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(American Journal of Botany. 2003;90:749-754.)
© 2003 Botanical Society of America, Inc.

Ecology

Phenotypic trade-offs in the sexual reproduction of Salicaceae from flood plains1

Sophie Karrenberg2 and Marianne Suter

Geobotanical Institute ETH, Zurichbergstrasse 38, 8044 Zurich, Switzerland

Received for publication August 15, 2002. Accepted for publication November 26, 2002.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
We studied the relationship of seed mass to seed longevity (controlled conditions) and to seed number in six species of Salicaceae (Populus nigra, Salix alba, S. daphnoides, S. elaeagnos, S. purpurea, and S. triandra) that frequently co-occur on European flood plains. These species regenerate sexually in the same habitat but differ in seed mass. Half-viability periods, i.e., the time after which 50% of the initially viable seeds no longer germinate, were short (between 6.5 ± 0.1 and 23.3 ± 0.3 d), and large numbers of seeds were produced (between 10 000 and 1 x 106 per plant). Mean seed mass ranged from 0.02 ± 0.001 mg in S. triandra to 0.80 ± 0.05 mg in P. nigra. Whereas seed mass was, against expectation, positively related to half-viability periods, seed number generally decreased with increasing seed mass. Thus, a phenotypic trade-off between seed mass and seed number appears to be accentuated by an increase in seed longevity with increasing seed mass.

Key Words: half-viability period • Populus • Salicaceae • Salix • seed longevity • seed mass • size–number trade-off


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Among the numerous life history traits that shape population structure, seed mass is one of the most prominent and mean seed mass is often a comparatively invariable species-specific trait (Harper et al., 1970 , and references therein). Generally, across species and families, seed mass is negatively correlated with seed longevity (or persistence in the soil) and shade tolerance (Rees, 1996 ; Hodkinson et al., 1998 ). On the other hand, small seeds are often dispersed better than larger ones, whereas larger seeds produce seedlings with superior competitive abilities (Westoby et al., 1996 ; Hewitt, 1998 ; Turnbull et al., 1999 ). Species with larger seeds, however, usually produce a smaller number of seeds (e.g., Smith and Fretwell, 1974 ; Jakobsson and Eriksson, 2000 ). Such a size–number trade-off is thought to impact the assembly of plant communities (Rees, 1995 ; Leishman, 2001 ).

Salicaceae from flood plains offer a good opportunity to study reproductive trade-offs within one family, because they frequently occur in mixed populations and have similar life histories. Apart from vegetative reproduction, these species produce large numbers of wind-dispersed, nondormant, and short-lived seeds, and seed mass varies by at least two orders of magnitude within the family (Karrenberg et al., 2002a ). Because of their limited longevity, Salix seeds were thought to be recalcitrant, i.e., not tolerant to desiccation; however, recent evidence shows that they exhibit orthodox storage behavior and their longevity is greatly enhanced under dry and cold storage conditions (Maroder et al., 2000 ). In the natural habitat, differences in seed longevity between species of Salicaceae are of particular importance, because sexual regeneration takes place only during a short period of time when seed release coincides with the availability of bare moist substrates (Niiyama, 1990 ; van Splunder et al., 1995 ; Mahoney and Rood, 1998 ). Pilot studies investigating methods for seed propagation in Salix species suggested that larger seeds might be longer-lived than small seeds (S. Karrenberg, unpublished data). Therefore, we hypothesize that, in this group, enhanced longevity may be one of the benefits conveyed by an increase in seed size. The production of larger seeds may, on the other hand, be associated with a lower seed number; i.e., a size–number trade-off may be present. Specifically, we investigated the following hypotheses in six species of Salicaceae: (1) seed size is positively correlated with seed longevity, and (2) there is a seed size–number trade-off.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study species
Six species of the Salicaceae were studied: the tree Salix alba L. and the shrub S. triandra L. of the subgenus Salix, the shrubs S. elaeagnos Scopoli, S. daphnoides Villars, and S. purpurea L. of the subgenus Vetrix (Skvortsov, 1999 ), and the tree Populus nigra L.

Seed collection and storage
Seeds were collected in spring 2000 in large mixed populations of the study species in the gravel-bed of the river Tagliamento near Pinzano, northeast Italy (46°12' N, 12°58' E). The Tagliamento is an unconstrained river with exceptionally low human impact (Ward et al., 1999 ). The study area (2 km long, 800 m wide) was characterized by multiple channels and gravel bars with pioneer stands composed of the five species of Salix, Populus nigra, and Alnus incana (Kollmann et al., 1999 ). To ensure sufficient spread of the collection plants, the study area was divided into five sections in which six female plants of each of the study species were marked and monitored for seed release every 1–3 d and seeds were collected until a sufficient number of individuals was sampled. As a result of changing weather conditions, seeds were collected from 15–22 of 30 marked individuals per species. Catkins were stored in paper bags and left protected from rain under outdoor conditions until all capsules were fully open. Bags were then transferred to insulated boxes that were open to air circulation. The aim of these storage conditions was to produce conditions close to the natural environment and at the same time to prevent a seasonal increase in storage temperature in order to compare results across species. At hourly intervals, temperature and humidity were monitored within these boxes and ambient temperature was measured in the shade (temperature/humidity logger HOBO Pro, Onset Computer, Pocasset, Massachusetts, USA; Fig. 1B). Mean storage conditions were 20.5° ± 0.03°C and 63.2 ± 0.16% humidity.



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  		Fig. 1. (A) Seeding periods and dates of seed collections and germination trials for six species of Salicaceae; (B) air temperature near the study area (flood plain of the river Tagliamento, northeast Italy), and temperature within the seed storage box

 
Germination experiments
At intervals of 1–3 d depending on species, 60 seeds of each individual were tested for germination (Fig. 1A). Hairs were cleaned from seeds with a set of sieves and placed in 9-cm petri dishes on filter paper wetted with tap water (cf. Baskin and Baskin, 1998 ). To distinguish differences between petri dishes from differences between individuals, seeds for each germination test were spread over six dishes. The dishes were radially partitioned in 10 sectors, and 10 seeds of each individual (collected on the same day) were placed in one sector in each of six petri dishes. Three dishes were placed in each of two germination chambers maintained at near 20°C with constant light (50–100 µmol · m–2 · s–1). The germination chambers were constructed from household refrigerators, each with a heating element and a temperature control circuit. A fan was installed to ensure homogeneous temperature within the chamber (Hendry and Grime, 1993 ). Mean temperatures were 19.3 ± 0.5°C in chamber 1 and 18.7 ± 0.6°C in chamber 2 as recorded at hourly intervals with temperature loggers (Minilog, Vemco, Shad Bay, Nova Scotia, Canada). Germination was scored after 4 d. Seeds that had not germinated were poked with a needle; if they appeared soft, they were regarded as dead (Baskin and Baskin, 1998 ).

Seed number
Ten catkins per study plant were harvested for counts of mature and undeveloped fruits. Catkin number per plant was counted directly in most individuals and estimated if exceeding 1000. On a random selection of 12 individuals per species, ovules were counted in one fruit. Seed numbers per catkin and per plant were estimated for each plant using the ovule number per fruit and the average number of mature fruits per catkin (Table 3). These numbers represent maximum seed numbers because usually not all ovules develop into seeds.


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  		Table 3. Seed production at different morphological levels for six species of Salicaceae (means ± 1 SE) from mixed populations on the flood plain of the river Tagliamento, northeast Italy. Because distributions of values for percentage of fruits matured, fruits per catkin, and catkins per plant were strongly skewed to the left, means and standard errors were calculated from log-transformed values and back-transformed

 
Seed mass
For each study plant, 100 seeds (300 seeds for S. triandra) without seed hairs were dried at 70°C until constancy. Bulk mass was determined to the nearest 0.001 mg.

Statistical analysis
Seed germination in relation to storage time was modelled as a binary response variate with binomial error distribution and logit link function (Collett, 1991 ). With these models, the percentage of initially viable seeds and the half-viability period (i.e., the time after which 50% of the initially viable seeds no longer germinated) were estimated for each individual. Because a slight overdispersion of the data (1.2–3.6) was detected for most individuals, heterogeneity factors were retrospectively applied to standard errors of predicted values (Collett, 1991 ). For each species, viability curves were calculated in an identical fashion to estimate initial viability and half-viability periods directly, rather than calculating these measures from the estimates per plant. Model fit was assessed by analysis of deviance. Diagnostic graphs of deviance residuals against storage time and normal plots of deviance residuals indicated a good fit of the models and a normal distribution of deviance residuals (Venables and Ripley, 1999 ).

Using a data set containing one record per plant and linear models, we investigated the effect of seed mass, genus identity, and species identity on half-viability periods and seed numbers. Half-viability periods and seed mass were log transformed prior to analysis. Model fit was assessed by analysis of variance (Venables and Ripley, 1999 ). The residuals of these models exhibited no major deviations from the normal distribution. To assess whether differences in prediction accuracy of the half-viability periods affected these results, standard errors of the predicted half-viability periods were plotted against the residuals of the linear models. There was no obvious relationship, and we concluded that the linear models used were a good reflection of trends in the data.

We compared seed mass, seed number, and germination traits between the species using multiple t tests with Bonferroni correction. To account for similarity by common descent (cf. Silvertown and Dodd, 1996 ), Populus nigra was first contrasted to the Salix species (genus identity) and, as a second step, multiple comparisons between the Salix species were made. Because phylogenic relationships within the genus Salix are at present unresolved (cf. Azuma et al., 2000 ) and all Salix species studied fall into separate sections as defined by Skvortsov (1999) , no further subgroups were used in the formal comparisons. Significance levels were {alpha} = 0.05 and all analyses were conducted using the program R.1.3.1 (Ihaka and Gentleman, 1996 ).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Viability and longevity of seeds
Germination of seeds of all species, when freshly collected, exceeded 90% (Table 1). Seeds of P. nigra had a significantly lower initial viability than the Salix species, but they lived longer (Fig. 2). Predicted half-viability periods (Table 1) ranged from 6.5 ± 0.07 d in S. purpurea to 23.3 ± 0.24 d in P. nigra. Populus nigra had a significantly longer half-viability period than the Salix species. Within these, S. alba and S. purpurea had significantly shorter half-viability periods than the other species, whereas S. daphnoides and S. elaeagnos had significantly longer half-viability periods of approximately 2 wk. The half-viability period of S. triandra was intermediate between these groups.


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  		Table 1. Seed mass, percentage of initially viable seeds, and half-viability period in dry storage (ca. 20°C, 60% humidity—i.e., the time after which 50% of the initially viable seeds no longer germinate) for six species of Salicaceae (means ± 1 SE) from mixed populations on the flood plain of the river Tagliamento, northeast Italy. Significant differences between means of Populus nigra and the Salix species are indicated with an asterisk. Within Salix, different letters indicate significant differences

 


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  		Fig. 2. Percentage of seed germination during dry storage (20°C, 63% humidity). Each point represents 14–22 trials with 60 seeds each; curves from logistic regression models are included

 
Germination percentage decreased in a clearly sigmoidal fashion (Fig. 2). The fit of a logistic regression model, with one curve for each species, was generally good, explaining 67.9% of the deviance (model 2, Table 2). This model was clearly superior to a model with identical slopes and different intercepts for each species (model 1). When separate curves were fitted for each individual, 84.1% of the deviance was explained (model 4); this was the best model. For S. elaeagnos, high values tended to be underfitted and low values were overfitted when data for this species were pooled (Fig. 2). This misfit in S. elaeagnos still persisted in the curves of individual study plants but to a lower degree. The use of the probit link function instead of the logit link function (Collett, 1991 ) did not alleviate this problem (analysis not shown); therefore, the models with the logit link function as explained earlier were used.


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  		Table 2. Analysis of deviance of logistic models on decrease in seed viability in dry storage in six species of Salicaceae (Populus nigra, Salix alba, S. daphnoides, S. elaeagnos, S. purpurea, S. triandra) from mixed populations on the flood plain of the river Tagliamento, northeast Italy. A total of 858 germination trials with 60 seeds using 15–22 individuals per species was analyzed. Parentheses refer to nested effects

 
Seed number
Ovule number per fruit was nearly constant within species; it ranged from two in S. elaeagnos to 22 in S. triandra (Table 3). Fruit number per catkin was rather similar in all species (50–70 fruits per catkin), except in S. daphnoides, which produced approximately three times more fruit per catkin (Table 3). Most species matured nearly all fruits (>95%, Table 3), but S. purpurea had a much lower fruit set because of a high incidence of insect herbivory and fungal attack (Alternaria spp.; A. Leuchtmann, Geobotanical Institute, ETH-Zürich, personal communication). Average catkin number was lowest in S. daphnoides and highest in S. triandra (Table 3). The estimated maximum seed number per catkin was highest in S. triandra and lowest in S. elaeagnos (Fig. 3B). Salix triandra also had the highest maximum seed number per plant, on average exceeding 1 x 106, whereas maximum seed number was below 10 000 in S. elaeagnos and S. purpurea (Fig. 3C).



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  		Fig. 3. Relationship between seed mass and seed number in six species of Salicaceae (A–C) at three morphological levels: (A) fruit, (B) catkin (inflorescence), and (C) whole plant. For symbol identification, see Fig. 2 . Small symbols represent individual plants; large symbols represent means per species

 
Seed mass and relationships to seed longevity and number
Seed mass differed by one order of magnitude among the Salix species investigated: S. triandra had the lowest seed mass and seeds of S. elaeagnos were the heaviest. Seeds of Populus were approximately four times heavier than S. elaeagnos seeds (Table 1). Seed mass was highly species-specific: P. nigra was significantly different from the Salix species and within these, the seed mass of each species was significantly different from all others.

Generally, the half-viability period increased exponentially with seed mass, yielding a linear relationship when seed mass is log transformed (Fig. 4). Salix triandra, however, had a longer half-viability period, despite its very small seed mass. In a linear model of half-viability periods, genus identity and species identity explained 75% of the variation in half-viability periods, whereas seed mass within genus explained only 46% of the variation in half-viability period (Table 4). When both factors were incorporated into one model, the percentage of explained variation of half-viability periods increased only slightly, but significantly, to 78%. On average, among Salix species, half-viability periods increased 9.6 ± 4.6 d per increase of each order of magnitude in seed mass. Within species, no relationship between seed mass and half-viability periods was found, as the addition of the factor seed mass nested within species was not significant (Table 4, model 5).



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  		Fig. 4. Relationship between seed mass and half-viability period (i.e., the time after which 50% of the seed are no longer able to germinate) in six species of Salicaceae. For symbol identification, see Fig. 2 . Small symbols represent individual plants; large symbols represent means per species

 

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  		Table 4. Summary of analyses of variance of linear models on the effect of genus identity, species identity, and seed mass on half-viability periods and maximum seed numbers in six species of Salicaceae (Populus nigra, N = 16; Salix alba, N = 17; S. elaeagnos, N = 22; S. daphnoides, N = 22; S. purpurea, N = 16; S. triandra, N = 16). Whole-model adjusted R2 and P values of the effects added to the model last (in boldface type) are given. Parentheses denote nested effects

 
Seed number decreased with seed mass at all morphological levels. This decrease was especially evident for ovule number within fruits within the Salix species (Fig. 3A). Our data allow no formal analysis of this relationship, because ovule number per fruit was constant in four of the species and not investigated in multiple fruits per plant. In a linear model of seed number per catkin (compare Fig. 3B), genus identity and seed mass explained 42% of the variation (model 3, Table 4), but an alternative model containing genus and species identity explained much more variation (model 2). The addition of seed mass as a factor in this model (model 4) yielded no significant improvement. Seed number per plant was also related to seed mass (Fig. 3C); however, only 34% of the variation was explained by genus identity and seed mass (model 3, Table 4). Genus and species identity together explained 61% of the variation. In this case, the addition of seed mass to the model was significant (model 4). Within species, no significant relationship between seed number and seed mass could be detected (model 5).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The short longevity of seeds of Salicaceae from flood plains (cf. Niiyama, 1990 ; van Splunder et al., 1995 ) may constitute an adaptation to frequent and devastating disturbance that renders seed bank formation useless. This interpretation is supported by the fact that other species growing on temperate flood plains have a similar germination ecology, such as the perennial herbs Tussilago farfara and Petasites hybridus (Grime et al., 1981 ) and the shrub Myricaria germanica (Bill et al., 1997 ). Furthermore, Salix species that do exhibit seed dormancy are from arctic habitats (Densmore and Zasada, 1983 ). However, other species from the flood plain habitat, such as Alnus incana, produce a short-term seed bank (Schütt et al., 1999 ).

Seed longevity under field conditions may be even shorter than in our study because fluctuations in temperature and humidity that result in a decrease in seed longevity (Junttila, 1976 ; Siegel and Brock, 1990 ) are more prominent in the field than under our storage conditions (cf. Fig. 1). According to Hung et al. (2001) , this effect is not from the fluctuations per se, but from a semi-logarithmic relationship between storage temperature and seed longevity (e.g., Ellis, 1988 ). The actual longevity of seeds in the field thus depends on the precise microclimatic conditions encountered. However, general differences between species are likely to be preserved under field conditions, although the differences between early- and late-seeding species may be reduced because of the seasonal increase in temperature (Fig. 1).

Because seeds germinate as soon as they contact a moist surface, our estimates of seed longevity are only relevant for dry weather. Such conditions often persist for several weeks during the seed release period (Francesco Baruffi, Autorita di Bacino dei Fiume Isonzo, Tagliamento, Livenza, Italy, personal communication), and Salicaceae seeds may remain in the air or in bulks entangled on obstacles such as woody debris or vegetation until washed down by rain (S. Karrenberg, personal observation). Such a situation would lead to an advantage of P. nigra over the Salix species, and S. elaeagnos and S. daphnoides would have a better chance for regeneration than S. triandra, S. purpurea, or S. alba. However, the seed release period was longer in S. triandra than in the other species during the study (Fig. 1) and in 1999 (Karrenberg et al., 2002b ) and was also observed by van Splunder et al. (1995) in the Netherlands. A prolonged dispersal period or increased variability in dispersal time between individuals could enhance regeneration chances in S. triandra.

Seed longevity was positively related to seed mass in accordance with our hypothesis and in contrast to the general contention that small seeds are longer lived than large seeds (Rees, 1996 ; Hodkinson et al., 1998 ). However, this relation is based on dormancy characteristics rather than on seed longevity in the absence of dormancy. A decrease of seed longevity with seed mass was also found in small-seeded Fabaceae by Gáspár et al. (1981) and is generally supported by Priestley (1986) . Conversely, seed mass was not related to seed longevity in six species of Salix from flood plains in Japan (Niiyama, 1990 ) but how seeds were collected, i.e., how many individuals they represented, was not mentioned. As our results show, differences between individuals in seed mass and seed longevity can be considerable. Both in our study and in the study of Niiyama (1990) there was no distinction between the two proposed subgenera of Salix, Salix and Vetrix (Skvortsov, 1999 ), in either seed longevity or seed mass, nor was there any relationship to flowering time. Reasons for differences between species could lie in the nature or amount of biochemical components that prevent damage to the embryo in the dry state (e.g., Walters, 1998 ). In addition, Salicaceae seeds are already green at dispersal, and Densmore and Zasada (1983) suggested that the rapid loss of viability in nondormant Salix seeds could be related to chlorophyll degeneration. Salix triandra might differ from the other species in our study biochemically, resulting in comparatively high seed longevity despite low seed mass.

Seed mass was negatively related to seed number, demonstrating a phenotypic seed size–number trade-off in the Salicaceae. The closest relationship was observed within the genus Salix at the smallest morphological level—individual fruits—as also found in Plantago (Primack, 1979 ) and Epilobium (Stöcklin, 1999 ). Seed number per catkin was less closely related to seed mass but it was species-specific, suggesting that selection pressures other than the size–number trade-off may have acted on seed number per catkin, such as the balance between insect and wind pollination (Karrenberg et al., 2002b ). Within species, we found no relationship between seed mass and seed number. Here we must take into account that the maximum seed numbers were estimated from ovule numbers and the percentage of matured fruits, but differences in the number of matured seeds per fruit were not detected.

Generally, a size–number trade-off can be treated as an optimization problem, suggesting one optimal seed size per habitat (e.g., Smith and Fretwell, 1974 ). On the other hand, game theoretical models, which also include the seed sizes of competitors, predict coexistence of several seed sizes in the same habitat as an evolutionary stable strategy (Rees and Westoby, 1997 ; Geritz et al., 1999 ). While phenological spread is an important factor in the coexistence of flood plain Salicaceae (Fagerström and Ågren, 1980 ; van Splunder et al., 1995 ), these species may also be an example of the multiple optima of seed mass in one habitat that are mediated by a size–number trade-off (Geritz et al., 1999 ). This phenotypic trade-off is emphasized by an increase of seed longevity with increasing seed size.


   FOOTNOTES
 
1 The authors thank D. Ramseier for the germination chambers, the department of statistics at ETH-Zürich for advice, and J. Kollmann and P. J. Edwards for valuable comments on earlier versions of this manuscript. This work was supported by Research Grant 0-20572-98 from the Forschungskommission ETH-Zürich. Back

2 Author for reprint requests, present address: Indiana University, Department of Biology, Jordan Hall, 1001 East Third Street, Bloomington, Indiana 47405 USA (tel.: 812 855 9018; fax: 812 855 6705; karrenberg{at}bio.indiana.edu ) Back


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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S. L. Halpern
Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses
Am. J. Botany, February 1, 2005; 92(2): 205 - 213.
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