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Keywords:

  • Asclepiadaceae;
  • flower production;
  • fruit production;
  • habitat quality;
  • pollen limitation;
  • population density;
  • population size;
  • resource limitation;
  • Vincetoxicum hirundinaria

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    In patchily distributed plant species, seed production is likely to be influenced both by local abiotic factors affecting plant size and conditions for fruit maturation, and by population characteristics affecting the intensity of interactions with mutualists and antagonists. However, the relative importance of these effects is poorly known.
  • 2
    We used multiple regression and path models to examine the importance of abiotic factors (sun exposure, soil depth) and population characteristics (size, density and connectivity) for variation in flower and fruit production and intensity of seed predation among 39 populations of the long-lived herb Vincetoxicum hirundinaria in three consecutive years. In addition, we manipulated water availability in a field experiment and recorded short-term and long-term effects on fruit output, and conducted a supplemental hand-pollination experiment.
  • 3
    Flower production varied little, while fruit initiation, fruit abortion and fruit predation varied considerably among years. Sun exposure and soil depth affected fruit production per plant indirectly and positively through their effects on flower number. Population density affected fruit production negatively through its effect on flower number. Both fruit initiation and the proportion of fruits attacked by the tephritid fly Euphranta connexa were related positively to population size.
  • 4
    The number of full-size fruits per plant was related positively to sun exposure and population size in two years each, and related negatively to population density in one year. However, because of seed predation, the number of intact mature fruits was related significantly to population characteristics in only one of three years.
  • 5
    The field experiments showed that both shortage of water and insufficient pollination may limit fruit set in V. hirundinaria.
  • 6
    Synthesis. These results demonstrate that the relative importance of local abiotic conditions and population characteristics may vary considerably along the chain of events from flower formation to intact fruit, and also among years. They further show that, at least in species with a naturally patchy distribution, connectivity may be relatively unimportant for variation in reproductive output compared to effects of habitat quality, population size and density.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Processes that govern spatial variation in flower and fruit production in plants are of fundamental importance because they influence both the persistence of plant species at a local and regional scale and the resource availability for insects and other organisms feeding on flowers and fruits. Many plant species occur as relatively small, widely spaced populations in habitats of different quality spread across the landscape (Eriksson 1996; Freckleton & Watkinson 2002). This is true for species associated with naturally patchy habitat types, but also for an increasing number of species affected by human-induced habitat fragmentation (Balmford et al. 2003; Fahrig 2003). Therefore, clarifying the extent to which the dynamics of such sets of local populations are determined by processes acting within and between populations, respectively, is a major challenge (Norton et al. 1995; Quintana-Ascencio & Menges 1996; Hobbs & Yates 2003; Armstrong 2005).

Most plants are sessile and strongly affected by abiotic conditions and competitive interactions at a very local spatial scale, but interactions at the landscape level may also be important. Long-distance dispersal of seeds is the basis for the occasional establishment of new populations. Many pollinators, herbivores and seed predators have strong dispersal powers and form important links between populations. Both pollination intensity and rates of herbivory and seed predation may be related to population size, density and measures of isolation (e.g. Förare & Solbreck 1997; Kéry et al. 2001; Colling & Matthies 2004; Waites & Ågren 2004; Östergård & Ehrlén 2005; Singer & Wee 2005; Ward & Johnson 2005). However, there is a lack of studies examining the relative importance of population characteristics and habitat quality for among-population variation in plant reproductive success (Brys et al. 2004; Kolb 2005).

Flower and fruit production are shaped by interactions with both the abiotic and biotic environment. Flower production is often correlated strongly with plant size, which generally increases with resource availability and decreases with population density (e.g. Weiner & Thomas 1986; Herrera 1993). Flower formation sets an upper limit to fruit production, but in many species only a small proportion of flowers develop into mature fruits (Sutherland 1986). Fruit set depends on resources available for fruit maturation, weather conditions during fruit development and interactions with pollinators and seed predators. Environmental factors such as light and water availability may thus affect fruit production directly because of their effects on resources available for fruit maturation, but also indirectly because of their effects on flower production and on abundance of pollinators and seed predators.

Similarly, population density may affect fruit output because of effects on plant size and flower production and because of effects on fruit set mediated by interactions with pollinators and seed predators. Density-dependent competitive interactions should result in a negative relationship between population density and mean flower production per plant, whereas attractiveness to pollinators and pollination success may increase with increasing population density (Kunin 1993; Ghazoul 2005), at least until the local pollinator populations are satiated (Baker et al. 2000). If pollinator visitation increases with population density, plant fecundity may display positive density dependence, and pollen limitation may increase the risk of local extinction of small, low-density populations (Kunin 1993; Groom 1998; Hackney & McGraw 2001).

Population size and isolation may affect seed output per plant because of effects on interactions with pollinators and seed predators, and also because of associations with genetic diversity and inbreeding. Large populations of reward-producing plants should be more attractive to both pollinators and seed predators compared to small, isolated populations. As a consequence, pollen limitation may decrease, but the risk of seed predation may increase with increasing population size (Ågren 1996; Colling & Matthies 2004; Waites & Ågren 2004; Kolb 2005; Östergård & Ehrlén 2005; Ward & Johnson 2005; but see Campbell & Husband 2007). The relationship between population size and seed output should depend on the relative importance of these two processes, but this balance has been quantified in very few species (Colling & Matthies 2004). Finally, seed output may be reduced in small, isolated populations because of both increased inbreeding and reduced number of compatible mates (Ågren 1996; Vergeer et al. 2003; Campbell & Husband 2007). Thus, flower and fruit production can be influenced by a variety of environmental factors and population characteristics. An assessment of their relative importance requires data from a large number of well-characterized populations, and ideally also from several years. However, this information is available for very few species (e.g. Hobbs & Yates 2003).

Here, we used data collected in 39 populations over 3 years to examine factors influencing spatial variation in flower and fruit production in the long-lived herb white swallow-wort, Vincetoxicum hirundinaria. This species has a naturally patchy distribution and is most common in open habitats with thin soils, but also occurs in shaded conditions on deeper soils. Fruit production by V. hirundinaria varies dramatically among years, and is correlated negatively with the number of sunshine hours in summer (a proxy for intensity of drought; Solbreck & Sillén-Tullberg 1986; Solbreck & Ives 2007). The population dynamics of its main pre-dispersal seed predator, the tephritid fly Euphranta connexa, is driven almost totally by the strong among-year variation in fruit availability (Solbreck & Ives 2007). The overall aim of the present study was to examine the relative importance of habitat quality and population size, density and connectivity for among-population variation in fruit production and the number of mature fruits escaping pre-dispersal seed predation. For each population, we quantified mean soil depth and sun exposure. We expected flower and fruit production to be related positively to soil depth and that this relationship would be particularly strong in dry summers. Sun exposure may affect plant reproductive output in rainy summers positively, but may affect flower and fruit production in dry summers negatively because it increases drought stress.

We asked: (i) whether spatial variation in production of flowers, full-size fruits and non-damaged mature fruits can be explained by differences in sun exposure, soil depth and population size, density and connectivity; and (ii) whether environmental factors influence fruit production directly by affecting the probability of fruit initiation, fruit abortion and seed predation, or indirectly through effects on flower production. More specifically, we examined the predictions that (i) flower production increases and fruit abortion decreases with increasing resource availability (quantified as sun exposure and soil depth), and (ii) fruit initiation and seed predation increase with increasing population size and density, but decrease with increasing isolation. Because fruit set and the relationships between fruit set and environmental variables may vary among years (e.g. Alexandersson & Ågren 1996; Waites 2005), the study was conducted over 3 years. To determine whether fruit production is limited by water availability, we manipulated water availability in a field experiment and recorded the short-term and long-term effects on fruit output. Finally, we conducted a hand-pollination experiment to examine whether fruit production was limited by insufficient pollination.

Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

study species

Vincetoxicum hirundinaria Med. (Asclepiadaceae) is native to Europe and western Asia, and has been introduced to North America (Hultén & Fries 1986; DiTommaso et al. 2005). In Sweden, V. hirundinaria occurs along the north-western fringe of its wide palaearctic range (Hultén & Fries 1986; Donadille 1965). It is abundant on the large Baltic islands Öland and Gotland, and has a patchy distribution along the Baltic coast and inland along Lake Mälaren. The plant typically forms a short, branched rhizome, from which a dense tussock of above-ground shoots develop. Individual plants may produce from a few to more than 100 flowering shoots [median (range), 12 (1–120), n = 765 plants sampled in the study area in 1999]. In a given plant, the shoots are of roughly equal length and flower synchronously. The plant grows in a variety of conditions from sun-exposed rock ledges to shaded deciduous woods below cliffs, and along forest margins.

Flowering usually peaks in June, but may continue even into early September. The flowers are creamy white, hermaphroditic and arranged in cyme-like inflorescences, which develop from leaf nodes on the above-ground shoot. The anthers are fused to the gynoecium to form a gynostegium, and the pollen is packed in five pairs of pollinia. The results of controlled crosses suggest that V. hirundinaria has a late-acting self-incompatibility system, but that the frequency of self-fertile individuals may be relatively high (Leimu 2004). High inbreeding coefficients have been documented in V. hirundinaria populations in south-western Finland, which is consistent with a mixed-mating system (Leimu & Mutikainen 2005). The flowers are visited by a multitude of insects, the vast majority of which are nectar thieves. The large empidid fly Empis tesselata, which has an extended flight period and is likely to be one of the main pollinators in the area (C. Solbreck, pers. obs.), is a very good flier and can fly long distances (Chvála 1994). Most fruits mature in July and August, and fruit production varies strongly between years (Solbreck & Sillén-Tullberg 1986; Solbreck & Ives 2007). Each fruit contains about 20 wind-dispersed seeds.

The larva of the tephritid fly E. connexa (Fabr.) may destroy close to 100% of the seeds (Solbreck 2000; Solbreck & Ives 2007). The adult fly oviposits on developing fruits, and is a strong flier that can easily move between patches of its host plant in the study area (Solbreck 2000). The lygaeid bug, Lygaeus equestris (L.), is both a pre- and a post-dispersal seed predator and a good flier (Solbreck 1995). It is sometimes abundant, but its impact is small compared to that of E. connexa. The plant contains toxic substances (Tullberg et al. 2000) and is not fed upon by grazing mammals in the study area.

study area

This study was conducted at Tullgarn (58°57′ N, 17°36′ E) on the coast of the Baltic Sea, about 50 km south-by-south-west of Stockholm, Sweden. This area receives relatively little rain. During the 3 years of study (1999–2001), precipitation during June–August ranged from 130 to 232 mm (Table 1). The presence of V. hirundinaria has been mapped in the 3 × 4 km study area since the late 1970s. The species is distributed patchily in the landscape, forming 51 discrete populations with a mean size of 237 flowering plants (median 62 plants, range 1–3100 plants in 1999) and a mean plant coverage of 25.3 m2 (range 0.25–371 m2) (Fig. 1).

Table 1.  Weather data collected at weather stations close to the study area at Tullgarn in 1991–2001, and 30-year means from the reference period 1961–90. Data on number of sunshine hours from Stockholm (50 km north-by-north-east of Tullgarn), temperature from Hårsfjärden (25 km east-by-north-east of Tullgarn) and precipitation from Åda (4 km south-west of Tullgarn)
Variable/periodMayJuneJulyAugustJune–August
Sunshine hours
 1999290320335261916
 2000263262159234655
 2001263282314223819
 Mean 1961–90276292260221773
Mean temperature (°C)
 1999  8.2 14.51 8.1 15.6 16.1
 2000 10.4 13.2 15.6 15.4 14.7
 2001  9.6 14.0 18.1 16.2 16.1
 Mean 1961–90  8.8 13.9 15.9 15.1 14.9
Precipitation (mm)
 1999 21 47 33 50130
 2000 31 45114 73232
 2001 25 15 65 62142
image

Figure 1. Map of the study area showing Vincetoxicum hirundinaria populations (circles) classified according to population size (number of flowering individuals). Populations included in the present study are indicated with filled circles; other populations are indicated with open circles. Grey areas denote sea (to the east and south-east) and lakes, and the thick line shows the eastern limit of the investigated area.

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comparative study

To determine how flower and fruit production were related to habitat variables and population characteristics, we gathered data in 39 populations over 3 years. The study populations were chosen to represent a wide range in size, density and isolation. A population was defined operationally as a group of plants separated by a distance of at least 25 m from the closest conspecific. In most cases, among-population distances were considerably larger than this (mean 152 m, median 100 m, range 25–1223 m; Fig. 1). We quantified the size of the study populations as the total number of flowering plants. There is wide variation in size, morphology and colour of flowers, making the delimitation of plant individuals straightforward during the flowering period, even in dense populations. To quantify population connectivity, we calculated for each population the total area (in m2) of other V. hirundinaria populations within a radius of 500 m. Other radii and other isolation measures, examined in preliminary analyses, were related less strongly to plant reproductive success. To characterize sun exposure, soil depth and local population density, we took measures in direct connection with the plants whose reproductive success was quantified. In each population, up to 20 individuals were selected randomly, marked and mapped in 1999 [except in two of the largest populations, in which 94 (population T18) and 29 (T23) plants were included for study]. For each marked plant, we recorded sun exposure, soil depth and local population density. To quantify sun exposure, we determined the number of hours the plant was reached by direct sunlight at midsummer. A transparent plastic sheet was mounted vertically along the periphery of a horizontal semi-circular plate mounted on a tripod. The path of the sun at midsummer (as viewed from the circle centre of the base plate) was delineated on the sheet and the sun's position for each hour marked. The device was placed at the top of the plant and aligned with the aid of a compass and a spirit level. Looking from the circle centre, the number of hours (between 0600 h and 1800 h) the plant was hit by direct sunlight (not shaded by vegetation) could then be recorded. To quantify soil depth, a steel probe was pushed into the ground until it reached rock at 10 regularly spaced locations within a 1 m2 circular area with the focal plant in the centre, and the mean depth was calculated. To quantify local plant density, we recorded the number of V. hirundinaria individuals within the same 1 m2 area.

The study populations varied considerably in size [mean 284 flowering plants, median (range) 80 (1–3100) plants], mean density [2.6 (1–4.5) flowering plants per m2] and connectivity [153 (0–429) m2 of V. hirundinaria cover within 500 m of the focal population; n = 39; Fig. 1]. Population size and density, in terms of the number and density of flowering plants, did not vary during the 3-year period.

Each year, we quantified flower and fruit production of the marked plants. We counted the number of flowering shoots and estimated the number of flowers per shoot. At the end of the flowering season, the number of leaf nodes with an inflorescence (x1) and the number of scars left by pedicels in the inflorescence at the lowermost node (x2) were recorded for up to three flower-producing shoots per plant. The number of flowers per shoot (y) was estimated using the expression y = 5.51x1 + 1.95x2. This formula was obtained from a sample of 190 shoots collected at many different localities at Tullgarn in 1999, on which x1, x2 and y were all measured (R2 = 0.93). For each plant, we estimated the total number of flowers produced as the number of flowering shoots multiplied by the mean number of flowers per shoot. We recorded the number of fruits that had initiated development, the number of initiated fruits that aborted and the number of fruits that reached full size. We quantified fruit initiation as the number of initiated fruits divided by the total number of flowers produced, and fruit abortion as the number of aborted fruits divided by the number of initiated fruits. In addition, we counted the total number of full-size fruits in each population, and determined how many of these were attacked by E. connexa. For each population, we quantified fruit predation as the proportion of full-size fruits attacked by E. connexa.

watering experiment

To determine whether water availability limits fruit production, we conducted a watering experiment in population T18, the largest V. hirundinaria population in the area. This population is subdivided into two distinct subpopulations: T18A (which is located in an open, rocky environment on the top of a hill) and T18B (which is located in a shaded environment at the base of the hill). Plants were marked in early June 1999. In subpopulation T18A, we marked a total of 80 plants, of which 30 plants were assigned to the watering treatment. In subpopulation T18B, we marked a total of 60 plants, of which 30 plants were assigned to the watering treatment. Plants in the watering treatment were watered 12 times during the period 16 June to 18 August. Water was added to a circular area of 0.5 m2 with the plant in the centre. The total amount of water added to each plant corresponded to 324 mm of rain (cf. Table 1). At the end of the flowering period, we recorded the number of flower-producing shoots, and estimated the number of flowers produced by up to 10 flower-producing shoots per plant, and total flower production using the procedure outlined earlier. At fruit maturation, we scored the number of flowers that had initiated fruit development and the number of full-size fruits on all experimental plants.

To determine whether watering in one year would influence flower and fruit production in ensuing years, we recorded flower and fruit production of the experimental plants in 2000 and 2001. Some plants lost their tags, which reduced the final sample somewhat.

hand-pollination experiment

To examine whether fruit set was limited by insufficient pollination, we conducted a hand-pollination experiment in subpopulation T18A in 2000. For this experiment, we marked four inflorescences, each on a separate shoot, on each of 20 plants. Flowers in two of the inflorescences received supplemental hand pollination, while the flowers in the other two inflorescences served as open-pollinated controls. Pollinia were transferred with the aid of a fine straw of grass, and the pollen source was a plant at least 5 m away from the focal plant. Supplemental hand pollinations were conducted during peak flowering. At fruit maturation, we recorded the number of flowers and full-size fruits produced by experimental inflorescences. To examine whether supplemental hand pollination reduced the likelihood of fruit set in open-pollinated control inflorescences on the same plant (cf. Zimmerman & Pyke 1988), we compared their fruit production to that of open-pollinated inflorescences on 40 unmanipulated plants that grew in the same area of the population and that were included in the survey of among-population variation in flower and fruit production.

analyses

We used two-way analysis of variance (anova) to quantify how much of the total variance in number of flowers, fruit initiation and number of full-size fruits and number of intact mature fruits (i.e. those that had escaped seed predation) per plant that could be attributed to variation among populations and variation among years, respectively (REML estimates using the software JMP version 5.01, SAS Institute Cary, NC, USA). Corresponding estimates could not be obtained for fruit abortion and fruit predation because fruits were not produced in all populations in all years.

We used multiple regression models that were based on population means and that explored all possible combinations of predictor variables to assess the effects of sun exposure, soil depth and population size, density and connectivity on number of flowers, number of full-size fruits and number of intact mature fruits per plant. We used the same approach to explore causes of variation in fruit survival during different stages of fruit development, i.e. variation in fruit initiation, fruit abortion and fruit predation. Relationships were examined separately for 1999, 2000 and 2001. We ranked models using the Akaike information criterion (AIC), and selected the model with the lowest AIC (Quinn & Keough 2002). Collinearity of independent variables may complicate the interpretation of partial regression coefficients in multiple regression (Graham 2003). In the present study, variance inflation factors (VIF) were low (VIF < 1.6 for all predictor variables), suggesting that multi-collinearity was weak and should not represent a problem (cf. Quinn & Keough 2002).

To examine further the causal relationships between environmental predictors, population characteristics, mean number of flowers and fruit production, we compared different path models of measured variables, as in the first step of structural equation modelling (Shipley 2000). In addition to environmental predictors and population characteristics, these models included the mean number of flowers, initiated fruits, full-size fruits and intact mature fruits produced per plant. Because of the limited sample sizes (n = 39 populations), we chose not to fit latent variables. The module ‘Build’ in the software TETRAD III (Scheines et al. 2006) was used to determine possible paths with significance set to 0.1. The software uses prior knowledge and covariation of supplied variables to determine conditional independence of these variables. The result is a series of possible path diagrams. We assigned variables to different tiers, where variables in higher tiers could not be causes of those in lower tiers (1: sun exposure, soil depth and connectivity; 2: population size and density; 3: number of flowers; 4: number of initiated fruits; 5: number of full-size fruits; 6: number of intact mature fruits). The degree of fit between the observed and expected covariance structures of the final path models was tested statistically with the ‘sem’ function in the free software R (R Foundation for Statistical Computing, Vienna, Austria) (R Development Core Team 2005). A significant goodness-of-fit chi-square statistic indicates that the model does not fit the data.

Because of lack of variation in some variables, multiple regression models and path models differed slightly between the three study years. In 1999, almost all fruits were consumed by seed predators and very few intact fruits were produced; in 2000, very few initiated fruits aborted. It was therefore not meaningful to analyse among-population variation in fruit predation and output of intact mature fruits in 1999 or in seed abortion in 2000 with multiple regression models. Similarly, we did not include number of intact mature fruits in path models based on data collected in 1999, or the number of full-size fruits in models based on data from 2000.

Population size, number of flowers per plant, number of initiated fruits per plant (+0.5), number of full-size fruits per plant (+0.5) and number of intact mature fruits per plant (+0.5) were log-transformed, sun exposure was square-root transformed, and fruit initiation, fruit abortion and fruit predation were arcsine square-root transformed before statistical analyses.

Two-way anova was used to examine the effects of subpopulation and watering treatment on flower production, fruit initiation, fruit abortion, fruit set and number of full-size fruit in the watering experiment.

We used paired t-tests to compare fruit initiation, fruit set and number of full-size fruits in open-pollinated control inflorescences and in inflorescences receiving supplemental hand-pollination on experimental plants. We used one-way anova followed by Tukey tests to determine whether fruit production varied among hand-pollinated inflorescences, open-pollinated control inflorescences on the same plants and open-pollinated inflorescences on plants that did not receive supplemental hand pollination (second control). Analyses were conducted on plant means.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

spatio-temporal variation in flower and fruit production

Flower production varied considerably among populations, but relatively little among years; fruit initiation, abortion and predation varied considerably among years and in most years also among populations (Fig. 2; Table 2). Flower production was about 40% higher in 2001 compared to the two preceding years (Fig. 2). Differences in the number of flowering shoots per plant (mean calculated based on population means: 1999, 18.1; 2000, 18.9; 2001, 22.1) and the number of flowers per flower-producing shoot (1999, 56.6; 2000, 52.6; 2001, 64.7) contributed roughly equally to among-year variation in flower production. Fruit initiation was markedly higher in the rainy summer of 2000 (0.89%) than in the dry summers of 1999 (0.27%) and 2001 (0.20%) (Table 1). Fruit abortion was very high in 1999, low in 2001 and negligible in 2000 (Fig. 2). The three study years represented the full range of variation in number of full-size fruits observed at Tullgarn during a 25-year period (1977–2001), with very high fruit production in 2000 (rank 2 in the 25-year period) and very low to intermediate fruit production in 1999 (rank 19) and 2001 (rank 12; C. Solbreck, unpubl. data). Seed predators consumed almost all non-aborted fruits in 1999, whereas predation levels varied more among populations in 2000 and 2001 (Fig. 2). Fruit output, i.e. the number of intact mature fruits produced per plant, varied strongly among years but also among populations in 2000 (Table 2; Fig. 2).

image

Figure 2. Mean number of flowers per plant, fruit initiation (proportion of flowers initiating fruit development), fruit abortion (proportion of initiated fruits that aborted), number of full-size fruits per plant, fruit predation (proportion of full-size fruits attacked by Euphranta connexa) and number of intact mature fruits per plant in 39 Vincetoxicum hirundinaria populations in 1999, 2000 and 2001. Means were calculated based on population means. Vertical lines indicate SE.

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Table 2.  Distribution of variance in number of flowers per plant, proportion of flowers initiating fruit development, number of full-size fruits per plant and number of intact mature fruits per plant. The analysis was conducted on population means for 1999, 2000 and 2001. Variance components could not be obtained for fruit abortion and fruit predation because of missing values in some populations in some years
 Proportion of total variance
Among populationsAmong yearsResidual
Number of flowers (log)0.8720.0700.057
Fruit initiation (arcsine square-root)0.1450.5000.355
Number of mature fruits (log n+ 0.5)0.2300.4900.280
Number of intact fruits (log n+ 0.5)0.0740.6700.256

effects of environmental variables and population charactersitics

The examined predictor variables explained a large proportion of the variance in flower production (69–72%), and a modest proportion of the variance in number of full-size fruits per plant (16–33%) and number of intact mature fruits per plant (10–24%) in the two years when most populations produced intact fruits (Table 3). They explained a modest proportion of the variance in fruit initiation (6–25%) and fruit abortion (3–23%), and a fair proportion of the variance in fruit predation the two years it varied among populations (41–42%; Table 3).

Table 3.  General linear models of the effect of five environmental predictor variables (sun exposure, soil depth, and population size, density and connectivity) on number of flowers, full-size fruits and intact fruits per plant, fruit initiation (proportion of flowers initiating fruit development), fruit abortion (proportion of initiated fruits that aborted) and fruit predation (proportion of full-size fruits consumed by Euphranta connexa) in 39 populations of Vincetoxicum hirundinaria in 1999, 2000 and 2001. Number of flowers and fruits per plant were log-transformed, and fruit initiation, abortion and predation were arcsine square-root transformed prior to analysis. Only the subsets of predictors included in the model with the lowest Akaike value are shown. Predictors significant at P < 0.05 are in bold
Dependent variableIndependent variabled.f.R2-adjustedAICP
Sun exposureSoil depthPopulation sizePopulation densityConnectivity
  1. AIC, Akaike information criterion.

Number of flowers
 1999 0.267 0.0360.070–0.101 0.000550.69–144.4<0.001
 2000 0.267 0.0450.112–0.166 0.000450.72–137.7<0.001
 2001 0.270 0.0490.162–0.159 0.000550.69–129.7<0.001
Number of full-size fruits
 1999 0.157 0.121–0.079 30.16–100.2 0.03
 2000 0.199 0.358–0.264 30.33 –70.0<0.001
 2001  0.214  10.22 –94.0 0.002
Number of intact fruits per plant
 2000  0.275–0.289 20.24 –71.2 0.002
 2001 0.123 0.082  20.10–100.6 0.06
Fruit initiation
 1999  0.0077  10.06–306.9 0.07
 2000  0.0233–0.0167 20.16–261.9 0.02
 2001  0.0111  10.25–331.6<0.001
Fruit abortion
 1999    –0.000610.03 –95.1 0.14
 2001 0.086–0.032  0.045 30.23–156.3 0.01
Fruit predation
 2000 0.277 0.230  20.42 –92.0<0.001
 2001–0.359 0.214 –0.000730.41 –93.9<0.001

Flower production was related to each of the five predictor variables examined in at least one year, whereas the number of full-size fruits per plant and the number of intact mature fruits per plant were related to only a subset of these variables. Flower production was related positively to sun exposure and soil depth, and negatively to density in all three years (Table 3). In 2000 and 2001, flower production was also related positively to population size, and in 1999 to connectivity. The number of full-size fruits per plant was related positively to sun exposure and population size in two years each, and negatively to population density in one year. The number of intact fruits was related positively to population size and negatively to population density, but these relationships were statistically significant in only one of three years (Table 3).

Fruit initiation, fruit abortion and fruit predation were affected by partly different abiotic factors and population characteristics. Fruit initiation was related positively to population size in all years (but only marginally so in 1999), and correlated negatively with density in 2000 (Table 3; Fig. 3). Fruit abortion was related positively to sun exposure and negatively to soil depth in the dry summer of 2001, but was not related to any of the environmental variables considered in the similarly dry summer of 1999 (Table 3). In the rainy summer of 2000, fruit abortion was negligible (Fig. 2). Fruit predation by the tephritid fly E. connexa was related positively to population size in 2000 and 2001. It was correlated positively with sun exposure in the rainy summer of 2000, but related negatively to sun exposure in the dry summer of 2001. In 1999, almost all fruits were attacked by E. connexa (Fig. 2). Seed predation partly negated the positive correlations between population size, flower number and fruit initiation, which could explain why the number of intact fruits per plant was related significantly to population size in only one year (Fig. 3; Table 3).

image

Figure 3. Relation between population size [log10(number of flowering plants)] and arcsine square-root proportion of flowers initiating fruit development, arcsine square-root proportion of full-sized fruits attacked by Euphranta connexa and number of intact mature fruits per plant in Vincetoxicum hirundinaria (n = 39 populations) in 1999, 2000 and 2001.

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The best path models of the causal relationships were very similar between the three study years. However, observed and predicted covariances differed significantly for data collected in 2000 and 2001, indicating that models did not explain adequately the covariance structure in these years (2000, χ2 = 36.5, d.f. = 19, P = 0.009; 2001, χ2 = 50.5, d.f. = 26, P = 0.003). For 1999, the best model included effects of sun exposure, soil depth and population density on number of flowers per plant (χ2 = 19.2, d.f. = 19, P = 0.44; Fig. 4). The number of flowers and population size influenced the number of initiated fruits. The number of full-size fruits was affected only by the number of initiated fruits. The number of intact, mature fruits was not included in the model for 1999, because in this year almost all fruits were damaged by E. connexa.

image

Figure 4. Path diagram depicting direct and indirect effects of soil depth, sun exposure, population size, density and connectivity on mean numbers of flowers, initiated fruits and mature fruits per plant in 39 Vincetoxicum hirundinaria populations in 1999. All effects were significant at P < 0.1. One-headed arrows represent causal relationships, and double-headed arrows represent free correlations. Numbers are path model estimates.

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supplemental watering

For control plants, both flower production and number of full-size fruits per plant were larger in the sun-exposed subpopulation T18A than in the shaded subpopulation T18B (Fig. 5; Table 4). Fruit initiation and fruit set (proportion of flowers forming a full-size fruit) were higher in the sun-exposed subpopulation than in the shaded population in the relatively rainy 2000, while the reverse was true in the dry summer of 2001.

image

Figure 5. Square-root number of flowers per plant, arcsine square-root fruit set (proportion of flowers developing into full-size fruits) and square-root number of full-size fruits per plant among plants that were watered in 1999, and among controls in an open and in a shaded subpopulation of Vincetoxicum hirundinaria population T18 in 1999, 2000 and 2001.

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Table 4.  Effects of subpopulation (open vs. shaded subpopulation) and water addition on flower production, fruit initiation (proportion of flowers initiating fruit development), fruit abortion (proportion of initiated fruits that aborted), fruit set (proportion of flowers developing into full-size fruits) and number of full-size fruits in Vincetoxicum hirundinaria population T18. Plants in the water-addition treatment were watered in 1999. Prior to analysis, the number of flowers and fruits produced per plant were square-root transformed; fruit initiation, fruit abortion and fruit set were arcsine square-root transformed
 199920002001
d.f.MSFd.f.MSFd.f.MSF
  • *

    P < 0.05,

  • P < 0.01,

  • P < 0.001.

Number of flowers
 Subpopulation  116691.091.0  119406.6102.3  122521.577.3
 Water addition  1  531.6 2.9  1  599.2  3.2  1   14.9 0.1
 Subpopulation × water  1   10.6 0.1  1  104.0  0.5  1  112.0 0.4
 Error124  183.4 125  189.7 125  291.3 
Fruit initiation
 Subpopulation  11.272 × 10−3 1.0  162.56 × 10−3 17.1  115.443 × 10−37.9
 Water addition  11.632 × 10−3 1.3  121.75 × 10−3  5.9*  1 2.127 × 10−31.1
 Subpopulation × water  10.143 × 10−3 0.1  1 1.23 × 10−3  0.3  1 0.214 × 10−30.1
1241.280 × 10−3 125 3.66 × 10−3 125 1.952 × 10−3 
Fruit abortion
 Subpopulation  10.007 0.03  1 0.1212  3.0 1 2.575 × 10−30.2
 Water addition  11.225 4.3*  1 0.0353  0.9 1 6.971 × 10−30.5
 Subpopulation × water  10.480 1.7  1 0.0129  0.3 1 0.399 × 10−30.03
 820.285 108 0.0402 9014.669 × 10−3 
Fruit set
 Subpopulation  11.298 × 10−3 2.0  154.46 × 10−3 15.5  115.601 × 10−38.2
 Water addition  16.446 × 10−3 9.7  120.27 × 10−3  5.8*  1 1.803 × 10−30.9
 Subpopulation × water  10.328 × 10−3 0.5  1 1.42 × 10−3  0.4  1 0.334 × 10−30.2
1240.664 × 10−3 125 3.52 × 10−3 125 1.900 × 10−3 
Full-size fruits
 Subpopulation  111.97122.2  1403.42127.2  14.2612.4
 Water addition  1 7.78614.4  1 39.89 12.6  12.8991.7
 Subpopulation × water  1 1.601 3.0  1 11.22  3.5  10.0810.04
125 0.539 125  3.17 1251.747 

Supplemental watering increased fruit production significantly both in the year of treatment and in the following year. Watering did not increase flower production significantly. However, it reduced fruit abortion in the year of treatment and it increased fruit initiation in the following year (Table 4). As a result, the proportion of flowers developing into full-size fruits increased significantly, and the number of full-size fruits per plant was about twice as high among plants receiving supplemental watering compared to control plants both in the year of treatment and in the following year (Fig. 5; Table 4). No effect of water addition on fruit production could be detected 2 years after the treatment was administered (Table 4).

supplemental hand pollination

The hand-pollination experiment indicated that fruit production was limited by insufficient pollination in the sun-exposed subpopulation T18A in 2000. On experimental plants, supplemental hand pollination increased the number of full-size fruits per inflorescence from 0.05 to 0.38 (paired t-test, t = 2.4, d.f. = 19, P = 0.03), corresponding to an increase in fruit initiation and fruit set from 0.65% to 7.0% (paired t-test on arcsine square-root transformed proportions, t = 2.7, d.f. = 19, P = 0.01). No fruits aborted in this experiment. Number of full-size fruits and fruit set of open-pollinated inflorescences on unmanipulated plants (second control, C2; 0.11 full-size fruits per inflorescence and 1.4% of flowers forming a full-size fruit) did not differ from those of control inflorescences on experimental plants (C1), but was lower than those of inflorescences receiving supplemental hand pollination (HP) (one-way anova, number of fruits per inflorescence, F2,77 = 7.2, P = 0.01; Tukey, HP > C1 = C2; fruit set, F2,77 = 9.7, P = 0.0002, HP > C1 = C2).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This 3-year study has shown that the relative importance of local abiotic conditions and population characteristics varies considerably along the chain of events from flower formation to intact fruit and also among years in the perennial herb V. hirundinaria. Field experiments demonstrated that both water availability and insufficient pollination may limit fruit production. Comparison of different path models suggested that population size has a positive direct effect on fruit initiation, whereas sun exposure, soil depth and population density affect fruit production primarily through their effects on flower number. Fruit predation also increased with population size and this partly negated the positive correlations between population size, flower production and fruit initiation. No significant effect of population isolation on measures of reproductive success was detected in this naturally patchy system.

flower production

Flower production varied much between populations, but was fairly constant from year to year. Sun exposure, soil depth and population characteristics explained a substantial proportion of the among-population variance in number of flowers per plant. A couple of observations suggest that this variation is determined primarily by resource availability. Firstly, the results of the multiple regression and path models were consistent among years and revealed that flower production increases with increasing soil depth and sun exposure. Secondly, flower number was related negatively to population density, indicating that plants compete locally for resources such as water or nutrients. The positive correlation between population size and flower number per plant in regression models for two of the three years indicates that environmental conditions at sites that harbour large populations are favourable also for the growth and flower production of individual plants.

fruit initiation

Fruit initiation was generally very low. The production of large numbers of surplus flowers that do not develop into fruits is a characteristic of many members of the Asclepiadaceae, and has been attributed to selection acting through both male and female function (Wyatt & Broyles 1994). The production of surplus flowers may represent a bet-hedging strategy, allowing the exploitation of occasional years that are favourable for fruit production (Lloyd 1980; Willson & Burley 1983; Ågren 1988), or providing a buffer against flower predation (Ehrlén 1993; Guitian 1993). However, even in the best year (2000), less than 1% of flowers on average initiated a fruit (population means, median 0.8%, range 0–4.0%; Fig. 2) and flower predation was negligible. Other possible benefits of surplus flower production include increased pollen receipt, increased opportunities for selective abortion and increased male reproductive success (e.g. Willson & Rathcke 1974; Burd 1998; Burd & Callahan 2000). These benefits are best evaluated based on within-population variation in floral display and reproductive success, and are pursued in a separate study (J. Ågren et al., unpubl. data).

Fruit initiation was related positively to population size (Table 3). Fruit initiation similarly tended to be higher in large than in small populations in a study of 10 Finnish V. hirundinaria populations (Leimu & Syrjänen 2002). Population size may affect attractiveness to pollinators (Ågren 1996; Waites & Ågren 2004; Kolb 2005; Ward & Johnson 2005), and the positive correlation between fruit initiation and population size may thus reflect among-population variation in pollination intensity. To test this hypothesis, hand-pollination experiments should be conducted in populations representing a wide size range (Ågren 1996). In the present study, supplemental hand pollination in a large sun-exposed population indicated that fruit initiation can be limited by insufficient pollen deposition. There was no evidence that the marked increase in fruit production observed following hand pollination was caused by reallocation of resources from open-pollinated control inflorescences on the same plant. However, the results should be interpreted with caution because only a low proportion of inflorescences on experimental plants received supplemental hand pollination and the power to detect effects of reallocation was therefore limited (cf. Zimmerman & Pyke 1988). Alternatively, fruit initiation may be related positively to population size because of a correlation between population size and some unmeasured habitat variable influencing resources available for fruit maturation (e.g. Oostermeijer et al. 1998). In the watering experiment, fruit initiation was higher among watered plants than among unwatered control plants in the year following the experimental treatment, suggesting that fruit initiation may be affected by resource availability. Finally, the reduced fruit initiation observed in small populations could be the result of increased inbreeding (Ellstrand & Elam 1993; Ouborg & van Treuren 1995; Vergeer et al. 2003). Controlled crosses indicated that self-compatible individuals of V. hirundinaria may be frequent in populations in south-western Finland, but that fruit initiation was overall lower after selfing than after cross-pollination (Leimu 2004). Still, fruit set was not correlated with gene diversity (expected heterozygosity) or inbreeding coefficients in 12 V. hirundinaria populations in the same area (Leimu & Mutikainen 2005). Additional experiments are needed to determine whether the effect of population size on fruit initiation is mediated by biotic interactions, whether it reflects variation in some unmeasured habitat variable correlated with population size, inbreeding in small populations or a combination thereof.

No strong effects of population density or isolation on fruit initiation were detected. Multiple regression models indicated that fruit initiation decreased with increasing density in one of the three years (Table 3), but this effect was not sufficiently strong to appear as a direct effect of population density on number of initiated fruits in the path models. No effect of population connectivity on fruit initiation was detected in multiple regression or path models, suggesting that isolation at the level observed in the study area does not affect pollination intensity strongly in V. hirundinaria.

fruit abortion

The number of full-size fruits per plant varied tenfold between years as a result of differences in fruit initiation and fruit abortion (Fig. 2). Both experimental and comparative data indicate that water availability influences spatio-temporal variation in fruit abortion. Water addition reduced fruit abortion significantly (Fig. 5). Moreover, fruit abortion was negligible in the rainy summer of 2000, and was related negatively to soil depth and positively to sun exposure in the dry summer of 2001, as would be expected if drought triggers fruit abortion. In accordance, the production of full-size fruits in V. hirundinaria in the study area was related negatively to the number of sunshine hours in June and July across the 7-year period 1977–83 (Solbreck & Sillén-Tullberg 1986). Interestingly, in the present study, experimental watering increased fruit output both in the year of treatment and in the following year. This suggests that resources used for fruit development are drawn not only from current production but also from stored reserves.

fruit predation

Fruit predation by the tephritid fly E. connexa has temporally variable and often very strong effects on the number of intact mature fruits in V. hirundinaria (Fig. 2; see also Solbreck & Sillén-Tullberg 1986; Solbreck & Ives 2007). In the present study, among-population variation in fruit predation was correlated with population size and sun exposure, but effects varied between years. Fruit predation was related positively to population size in two of the three years; in the third year, almost all fruits were consumed. The positive correlation between population size and fruit predation partly negated the positive correlations between population size, flower number and fruit initiation; multiple regression models indicated that the number of intact mature fruits produced per plant was related significantly to population size in only one of the three years. Seed predation is also related to host plant population size in other species (e.g. Östergård & Ehrlén 2005), and has similarly been found to cancel the positive effects of population size on fruit initiation in the perennial herb Scorzonera humilis (Colling & Matthies 2004). This emphasizes the need to consider interactions with both mutualists and antagonists when exploring the relationship between population characteristics and plant reproductive success. Fruit predation by E. connexa was related positively to sun exposure in 2000, but negatively to sun exposure in 2001. The different signs of these correlations were related to differences in phenological fit between the tephritid fly and the host plant in sun-exposed and shaded habitats in the two years (C. Solbreck, unpubl. data). Fruit predation was not related to connectivity, suggesting that variation in isolation was not sufficient to affect the risk of attack by E. connexa in the study area. This is consistent with the observation that following local extinctions of E. connexa, populations of V. hirundinaria are recolonized rapidly (Solbreck & Sillén-Tullberg 1986). Additional demographic studies of V. hirundinaria are needed to assess the consequences of the low production of intact mature fruit for local population dynamics and colonization of new sites.

An understanding of the processes governing variation in plant reproductive success is essential for an understanding of spatiotemporal variation in population dynamics and the proper management of threatened populations. The results of the present study suggest that both local abiotic conditions and population size and density are important for among-population variation in plant reproductive success in this naturally patchy system. Local abiotic conditions and population density were important for variation in flower production, while population size affected the production of intact mature fruits because of effects on fruit initiation and fruit predation. In contrast, isolation played a minor role for among-population variation in plant fecundity. Comparable data are rare for other plant species (Hobbs & Yates 2003; Ghazoul 2005). Additional studies of among-population variation in plant fecundity and its causes are therefore needed to determine the extent to which the relative importance of abiotic factors, population isolation, density and size are affected by foraging ranges and behaviour of pollinators and seed predators (Tscharntke & Brandl 2004; Westphal et al. 2006; Garcia & Chacoff 2007), plant breeding system and population history (Young et al. 1996; Aguilar et al. 2006), and the extent to which threshold effects can be detected with increasing fragmentation in human-altered environments (e.g. Lennartsson 2002; Ghazoul 2005). The present results suggest that, at least for species occurring in habitats with a naturally patchy distribution, isolation may be relatively unimportant for reproductive output compared to the effects of habitat quality, population size and density.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank S. Sandring and K. Skagerlind for assistance in the field, and P. Klinkhamer, R. Wesselingh and an anonymous referee for helpful comments on the manuscript. This study was supported financially by grants from the Swedish Research Council to J.Å., J.E. and C.S..

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  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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