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