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Annals of Botany 2005 95(6):1017-1023; doi:10.1093/aob/mci109
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© The Author 2005. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oupjournals.org

Selective Seed Abortion Affects the Performance of the Offspring in Bauhinia ungulata

JORGE I. MENA-ALÍ* and OSCAR J. ROCHA{dagger}

Escuela de Biología, Universidad de Costa Rica, Ciudad Universitaria Rodrigo Facio, San José, Costa Rica

* For correspondence at: Department of Biology, Pennsylvania State University. 208 Mueller Laboratory, University Park, PA 16802, USA. E-mail jim123{at}psu.edu

Received: 11 November 2004    Returned for revision: 12 January 2005    Accepted: 22 January 2005    Published electronically: 4 March 2005


   ABSTRACT
TOP
 FOOTNOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

• Background and Aims Under the microgametophytic competition hypothesis, a non-random pattern of seed abortion is expected, in which only the most vigorous seeds reach maturity. In a previous study, it was found that Bauhinia ungulata (Fabaceae) exhibits a pattern of seed abortion dependent on the position of the ovule within the ovary; ovules located in the stylar half of the fruit, close to the point of entry of pollen tubes to the ovary, have a low probability of seed abortion, whereas ovules in the basal half of the fruit are aborted with a high probability.

• Methods A series of experimental fruits was generated, in which ovules from either the stylar (treatments 1 and 2) or the basal (treatments 3 and 4) half of fruits were destroyed, to evaluate whether these patterns of selective seed abortion have an effect on the vigour of the offspring in B. ungulata.

• Key Results Only 53 % of the seed from control fruits germinated. Seed set in fruits from treatments 1 and 2 showed a significantly lower (33–43 %) percentage of germination; the germination of seeds from fruits in treatments 3 and 4 (49–51 %) did not differ from control seeds. In addition, it was found that the differences in vigour of the offspring are not random with respect to the position of the ovule in the pod.

• Conclusions The overall performance of the seeds correlated with their likelihood of maturation. Seeds located at the basal half of the treatment fruits showed lower values of vigour than seeds located on the stylar half. The differences were more marked for early measures of fitness.

Key words: Bauhinia ungulata, Fabaceae, fitness, Guanacaste Conservation Area, microgametophytic competition, offspring vigour, selective seed abortion


   INTRODUCTION
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Seed growth and development during reproduction represent a major investment of resources by the maternal plant. Each seed must have enough reserves to go through the initial stages of germination and seedling establishment. However, successful establishment will depend, at least in part, on the overall vigour of each seed. Since resources for reproduction are typically limited, plants can only mature a certain fraction of the seeds that initiate growth (Lee and Bazzaz, 1982Go; Lee, 1988Go; Helenurm and Schaal, 1996Go; Corbet, 1998Go). From an evolutionary perspective, selective allocation of resources to those seeds with a higher probability of survival should be favoured by natural selection (Bawa and Webb, 1984Go). The critical question is: How can plants determine the vigour of their progeny?

Several studies have observed that, even during early stages of seed development, the fitness of the offspring is often correlated with the fitness of the male parent (Stephenson, 1981Go; Marshall and Ellstrand, 1986Go; Niesenbaum, 1999Go; Winsor et al., 2000Go). Therefore, one potential way to detect differences in quality among seeds is by screening the vigour of the potential fathers (Davis et al., 1987Go), based on the performance of the pollen tubes growing towards the ovary. Stronger and faster-growing pollen tubes will reach the ovary first and fertilize more ovules, while slower-growing tubes, on the other hand, will have a lower probability of fertilizing any ovules (Latta, 1995Go; Brown and Kephart, 1999Go). Consequently, ovules fertilized by stronger pollen tubes will produce stronger embryos, while weaker embryos are the product of fertilization by slower-growing tubes. Under resource limitation, the developing embryos in turn will have to compete with each other for the limited maternal resources. Therefore, stronger embryos will have a higher probability of reaching maturity, whereas weaker embryos will not gather enough resources, and will starve and eventually die. This has been called the hypothesis of microgametophytic competition and it provides a mechanism for female choice in plants (Stephenson and Bertin, 1983Go; Marshall and Ellstrand, 1986Go).

The establishment of a highly competitive environment where only the stronger, more vigorous embryos will complete their development and mature into seeds is critical for microgametophytic competition to operate. If competition is relaxed, then the probability of each embryo reaching maturity increases. This could lead to the production of offspring that are, on average, less fit than offspring produced in highly competitive environments (Rocha and Stephenson, 1990Go, 1991Go). In legumes, the ovules are arranged in a linear fashion within the ovary (Bawa and Buckley, 1989Go). Some ovules are located closer to the point of entry of pollen tubes to the ovary. Therefore, those ovules will be more likely to be fertilized by fast-growing tubes. By contrast, ovules located farther from the point of entry to the ovary will be fertilized by slow-growing tubes.

In a previous study (Mena-Alí and Rocha, 2005Go) it was found that the probability of seed abortion in fruits of Bauhinia ungulata is non-random and dependent upon the position of the ovule within the ovary. Ovules located far from the style showed lower rates of fertilization, and seeds developed in these positions showed a higher probability of early seed abortion. These patterns seemed to follow the expectations of the microgametophytic competition hypothesis. If this is true, then the fitness of the offspring would be affected when the competition is relaxed. Seeds set in positions with a high probability of abortion (farther from the point of entry of pollen tubes into the ovary) are expected to show a reduced fitness under conditions of relaxed competition; seeds set in positions with a low probability of abortion (closer to the style), on the other hand, are expected to show no difference in fitness when the competition is reduced.

In this study, the effect of ovule position was examined within the fruit on progeny in B. ungulata. In order to do so, a series of experimental manipulations was conducted to remove ovules from certain positions within the fruit, assuming that such manipulations should reduce the levels of competition and favour the development of otherwise abortive ovules. Finally, an evaluation was carried out to see if relaxing the competition among developing embryos would result in a reduction in vigour of the seedlings of B. ungulata, and to see if this reduction is dependent upon the likelihood of selective abortion.


   MATERIALS AND METHODS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Study site
This study was conducted in Santa Rosa National Park, which is located in north-western Costa Rica (10°45' to 11°00'N and 85°30' to 85°45'W) and is part of the Guanacaste Conservation Area (ACG). The vegetation in the study area is classified as moist transition dry forest (Holdridge, 1967Go; Hartshorn, 1983Go). The park includes a mosaic of forests of different ages and abandoned pastures (Hartshorn, 1983Go; Janzen, 1983Go; Gerhardt, 1993Go). The climate is highly seasonal, with a well-defined dry season from late November to mid-May. Annual rainfall ranges between 800 and 2600 mm, with an annual mean of 1423·4 mm. The annual mean temperature is 25·7 °C, and the mean annual relative humidity is 81 % (Rojas Jiménez, 2001Go).

Study species
Bauhinia ungulata L. (Fabaceae: Caesalpinioideae) is a self-incompatible, small tree, 5–10 m high, typical of semideciduous and deciduous forests. It is distributed from southern Mexico to the dry areas of Venezuela and Colombia (Holdridge et al., 1997Go). In Costa Rica, this species is found only in the dry parts of the North Pacific region.

Flowering occurs during the dry season, from December to March. Bauhinia ungulata has a floral dimorphism based on the length of the pistil. Most of the flowers have a pistil longer than the anthers. However, some flowers have a very short pistil, the stigma being found right next to the anthers (Wunderlin, 1983Go). Flower anthesis is crepuscular, the flowers opening around 1700 h and releasing pollen soon afterwards. Nectar is secreted within 1 h of flower opening and seems to be secreted throughout the night (Mena-Alí, 2003Go; J. I. Mena-Alí, unpubl. res.). Bauhinia ungulata is bat-pollinated. The main pollinator is Glossophaga soricina (Heithaus et al., 1974Go, 1982Go), although it is commonly visited by other species of bats, including Phyllostomus discolor (Ramirez et al., 1984Go), Carollia perspicillata and Anoura sp. (Fischer, 1992Go). Fruit set occurs from January to May, at the time when the species is flushing its new foliage. The pod is dehiscent and the seeds (mean length ± standard deviaiton: 4·841 ± 0·014 mm) are ballistically dispersed by the sudden split of the two parts of the pod (Holdridge et al., 1997Go) throwing the seeds away from the mother tree. The mean number of seeds is 19, although it ranges from 10 to 30 seeds per pod (Mena-Alí, 2003Go).

Experimental manipulations
A series of experimental manipulations was conducted to test for the effects of selective seed abortion on the likelihood of seed development and progeny vigour. During the dry season of 2001, two trees of B. ungulata were selected, on the basis of their fruit production, size and location. The high average fruit production of the two selected trees assured access to enough fruits to replicate all experimental manipulations. Finally, both trees were located near the laboratory facilities of ACG, which aided in the access of fruits for manipulation and collection.

For each tree, long-styled flowers bearing between 19 and 21 ovules per ovary were selected; the number of ovules was determined by viewing each ovary against a light. To simplify the definition of the experimental manipulations, open pollination was allowed to occur; supplemental pollination was performed late during the night to assure proper levels of pollination. Thirty-six hours after pollination, each developing fruit was assigned to one of four experimental manipulations. Each manipulation consisted of the selective destruction of some of the ovules within the developing fruits by piercing them with a fine needle (Fig. 1). To define the manipulations, the ovary was divided into four sections, each section containing five ovules. Each treatment involved the destruction of all the ovules within one of these sections within the ovary. This manipulation was conducted on a total of 80 fruits, where ten fruits had their ovules destroyed in one of the four possible sections (ten fruits/treatment x four treatments/tree x two trees). A control treatment was defined, in which none of the ovules were killed; however, these fruits were pierced between the ovules, to account for possible effects of fruit piercing and manipulation on fruit and seed success. This control treatment was replicated ten times per tree, for a total of 20 control fruits.



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  		FIG. 1. Diagram of experimental design. The fruits were divided into four sections of five ovules each. Sections located on the stylar half contain ovules with a low probability of seed abortion, while sections 3 and 4 have a high probability of seed abortion (Mena-Alí and Rocha, 2005Go). The analysis consisted of the comparison of each section from three categories: control fruits, fruits with a stylar section removed, and fruits with one basal section removed. For instance, the effect of the relaxation experiment on the performance of seeds developed in section 1 was assessed by comparing seeds from section 1 of control fruits, fruits from treatment 2 (seldom aborted seeds removed) and fruits from treatments 3 and 4 (often aborted positions removed). By comparing the results for each section, it is possible to measure the relative competitive ability of seeds located in different regions of the fruit.

 
After fruit maturation, all fruits were collected before dehiscence. If for any reason a particular fruit was lost during the set-up period, an attempt was made to replace it to keep the sample size as high and constant as possible. However, some fruits were lost during the maturation period, mainly due to mechanical damage, as some treated fruits did not expand in the region where the embryos were killed; this made that section of the fruit more prone to breakage. At the end of the season a total of 74 fruits was collected. These fruits were brought to the laboratory, where all of them were opened and each seed stored according to its position within the fruit, maternal tree, and experimental manipulation. All seeds were weighed (in mg), and their length and width (both in cm) measured. Lastly, an index of seed size as the ratio weight/(length x width) was calculated (hereafter presented as arbitrary units).

Progeny performance
To determine whether the relaxation of competition in treated fruits led to a reduced vigour of the seeds, a greenhouse experiment was conducted to measure the performance of the offspring. This experiment was performed in the greenhouse of the Escuela de Biología, Universidad de Costa Rica, from May to December 2001. Each seed was planted in an individual 10-oz. (approx. 300 g) pot. The pots were randomly distributed on the greenhouse bench, and watered as required.

For each seed, the time to germination and to the production of the first fully extended leaf was recorded. For each seedling, at both 15 d and 60 d after germination, the number of leaves, the height (in mm) and the diameter above the cotyledon scar (in mm) was recorded. In addition, at 60 d after germination, the seedlings were collected, and the total leaf area (in cm2), the length of the root (in mm) and the total biomass of the shoot and root (in mg) were recorded.

A {chi}2 analysis was performed to determine differences in percentage seed germination between trees, among manipulations, and among sections/positions. In order to examine the effects of seed position on the vigour of the progeny of the control fruits, a fixed-model analysis of variance (GLM; SAS, 1985Go) was conducted. To examine for the effects of the probability of seed abortion on the vigour of the progeny produced by treated fruits compared with the control fruits, a separate analysis for each section was performed, using a fixed-model analysis of variance (GLM; SAS, 1985Go). In these analyses, the index of seed size described above was used as a covariate.


   RESULTS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Progeny performance
The overall seed germination was 46·95 %; however, tree 1 showed a significantly higher percentage germination than tree 2 (51·68 % and 42·33 % for tree 1 and tree 2, respectively, , P = 0·001; Table 1). Seed germination also differed among treatments. Seed from control fruits had the highest percentage germination (52·8 %). Seed from treatments 1 and 2, which involved the destruction of a section with low probability of abortion (sections 1 and 2; see Fig. 1), showed a significantly lower percentage germination (33·67 % for treatment 1; 43·88 % for treatment 2), compared with control seeds ({chi}22,0·95 = 18·167, P < 0·001). For treatments 3 and 4, in which seeds with a high probability of abortion were destroyed, seed germination was slightly lower (48·98 % for treatment 3; 51·13 % for treatment 4) when compared with the control, but the difference was not significant (, P < 0·5).


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  		TABLE 1. Percentage germination of seeds from control and treatment fruits in Bauhinia ungulata

 
The size of the seed did not differ between maternal trees (tree 1: mean = 1·319 ± 0·197; tree 2: mean = 1·336 ± 0·185; t = 1·48, P = 0·140); however, size did vary among treatments (Fig. 2). The control fruits produced larger seeds (mean = 1·3480 ± 0·0106) than any of the treatment fruits. Furthermore, seeds from treatments 1 (mean = 1·2840 ± 0·0136) and 2 (mean = 1·3200 ± 0·0136) were smaller than seeds set in treatments 3 (mean = 1·3290 ± 0·0136) and 4 (mean = 1·3430 ± 0·0128; F4,1127 = 4·06, P = 0·003).



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  		FIG. 2. Effect of ovule removal on seed size in Bauhinia ungulata. The mean (± s.e.) of the seed size index (arbitrary units; see text) is plotted against the respective treatment. Each treatment consisted of the removal of all ovules within certain section of the fruit (see text for details). Removing seeds from a section with low probability of abortion resulted in a significant decrease of seed size; no effect was observed when seeds with a high probability of abortion were removed.

 
Analysis of control fruits
The results for the analysis of variance revealed that there is no significant effect of position on any of the measured variables for vigour in control fruits (Table 2). Seed size had a significant effect on the time to germination and the number of days from germination to the opening of the first leaf (Table 2). The maternal trees seemed not to differ for almost all of the estimates of fitness; however, time to germination and the increase in diameter at 60 d were strongly affected by the identity of the tree that produced the seed.


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  		TABLE 2. Analysis of variance for the effects of ovule position on the vigour of seeds set on control fruits in Bauhinia ungulata

 
Analysis of treatment fruits
Time to germination was affected by seed size, tree and treatment, for all experimental plants regardless of the section in which seeds were destroyed (Table 3). Overall, it was found that the time to the first leaf was affected by seed size for ovules from section 4 where, in general, plants from larger seed needed less time to produce their first leaf. Multivariate analysis of variance also revealed significant variation in the days to first leaf between trees in ovules from sections 2 and 3.


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  		TABLE 3. Analysis of variance for the effects of ovule position on the vigour of seeds of treated and control fruits in Bauhinia ungulata

 
The number of leaves at 15 d after germination was affected by seed size for ovules in section 2 only. This trait also showed significant variation between trees when ovules were produced in the first three sections; only in section 3 did this variable vary among treatments.

At 60 d, the original seed size had a significant effect on shoot weight and leaf area in seeds from section 1; treatment had an effect on the length of the root for these ovules. For ovules from section 3, seed size and seed position had significant effects on three of the indicators of vigour at 60 d: increase in diameter, root weight and root ratio at 60 d. These ovules showed differences in the number of new leaves and the shoot ratio at 60 d when the treatments were compared. When ovules developed seeds in section 4, seed size had an effect on increase in height at 60 d.


   DISCUSSION
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
The results presented in this study show that only approximately half of the seeds produced by the fruits of Bauhinia ungulata are able to germinate, and that seed germination is affected by the position in which the seed is produced. In addition, the present data revealed that the differences in vigour among offspring of B. ungulata are not random with respect to the position of ovules in the pod: the overall performance of the seeds is, on the contrary, associated with the likelihood of seed maturation. Overall, seed positions located at the basal half of the treatment fruits showed lower vigour than seeds located on the stylar half of the fruits. The effect of position on vigour is observed mainly in ovules from the two basal sections, 3 and 4; in general, seed size and tree identity are the main variables affecting vigour, especially at early stages.

There are many factors affecting seed germination, some of them being genetic differences among seeds. However, seed germination also depends on external variables such as temperature and water availability. One factor that might be affecting germination success is the absence of scarification treatments, making water uptake and root emergence harder for the seeds to complete.

When seed germination was analysed among treatments, it was found that treatments 1 and 2 had a lower percentage germination than the control, whereas treatments 3 and 4 showed values of percentage germination similar to the control fruits. In treatments 1 and 2, seeds with a low probability of abortion were selectively destroyed; this reduction in competition probably allowed less-fit offspring to complete their development and reach maturity. This might explain the lower probability of germination observed. By contrast, for treatments 3 and 4, seeds with a high probability of abortion were removed; therefore the reduction of competition was expected to have a lesser effect on the performance of the remaining seeds. In accordance with this expectation, the percentage germination on these treatments was not significantly different from the control fruits (Table 1). Gutierrez et al. (1996)Go found similar patterns in Ulex gallii (Fabaceae); the probability of seed maturation depended on the position it occupied in the fruit. Furthermore, positions with a high probability of abortion produced lighter seeds than positions with a low probability of abortion; this trait correlated with germination.

This dependence of the performance of the offspring on the position of the seed in Bauhinia was further supported when each section was analysed separately. Seeds developed in the stylar half of treated fruits gave patterns of offspring performance similar to the control fruits (Tables 2 and 3A and B). By contrast, the performance of the seedlings produced in the basal half (sections 3 and 4) was affected by this reduction in competition. This difference in responses suggests that the reduction in fitness may be caused by an increase in the frequency of maturation of less-fit seed when the competition is relaxed, rather than by the piercing technique used to obtain the experimental conditions of reduced competition.

In Phaseolus coccineus, Rocha and Stephenson (1990Go, 1991Go) found that, when competition was relaxed allowing maturation of seeds with a high probability of abortion, these showed a lower vigour than seeds produced in positions with a low probability of abortion. Other studies have found similar results. Selective seed abortion in Cynoglossum officinale (Boraginaceae) resulted in fitter offspring with increased percentages of survival (Melser and Klinkhamer, 2001Go). In Mirabilis jalapa (Nyctaginaceae), pollen performance correlated with the vigour of the offspring; furthermore, selective abortion produced more vigorous progeny (Niesenbaum, 1999Go). In Acacia caven (Fabaceae), the performance of seedlings was associated with the probability of maturation of fruits (Torres et al., 2002Go).

In B. ungulata, it was found that the only consistent effects of treatment were on early fitness variables: days to germination and days to first leaf (Tables 2 and 3). This is by contrast with findings in other studies. In P. coccineus, the position of the seed had a significant effect on all estimates of fitness, from seed weight and germination to flower production (Rocha and Stephenson, 1991Go).

One reason why it was not possible to detect differences at later stages of seedling growth might be that the parameters of late fitness measured in B. ungulata dealt with general seedling growth. These variables might be under strong selective canalization, therefore showing less observable variation than early estimates of vigour. This also suggests that early establishment is the critical stage for the survival of the seeds. Once the seedlings become established, their growth might follow a strongly canalized allometric pattern; therefore the variables we measured would not reflect any differences in vigour among offspring at later stages.

Another reason why it was not possible to detect differences at later stages of growth might be that other variables, like protection against herbivores or responses to drought, were not examined. Variation in the vigour of the offspring might affect the differential allocation of resources to these factors at post-establishment stages. These factors might be especially important, since each individual has to grow for several years before reaching a reproductive status. These factors might exert a strong selection on young plants in nature (Gerhardt, 1993Go), but it might be hard to detect any differences under greenhouse conditions. Studies of seed production and survival have shown that, in the Santa Rosa National Park, the initial seed output of many tree species is highly reduced by rodent predation (Janzen, 1967Go; Janzen et al., 1990Go; O. J. Rocha, Universidad de Costa Rica, unpubl. res.). Therefore, faster rates of germination might be constantly selected and faster-germinating seeds might have a higher probability of survival. Studies of survival and establishment under natural conditions are needed, along with long-term follow-up studies to determine to what extent the performance of the offspring is affected by the patterns of seed abortion in perennial species.


   ACKNOWLEDGEMENTS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
We thank M. Zaldívar, J. Blair and two anonymous reviewers for advice, comments, and/or criticisms on a previous version of this manuscript, The Guanacaste Conservation Area (ACG) and the staff of Santa Rosa National Park for their collaboration. This work was supported by the International Plant Genetic Resources Institute and the Center for International Forestry Research (grants 96/073, 97/052, 98/049 and 00/066), a University of Costa Rica grant (VI-111-91223) to O.J.R., and an Andrew W. Mellon Foundation grant to O.J.R.


   FOOTNOTES
TOP
 FOOTNOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
{dagger} Present address: Department of Biological Sciences, Kent State University, Kent, OH 44242, USA Back


   LITERATURE CITED
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 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

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