Plant Reprod (2015) 28:111–119 DOI 10.1007/s00497-015-0260-8
ORIGINAL ARTICLE
Reproduction and vegetative growth in the dioecious shrub Acer barbinerve in temperate forests of Northeast China Juan Wang • Chunyu Zhang • Klaus V. Gadow Yanxia Cheng • Xiuhai Zhao
•
Received: 8 October 2014 / Accepted: 19 February 2015 / Published online: 18 March 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Key message Trade-off in dioecious plant. The trade-off between reproduction, vegetative growth and maintenance is a major issue in the life history of an organism and a record of the process which is producing the largest possible number of living offspring by natural selection. Dioecious species afford an excellent opportunity for detecting such possible trade-offs in resource allocation. In this study, we selected the dioecious shrub Acer barbinerve to examine possible trade-offs between reproduction and vegetative growth in both genders at different modular levels during three successive years. Reproductive and vegetative biomass values were assessed during successive years to evaluate their intra-annual and inter-annual trade-offs. These trade-offs were examined at shoot, branch and shrub modular levels in Acer barbinerve shrubs. An intra-annual trade-off was detected at the shoot level for both genders in 2011 and 2012. Both males and females
showed a negative correlation between reproduction and vegetative growth, but this was more prominent in males. For the females of the species, inter-annual trade-offs were only found at branch and shrub levels. Slightly negative correlations in females were detected between the reproduction in 2012 and the reproduction in the two previous years. The gender ratio was significantly male biased during the three successive years of our investigation. Females had higher mortality rates in the larger diameter classes, both in 2011 and 2012. This study revealed a clear trade-off between reproduction and vegetative growth in Acer barbinerve, but results varied between males and females. The degree of autonomy of the different modular levels may affect the ability to detect such trade-offs. Keywords Trade-off Modular level Acer barbinerve Dioecious species
Introduction Communicated by Andrew Stephenson.
Electronic supplementary material The online version of this article (doi:10.1007/s00497-015-0260-8) contains supplementary material, which is available to authorized users. J. Wang C. Zhang Y. Cheng (&) X. Zhao (&) Forest College, Key Laboratory for Forest Resources and Ecosystem Processes of Beijing, Beijing Forestry University, No. 35 Qinghua East Road, Haidian District, Beijing, People’s Republic of China e-mail: [email protected] X. Zhao e-mail: [email protected] K. V. Gadow Faculty of Forestry and Forest Ecology, Georg-AugustUniversity Go¨ttingen, Bu¨sgenweg 5, 37077 Go¨ttingen, Germany
The theory of life history, which records the key events in an organisms’ lifetime, is concerned with the age of sexual maturity, the reproductive lifespan and aging, as well as the number and size of the offspring (Kozlowski and Wiegert 1986). Any organism must allocate resources to vegetative growth, reproduction and survival. These processes depend on the physical and ecological environment of the organism. Available resources are limited; hence, energy used for one function by an individual organism will diminish the energy used for another function (Gadgil and Bossert 1970; Bell 1980; Stearns 1989). Different investments in these functions reflect the various ways of resource allocation in an individual organism to sustain life. The goal of life history theory is to understand the variation in such
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strategies. Given this knowledge, models can be built in order to predict what kinds of traits will be favored in different environments (Wang et al. 2013a, b; Knapp et al. 2001; Hesse and Pannell 2011). The trade-off among reproduction, vegetative growth and maintenance is a key to the life history of an organism. When resources in a particular environment are limited, plants may increase resource allocation to reproduction from their limited reserves, and consequently, the allocation to other functions, such as vegetative growth, maintenance and even future reproduction, is reduced (Willson 1983; Bazzaz et al. 1987). A high vegetative growth rate can increase the possibility of higher reproduction in the future, a typical trade-off which may occur in perennial organisms. The physiological functions will start declining; the higher cost of reproduction may lead to a higher possibility of mortality. This trade-off in an organism not only occurs in the current reproduction season, but also is maintained during its entire lifespan (Wenk and Falster 2014). Dioecious plants, in which the male and female flowers are borne on separate individuals, present an excellent opportunity for detecting such possible trade-offs in resource allocation. In dioecious plants, resource allocation may differ between males and females (Lloyd and Webb 1977). Males promote their mating chances by increasing resource allocation in pollen reproduction and pollinator attractiveness. Females promote the number and quality of offspring by increasing resource allocation in fruit and seed production. The energy requirements for producing fruits and seeds are far greater than for just producing flowers (Lloyd and Webb 1977; Jing and Coley 1990). Consequently, females are likely to allocate more resources to reproduction than males. Biomass allocation to reproduction in three Chamaedorea palms was 3 times higher in female than in male plants (Cepeda-Cornejo and Dirzo 2010). Females in Eurya japonica allocated about 1.6 times more biomass per tree to reproduction than males. At branch level, the biomass of reproduction was 4.4 times higher in females than in males (Suzuki 2005). When the resources, which plants gain from the environment, are limited, the trade-offs in females between reproduction and growth, future reproduction or survival were found to be more pronounced than that in males (Antos and Allen 1990; Delph 1999). However, there are indications that the interpretation of such trade-offs is not always very clear regarding females. Compensatory mechanisms for higher reproductive costs in females have been examined in several studies. Female reproductive organs in Silene latifolia are longer lived and contribute more carbon to their own support than male reproductive structures (Laporte and Delph 1996). Females in Salix integra had greater biomass allocation to
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photosynthetic organs and higher photosynthetic rates than males. Females which had greater reproductive costs did not reduce growth, but increased the carbon uptake ability of different modular units in well-illuminated microenvironments (Tozawa et al. 2009). Females pay a high price for reproduction during their lifetime. They often have lower frequency of reproduction, lower growth rates (especially in woody species) and higher mortality rates and are older at their first reproductive stage than males (Delph 1999; Obeso 2002). Often, the trade-off between reproduction and vegetative growth may be difficult to detect, even in dioecious species. The trade-off may be hidden at higher modular levels but may be more discernable at a lower modular level. The degree of autonomy of the different plant organs might be an important reason for this (Obeso et al. 1998). For example, if branches are autonomous, the resource allocation may show a small-scale balance between reproduction and vegetative growth at branch level. But the cost of reproduction may be compensated by non-reproductive branches at shrub level. The trade-off can only be detected at branch level but not at shrub level. Conversely, if branches are partially autonomous, the resources for reproduction will be translated among branches. The tradeoff will be just detected at shrub level but not at branch level. Matsuyama and Sakimoto (2008) identified a tradeoff between reproduction and vegetative growth at shoot level, while this trade-off disappeared at the whole shrub level. Therefore, our objective in this study is to determine the trade-offs at different modular levels. The dioecious shrub Acer barbinerve was chosen as a convenient species because it is a shrub that can be studied at several such modular levels. Moreover, it is a perennial which allows for the study of the cost of reproduction on future growth and reproduction during three successive years. We hypothesize that there is a trade-off between reproduction and vegetative growth in this particular species. If such a trade-off exists, then we want to know whether it exists within the same year (intra-annually) and/ or between different years (inter-annually) and whether there are differences in the trade-off between the two genders. Finally, we want to know whether the modular level (shoot, branch or shrub) has an effect on detecting possible trade-offs.
Materials and methods Study site and species Our study was conducted at the Jiaohe forest in Jilin province, northeastern China (43°580 N, 127°430 E; elevation 450 m a.s.l.), within a temperate continental mountain
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climate zone. The average annual temperature is 3.8 °C. The hottest month is July with an average day temperature of 21.7 °C; the coldest month is January with an average day temperature of -18.6 °C. The average annual precipitation is 695.9 mm. The soils are dark brown forest soils varying in depth between 20 and 100 cm. The forest type is a mixed broadleaf–conifer forest (Wang et al. 2013a, b). An experimental field plot, covering an area of 11.52 ha (320 m 9 360 m), was established in 2009. The main coniferous species in the plot are Picea jezoensis, Pinus koraiensis and Abies nephrolepis. The dominant deciduous species are Fraxinus mandshurica and so on. The studied species is Acer barbinerve which is quite common in the plot. Acer barbinerve is a perennial dioecious shrub or small multi-stemmed shrub which occurs in Korea, Russia and northeastern China. The life span of Acer barbinerve is about 10 years. The flowering season is in May, and the fruit season is from June to July. Acer barbinerve is a phenophase overlapper, simultaneously producing leaves and flowers, followed by fruiting. The leaves are deciduous. The inflorescence is racemose which contains 5–7 flowers. Every single male flower has four petals and four stamens, while a single female flower has four petals and one stigma. The infructescence contains 5–7 samaras (Wu and Raven 2004). Measurements The number of reproductive male and female trees were different in the three successive years, involving 25 females and 50 males in 2010, 100 females and 100 males in 2011, and 78 females and 100 males in 2012. This study is concerned with the trade-off between reproduction and vegetative growth at four modular levels, i.e., shoot, branch, shrub as well as population. Under field conditions, the different positions of the tree crown may be subjected to slightly different micro climates, causing different biomass allocations in the different horizontal sections of the crown. Thus, five to ten reproductive branches from every single shrub were randomly selected in four crown compartments, i.e., four horizontal sections, following Henriksson (2001). Each sampled reproductive branch is made up of several shoots. A shoot includes leaves, flowers or fruits (Fig. 1). At shoot level, the flowers (male and female) and leaves of all shoots on the sampled branches were counted in May (flowering season), while fruits were counted in July (fruiting season). At branch level, the number of flowers, leaves, new shoots and fruits from all selected branches in the sample shrubs were assessed. At shrub level, the branches were counted in every sampled shrub. The number of branches was multiplied by the mean number of flowers, leaves and fruits of sampled branches
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on each shrub. This approach produced an estimate of the number of flowers, leaves and fruits on every single flowering shrub. One reproductive branch was taken from every single sample shrub for estimating the biomass of flowers, new shoots and leaves. At least ten fruits were taken from every single shrub for estimating the fruit biomass. Every sampled shrub had its individual flower, leaf and fruit biomass. All harvested branches and fruits were weighed after oven drying at 80 °C for 2 days. The numbers of leaves, new shoots, flowers and fruits at each modular level were multiplied by the mean biomass of leaves, new shoots, flowers and fruits to estimate the biomass of leaves, new shoots, flowers and fruits for every sampled shrub at each modular level. The biomass of flowers and fruits represented the reproductive growth; the biomass of leaves and new shoots represented the vegetative growth. The equations used to calculate the biomass of flowers, fruits, foliage and new shoots at shoot, branch and shrub level are presented in Table 1. At population level, we investigated the numbers of all flowering shrubs in the plot during each of the three successive years. The numbers of flowering female, male and non-reproductive shrubs were recorded for every year and used to estimate the sex ratio in the successive years. The diameter at breast height (DBH) of all shrubs was measured at the beginning of the growing season in each year. If the shrubs were multi-stemmed, the diameter at breast height (DBH) of each stem was measured. Statistical analysis A general linear model (GLM) was used to examine the trade-off between reproductive and vegetative structures at shoot, branch and shrub levels, both within the same year (intra-annually) and between different years (inter-annually), using the R statistical software. In the GLM examination of the intra-annual trade-off, the vegetative biomass values represented the explanatory variables, the reproductive biomass was the response variable. The reproductive biomass was the biomass of flowers in male and the biomass of flowers and fruits in female. In the GLM examination of the inter-annual trade-off, the reproductive biomass in 2010 and 2011 were the explanatory variables, while the reproductive biomass in 2012 was the response variable. The reproductive biomass included the biomass of flowers in males and the biomass of flowers and fruits in females. Shrubs were grouped into diameter at breast height (DBH) classes, and the sex ratio was determined for each DBH class and each year during the study period. The likelihood-ratio test was used to test whether two observed frequency distributions belong to the same theoretical distribution. This test was used to detect deviations from the 1:1 sex ratio for this species in three successive years.
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Fig. 1 Sketch of the morphology in the dioecious Acer barbinerve in Jiaohe (a male; b female)
Table 1 Equations for calculating biomass in Acre barbinerve in Jiaohe
Symbols
Equations
Equation 1
Flower biomass = number of flowers 9 average dry mass of one flower
Equation 2
Fruit biomass = number of fruits 9 average dry mass of one fruit
Equation 3
Foliage biomass = number of leaves 9 average dry mass of one leaf
Equation 4
New shoot biomass = number of new shoots 9 average dry mass of one new shoot
Results Not all Acer barbinerve shrubs reproduced in 2010, 2011 and 2012. Some shrubs produced flowers and fruits continuously in each of the 3 years, others only reproduced in one or two of the 3 years, while some did not reproduce at all. These three ‘‘reproductive situations’’ may have different resource allocation strategies. The two genders showed different trade-off results at different hierarchical levels. Accordingly, this section presents the results for the intra-annual and inter-annual trade-off at different hierarchical levels in both genders of Acer barbinerve.
Table 2 Results of GLM examination of the intra-annual trade-off between reproductive and vegetative structures at different modular levels in Acer barbinerve in Jiaohe Modular level
Gender
2010
2011
2012
Male
-0.365
-4.665***
-58.473***
Female
-0.018
-0.447***
-21.603***
Shoot Foliage Branch Foliage New Shoots
Male
0.071
0.115***
0.507***
Female
0.001
0.084***
0.415***
Male
0.294
0.436**
Female
0.037
2.027***
Shrub Foliage
Intra-annual trade-off at shoot level New Shoots
The intra-annual trade-off between reproductive structure and foliage biomass was statistically significant at the shoot level in both genders in 2011 and 2012; this trade-off was more pronounced in males than in females. However, the intra-annual trade-off was not significant in either gender in 2010 (Table 2). At the shoot level, females had higher foliage biomass than males in 2010 and 2011, and higher flower biomass in 2011 and 2012 (Fig. 2A, D).
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Male
0.002***
0.002***
0.009***
Female
0.004***
0.001***
0.020***
Male
0.010***
0.047***
Female
0.004***
0.067***
The regression coefficients are the slopes of linear relationships *** p \ 0.001; ** p \ 0.01; * p \ 0.05
Intra-annual trade-off at branch level There was no intra-annual trade-off at branch level in either gender in the three successive years. Foliage biomass was positively correlated with the
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Fig. 2 Comparison of foliage biomass, flower biomass and fruit biomass between males and females in three successive years at different levels in Acer barbinerve in Jiaohe. White indicates female; gray indicates male. Graph A, B, C were about the foliage biomass in both sexes at three different modular level; graph D, E, F were about the flower biomass in both sexes at three different modular level; and
graph G, H, I were about the fruit biomass in female at three different modular level. Letters denote significant differences (p \ 0.05), in multiple comparisons (LSD). The bottom and top of the box indicate the first and third quartiles, and the band inside the box is the median. Data which were not included between the dotted lines were plotted as outliers with small circles
reproductive structure in both genders in 2011 and 2012, and the same result was found for the new shoot biomass in 2012 (Table 2). Males had higher flower biomass and lower foliage biomass than females in 2011, while the inverse was observed in 2012 (Fig. 2E). Males had higher new shoot biomass than females in 2012 at the branch level (Online Resource 1).
Intra-annual trade-off at shrub level There was no intra-annual trade-off in the three successive years at the shrub level. The biomass of both foliage and new shoots were all positively correlated with the reproductive biomass in both genders in the three successive years (Table 2). Although males and females allocated resources differently to reproduction, both had similar
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resource allocation in foliage biomass in each of the 3 years and similar allocations in new shoot growth in 2012 (Fig. 2C, Online Resource 1). Inter-annual trade-off at shoot level An inter-annual reproductive trade-off was not detected in either gender in the three successive years at shoot level (Table 3). Females reduced their resource allocation in fruit biomass over the 3 years (Fig. 2G). Both genders showed a decreased allocation to foliage biomass and flower biomass in the 3 years (Fig. 2D). Males and females showed lower vegetative growth in 2012 at shoot level (Fig. 2A) and higher reproductive biomass in 2010 at shoot level (Fig. 2D, G). Inter-annual trade-off at branch level An inter-annual trade-off was observed during 2011 and 2012 in female shrubs. The female reproductive biomass in 2012 was negatively correlated with the reproductive biomass in 2011 (Table 3). Reproduction fluctuated in both genders, while the amounts of foliage biomass and new shoot biomass were reduced over the 3 years (Fig. 2B, E, H, Online Resource 1). Inter-annual trade-off at shrub level Inter-annual trade-off was barely detected in females in 2010 and 2011 at the shrub level. The reproductive biomass in 2012 was negatively correlated with the reproductive biomass in 2010 and 2011 (Table 3). Both genders had reduced vegetative biomass and reproductive biomass in 2012 at this level (Fig. 2C, F, I, Online Resource 1). Table 3 Results of GLM examination of the inter-annual trade-off in reproductive structures at different modular levels in Acer barbinerve in Jiaohe Modular level Shoot Branch Shrub
Gender
2010
2011
2010 9 2011
Male
10.224
0.530
-6.660
Female
10.224
0.530
-6.660
Male
-1.966
1.694
0.958
Female
-0.106
-0.221*
0.087
Male
-0.110
Female
-0.016**
0.040***
0.000
-0.007***
0.000
The biomass of reproductive structures in 2010 and 2011 was explanatory variables, and the biomass of reproductive structure in 2012 was response variable. 2010 indicates the relation between reproductive biomass of 2010 and 2012; 2011 indicates the relation between reproductive biomass of 2011 and 2012; and 2010 9 2011 indicates the interaction of reproductive biomass in 2010 and 2011 to the reproductive biomass in 2012 *** p \ 0.001; ** p \ 0.01; * p \ 0.05
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Variation in gender ratios and mortality The reproductive status of all Acer barbinerve shrubs was assessed in the study area during the three successive years. The gender ratios were male biased in these 3 years. The number of flowering male shrubs was far greater than the number of flowering and fruit bearing female shrubs in each DBH class and in each year (Table 4). The number of non-reproductive shrubs in each DBH class was highest in 2010 and lowest in 2011 (Table 4). The relatively high number of reproducing individual shrubs in 2011 and 2012 is difficult to explain. Rainfall was much higher than in 2010, but the rainy season usually starts in June, well after the flowering season which starts in early May. Female mortality was higher in the bigger DBH classes than male mortality, but lower in the smaller DBH classes (Fig. 3). Females had higher mortality in the [4 cm DBH in both 2011 and 2012, while the mortality of males was slightly higher than that of females in the 0–2 cm DBH class (Fig. 3). The size-dependent mortality of males, shown in Fig. 3 for 2 years, differs from that of females. Males show a higher mortality in the small DBH classes, but lower mortality than females in the bigger size classes. Larger females are likely to be older ones, and it is possible that the accumulated cost of reproduction during their life span may have affected their survival. Accordingly, we may assume that the greater the number of accumulated fruits produced by a female year after year, the lower is her chance of survival. This observation confirms the findings by Obeso (2002).
Discussion Intra-annual trade-off at different modular levels The intra-annual trade-off between reproduction and vegetative growth which was detected at shoot level confirms the observations by Matsuyama and Sakimoto (2008) who also detected a trade-off at shoot level in Rhus trichocarpa. In our study, this trade-off was considerably reduced, both at branch and whole plant level. This reduction from shoot to whole plant again corroborates Matsuyama and Sakimoto (2008). At the same sampled branch, not every shoot has flowers, or flowers and fruits, in the same year. Some shoots carry only flowers, or flowers and fruits, on a sampled branch, but some shoots do not carry any reproductive organs. Therefore, some nonreproductive shoots may reduce the cost of reproduction at branch level. This appears to be a likely reason for the positive slopes in Table 2. Our findings thus suggest that the autonomy of the different modular levels affects the potential to detect trade-offs between reproduction and vegetative growth (see also Obeso et al. 1998).
Plant Reprod (2015) 28:111–119 Table 4 Number of reproducing shrubs and gender ratios of Acer barbinerve in Jiaohe in three DBH classes during three successive years in the study area
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Year
2010
2011
2012
Gender
DBH classes (cm)
Total
0–2
2–4
[4
Male
168
90
13
271
Female
13
10
2
25
Non-reproduction
325
89
8
422
Male/female
12.9
9.0
6.5
10.8
G(P)
157.40***
73.61***
9.01**
238.94***
Male
311
116
17
444
Female
125
50
4
179
Non-reproduction
47
4
1
52
Male/female
2.5
2.3
4.2
2.5
G(P)
81.95***
26.98***
8.66**
116.39***
Male Female
205 52
79 24
16 2
300 78
G tests were used to analyze deviations from a 1:1 sex ratio
Non-reproduction
158
23
1
182
Male/female
3.9
3.3
8.0
3.9
*** p \ 0.001; ** p \ 0.01; * p \ 0.05
G(P)
97.42***
30.95***
12.40***
139.16***
Fig. 3 Mortality of females (white columns) and males (gray columns) in Acer barbinerve in Jiaohe in three DBH classes in 2011 and 2012
Although both genders showed intra-annual trade-offs between reproduction and vegetative growth at shoot level, the negative correlation between reproduction and vegetative growth was of greater magnitude in the male shrubs (Table 2). Acer barbinerve is a phenophase overlapper, simultaneously producing leaves and flowers, followed by fruiting. When resources from the environment are limited, and if Acer barbinerve would allocate the available resource equally to vegetative growth and reproduction, then the intra-annual trade-off will be easily detected. Wang et al. (2013a, b) did not detect intra-annual tradeoffs between reproduction and vegetative growth in two dioecious Rhamnus species which are phenophase sequencers, where leafing is followed by flowering and fruiting. These phenophase types differ between Rhamnus species and Acer barbinerve which suggests that phenophase types may also affect the detection of trade-off (Matsuyama and Sakimoto 2008). In 2010 and 2011, females allocated more resources to reproduction than males
in Acer barbinerve, while they also had higher foliage biomass than males. It is likely that females have some compensatory mechanisms. For example, Tozawa et al. (2009) suggested that females allocate more biomass to photosynthetic organs and have higher photosynthetic rates than males. Inter-annual trade-off at different modular levels Questions related to inter-annual trade-offs must deal with the effects of reproduction that extend beyond one vegetation period. Our study includes observations collected during three successive years. When females are fruiting, they allocate more resources to reproduction than males. When this happens during several years in succession, the cumulative effect of reproduction may reduce vegetative growth or reproduction or even increase the chance of mortality (Pianka 2000). This cumulative effect of reproduction will not be detected immediately, but probably only after a long period of time, and perhaps only at old age of a plant.
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Males and females showed reduced vegetative growth in 2012 at the three modular levels (Fig. 2A–C). They also showed higher reproductive biomass in 2010 at shoot level and in 2011 at branch and shrub level (Fig. 2D–I). This observation suggests that both males and females experienced an inter-annual trade-off involving previous reproduction and subsequent vegetative growth. The female reproductive biomass in 2012 was negatively correlated with that in 2011 at branch level. This negative correlation was also detected at shrub level (Table 3), which is an indication that the reproductive behavior in previous years affected the reproduction in subsequent years. This presumed delay in the cost of reproduction was only observed on females. Similar findings were also reported for other species (Vaughton and Ramsey 2011; Fox and Stevens 1991; Cipollini and Whigham 1994). Cumulative reproduction and survival of females A number of studies found that gender ratios in dioecious plant populations deviate from the normal ratio of 1:1 (Wheelwright and Bruneau 1992; Morellato 2004; Andrew 2010; Wang et al. 2013a, b). The gender ratio in our study was male biased during the three consecutive years (Table 4). Zhang et al. (2010) found a male-biased gender ratio in Fraxinus mandshurica in old-growth forests in northeastern China. Ortiz et al. (2002) studying Juniperus communis subsp. alpina reported that the gender ratio (male: female) increased significantly with increasing elevation and was significantly male biased above 2600 m. Several authors reported that male-biased gender ratios often occur in stressful environments (Delph 1999; Obeso 2002; Rau´l and Numa 2002; Graff et al. 2013). In our field study, female mortality was found to be higher than that of males in the larger DBH classes (Fig. 3). This may have been caused by the higher accumulated allocation of resources to reproduction in females over their lifetime, an observation that agrees with Lovett and Lovett (1988) and Allen and Antos (1993). Interestingly, such a result may also apply to some animal species. For example, Orell and Belda (2002) found a significant decline in the survival of Parus montanus females after age 5 (see also McCleery et al. 1996). However, results are not always very clear because this is a complex problem involving competition, microsite effects and compensatory mechanisms.
Conclusion The most important result of our study is the finding that the degree of autonomy of the different modular levels
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affects the trade-offs between reproduction and vegetative growth. Although both genders of Acer barbinerve revealed intra-annual trade-offs between reproduction and vegetative growth at shoot level, the negative correlation between reproduction and vegetative growth was greater in males. Females may have compensatory mechanisms which need to be explored in future studies. The high accumulated allocation of resources to reproduction is more obvious in females than in males. Author contribution statement CZ and JW conceived and designed research. YC and XZ conducted experiments. CZ and JW analyzed data. JW and KG wrote the manuscript. All authors read and approved the manuscript. Acknowledgments This work is supported by the 12th five-year National Science and Technology plan of China (2012BAD22B0203), the Program for New Century Excellent Talents in University of Ministry of Education of China (NCET-12-0781), the National Basic Research Program of China (973 Program; 2011CB403203) and the National Natural Science Foundation of China (31200315). Conflict of interest of interest.
The authors declare that they have no conflict
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119 Pianka ER (2000) Evolutionary ecology. Addison-Wesley Longman, San Francisco Rau´l OP, Numa PP (2002) Influence of slope orientation on sex ratio and size distribution in a dioecious plant Bursera fagaroides var. purpusii (Brandeg.) McVaugh and Rzed. (Burseraceae). Plant Ecol 208:271–277. doi:10.1007/s11258-009-9704-2 Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268 Suzuki AA (2005) Reproductive investment in male and female Eurya Japonica (Theaceae) at tree and branch levels. Am J Bot 92(12):2003–2009 Tozawa M, Ueno N, Seiwa K (2009) Compensatory mechanisms for reproductive costs in the dioecious tree Salix integra. Botany 87:315–323. doi:10.1139/B08-125 Vaughton G, Ramsey M (2011) Reproductive allocation and costs in gynodioecious Leucopogon melalieucoides (Ericaceae): implications for the evolution of gender dimorphism. Plant Biol 13:888–895. doi:10.1111/j.1438-8677.2011.00457.x Wang J, Zhang C, Zhao X, Gadow KV (2013a) Limitations to reproductive success in the dioecious tree rhamnus davurica. PLoS ONE 8(12):e81140. doi:10.1371/journal.pone.0081140 Wang J, Zhang CY, Zhao XH, Gadow Kv (2013b) Reproductive allocation of two dioecious Rhamnus species in temperate forests of northeast China. iForest 7:25–32. doi:10.3832/ifor1020-007 Wenk EH, Falster DS (2014) Quantifying and understanding reproductive allocation schedules in plants: a lifetime of decisions. BioRxiv. doi:10.1101/008508 Wheelwright NT, Bruneau A (1992) Population sex ratio and spatial distribution of Ocotea tenera (Lauraceae) trees in a tropical forest. J Ecol 80:425–432 Willson MF (1983) Plant reproductive ecology. Wiley, New York Wu ZY, Raven P (2004) Flora of China. Science Press, Beijing Zhang CY, Zhao XH, Gao LS, Gadow Kv (2010) Gender-related distributions of Fraxinus mandshurica in secondary and oldgrowth forests. Acta Oecol 36:55–62
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ORIGINAL ARTICLE
Reproduction and vegetative growth in the dioecious shrub Acer barbinerve in temperate forests of Northeast China Juan Wang • Chunyu Zhang • Klaus V. Gadow Yanxia Cheng • Xiuhai Zhao
•
Received: 8 October 2014 / Accepted: 19 February 2015 / Published online: 18 March 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Key message Trade-off in dioecious plant. The trade-off between reproduction, vegetative growth and maintenance is a major issue in the life history of an organism and a record of the process which is producing the largest possible number of living offspring by natural selection. Dioecious species afford an excellent opportunity for detecting such possible trade-offs in resource allocation. In this study, we selected the dioecious shrub Acer barbinerve to examine possible trade-offs between reproduction and vegetative growth in both genders at different modular levels during three successive years. Reproductive and vegetative biomass values were assessed during successive years to evaluate their intra-annual and inter-annual trade-offs. These trade-offs were examined at shoot, branch and shrub modular levels in Acer barbinerve shrubs. An intra-annual trade-off was detected at the shoot level for both genders in 2011 and 2012. Both males and females
showed a negative correlation between reproduction and vegetative growth, but this was more prominent in males. For the females of the species, inter-annual trade-offs were only found at branch and shrub levels. Slightly negative correlations in females were detected between the reproduction in 2012 and the reproduction in the two previous years. The gender ratio was significantly male biased during the three successive years of our investigation. Females had higher mortality rates in the larger diameter classes, both in 2011 and 2012. This study revealed a clear trade-off between reproduction and vegetative growth in Acer barbinerve, but results varied between males and females. The degree of autonomy of the different modular levels may affect the ability to detect such trade-offs. Keywords Trade-off Modular level Acer barbinerve Dioecious species
Introduction Communicated by Andrew Stephenson.
Electronic supplementary material The online version of this article (doi:10.1007/s00497-015-0260-8) contains supplementary material, which is available to authorized users. J. Wang C. Zhang Y. Cheng (&) X. Zhao (&) Forest College, Key Laboratory for Forest Resources and Ecosystem Processes of Beijing, Beijing Forestry University, No. 35 Qinghua East Road, Haidian District, Beijing, People’s Republic of China e-mail: [email protected] X. Zhao e-mail: [email protected] K. V. Gadow Faculty of Forestry and Forest Ecology, Georg-AugustUniversity Go¨ttingen, Bu¨sgenweg 5, 37077 Go¨ttingen, Germany
The theory of life history, which records the key events in an organisms’ lifetime, is concerned with the age of sexual maturity, the reproductive lifespan and aging, as well as the number and size of the offspring (Kozlowski and Wiegert 1986). Any organism must allocate resources to vegetative growth, reproduction and survival. These processes depend on the physical and ecological environment of the organism. Available resources are limited; hence, energy used for one function by an individual organism will diminish the energy used for another function (Gadgil and Bossert 1970; Bell 1980; Stearns 1989). Different investments in these functions reflect the various ways of resource allocation in an individual organism to sustain life. The goal of life history theory is to understand the variation in such
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strategies. Given this knowledge, models can be built in order to predict what kinds of traits will be favored in different environments (Wang et al. 2013a, b; Knapp et al. 2001; Hesse and Pannell 2011). The trade-off among reproduction, vegetative growth and maintenance is a key to the life history of an organism. When resources in a particular environment are limited, plants may increase resource allocation to reproduction from their limited reserves, and consequently, the allocation to other functions, such as vegetative growth, maintenance and even future reproduction, is reduced (Willson 1983; Bazzaz et al. 1987). A high vegetative growth rate can increase the possibility of higher reproduction in the future, a typical trade-off which may occur in perennial organisms. The physiological functions will start declining; the higher cost of reproduction may lead to a higher possibility of mortality. This trade-off in an organism not only occurs in the current reproduction season, but also is maintained during its entire lifespan (Wenk and Falster 2014). Dioecious plants, in which the male and female flowers are borne on separate individuals, present an excellent opportunity for detecting such possible trade-offs in resource allocation. In dioecious plants, resource allocation may differ between males and females (Lloyd and Webb 1977). Males promote their mating chances by increasing resource allocation in pollen reproduction and pollinator attractiveness. Females promote the number and quality of offspring by increasing resource allocation in fruit and seed production. The energy requirements for producing fruits and seeds are far greater than for just producing flowers (Lloyd and Webb 1977; Jing and Coley 1990). Consequently, females are likely to allocate more resources to reproduction than males. Biomass allocation to reproduction in three Chamaedorea palms was 3 times higher in female than in male plants (Cepeda-Cornejo and Dirzo 2010). Females in Eurya japonica allocated about 1.6 times more biomass per tree to reproduction than males. At branch level, the biomass of reproduction was 4.4 times higher in females than in males (Suzuki 2005). When the resources, which plants gain from the environment, are limited, the trade-offs in females between reproduction and growth, future reproduction or survival were found to be more pronounced than that in males (Antos and Allen 1990; Delph 1999). However, there are indications that the interpretation of such trade-offs is not always very clear regarding females. Compensatory mechanisms for higher reproductive costs in females have been examined in several studies. Female reproductive organs in Silene latifolia are longer lived and contribute more carbon to their own support than male reproductive structures (Laporte and Delph 1996). Females in Salix integra had greater biomass allocation to
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photosynthetic organs and higher photosynthetic rates than males. Females which had greater reproductive costs did not reduce growth, but increased the carbon uptake ability of different modular units in well-illuminated microenvironments (Tozawa et al. 2009). Females pay a high price for reproduction during their lifetime. They often have lower frequency of reproduction, lower growth rates (especially in woody species) and higher mortality rates and are older at their first reproductive stage than males (Delph 1999; Obeso 2002). Often, the trade-off between reproduction and vegetative growth may be difficult to detect, even in dioecious species. The trade-off may be hidden at higher modular levels but may be more discernable at a lower modular level. The degree of autonomy of the different plant organs might be an important reason for this (Obeso et al. 1998). For example, if branches are autonomous, the resource allocation may show a small-scale balance between reproduction and vegetative growth at branch level. But the cost of reproduction may be compensated by non-reproductive branches at shrub level. The trade-off can only be detected at branch level but not at shrub level. Conversely, if branches are partially autonomous, the resources for reproduction will be translated among branches. The tradeoff will be just detected at shrub level but not at branch level. Matsuyama and Sakimoto (2008) identified a tradeoff between reproduction and vegetative growth at shoot level, while this trade-off disappeared at the whole shrub level. Therefore, our objective in this study is to determine the trade-offs at different modular levels. The dioecious shrub Acer barbinerve was chosen as a convenient species because it is a shrub that can be studied at several such modular levels. Moreover, it is a perennial which allows for the study of the cost of reproduction on future growth and reproduction during three successive years. We hypothesize that there is a trade-off between reproduction and vegetative growth in this particular species. If such a trade-off exists, then we want to know whether it exists within the same year (intra-annually) and/ or between different years (inter-annually) and whether there are differences in the trade-off between the two genders. Finally, we want to know whether the modular level (shoot, branch or shrub) has an effect on detecting possible trade-offs.
Materials and methods Study site and species Our study was conducted at the Jiaohe forest in Jilin province, northeastern China (43°580 N, 127°430 E; elevation 450 m a.s.l.), within a temperate continental mountain
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climate zone. The average annual temperature is 3.8 °C. The hottest month is July with an average day temperature of 21.7 °C; the coldest month is January with an average day temperature of -18.6 °C. The average annual precipitation is 695.9 mm. The soils are dark brown forest soils varying in depth between 20 and 100 cm. The forest type is a mixed broadleaf–conifer forest (Wang et al. 2013a, b). An experimental field plot, covering an area of 11.52 ha (320 m 9 360 m), was established in 2009. The main coniferous species in the plot are Picea jezoensis, Pinus koraiensis and Abies nephrolepis. The dominant deciduous species are Fraxinus mandshurica and so on. The studied species is Acer barbinerve which is quite common in the plot. Acer barbinerve is a perennial dioecious shrub or small multi-stemmed shrub which occurs in Korea, Russia and northeastern China. The life span of Acer barbinerve is about 10 years. The flowering season is in May, and the fruit season is from June to July. Acer barbinerve is a phenophase overlapper, simultaneously producing leaves and flowers, followed by fruiting. The leaves are deciduous. The inflorescence is racemose which contains 5–7 flowers. Every single male flower has four petals and four stamens, while a single female flower has four petals and one stigma. The infructescence contains 5–7 samaras (Wu and Raven 2004). Measurements The number of reproductive male and female trees were different in the three successive years, involving 25 females and 50 males in 2010, 100 females and 100 males in 2011, and 78 females and 100 males in 2012. This study is concerned with the trade-off between reproduction and vegetative growth at four modular levels, i.e., shoot, branch, shrub as well as population. Under field conditions, the different positions of the tree crown may be subjected to slightly different micro climates, causing different biomass allocations in the different horizontal sections of the crown. Thus, five to ten reproductive branches from every single shrub were randomly selected in four crown compartments, i.e., four horizontal sections, following Henriksson (2001). Each sampled reproductive branch is made up of several shoots. A shoot includes leaves, flowers or fruits (Fig. 1). At shoot level, the flowers (male and female) and leaves of all shoots on the sampled branches were counted in May (flowering season), while fruits were counted in July (fruiting season). At branch level, the number of flowers, leaves, new shoots and fruits from all selected branches in the sample shrubs were assessed. At shrub level, the branches were counted in every sampled shrub. The number of branches was multiplied by the mean number of flowers, leaves and fruits of sampled branches
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on each shrub. This approach produced an estimate of the number of flowers, leaves and fruits on every single flowering shrub. One reproductive branch was taken from every single sample shrub for estimating the biomass of flowers, new shoots and leaves. At least ten fruits were taken from every single shrub for estimating the fruit biomass. Every sampled shrub had its individual flower, leaf and fruit biomass. All harvested branches and fruits were weighed after oven drying at 80 °C for 2 days. The numbers of leaves, new shoots, flowers and fruits at each modular level were multiplied by the mean biomass of leaves, new shoots, flowers and fruits to estimate the biomass of leaves, new shoots, flowers and fruits for every sampled shrub at each modular level. The biomass of flowers and fruits represented the reproductive growth; the biomass of leaves and new shoots represented the vegetative growth. The equations used to calculate the biomass of flowers, fruits, foliage and new shoots at shoot, branch and shrub level are presented in Table 1. At population level, we investigated the numbers of all flowering shrubs in the plot during each of the three successive years. The numbers of flowering female, male and non-reproductive shrubs were recorded for every year and used to estimate the sex ratio in the successive years. The diameter at breast height (DBH) of all shrubs was measured at the beginning of the growing season in each year. If the shrubs were multi-stemmed, the diameter at breast height (DBH) of each stem was measured. Statistical analysis A general linear model (GLM) was used to examine the trade-off between reproductive and vegetative structures at shoot, branch and shrub levels, both within the same year (intra-annually) and between different years (inter-annually), using the R statistical software. In the GLM examination of the intra-annual trade-off, the vegetative biomass values represented the explanatory variables, the reproductive biomass was the response variable. The reproductive biomass was the biomass of flowers in male and the biomass of flowers and fruits in female. In the GLM examination of the inter-annual trade-off, the reproductive biomass in 2010 and 2011 were the explanatory variables, while the reproductive biomass in 2012 was the response variable. The reproductive biomass included the biomass of flowers in males and the biomass of flowers and fruits in females. Shrubs were grouped into diameter at breast height (DBH) classes, and the sex ratio was determined for each DBH class and each year during the study period. The likelihood-ratio test was used to test whether two observed frequency distributions belong to the same theoretical distribution. This test was used to detect deviations from the 1:1 sex ratio for this species in three successive years.
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Fig. 1 Sketch of the morphology in the dioecious Acer barbinerve in Jiaohe (a male; b female)
Table 1 Equations for calculating biomass in Acre barbinerve in Jiaohe
Symbols
Equations
Equation 1
Flower biomass = number of flowers 9 average dry mass of one flower
Equation 2
Fruit biomass = number of fruits 9 average dry mass of one fruit
Equation 3
Foliage biomass = number of leaves 9 average dry mass of one leaf
Equation 4
New shoot biomass = number of new shoots 9 average dry mass of one new shoot
Results Not all Acer barbinerve shrubs reproduced in 2010, 2011 and 2012. Some shrubs produced flowers and fruits continuously in each of the 3 years, others only reproduced in one or two of the 3 years, while some did not reproduce at all. These three ‘‘reproductive situations’’ may have different resource allocation strategies. The two genders showed different trade-off results at different hierarchical levels. Accordingly, this section presents the results for the intra-annual and inter-annual trade-off at different hierarchical levels in both genders of Acer barbinerve.
Table 2 Results of GLM examination of the intra-annual trade-off between reproductive and vegetative structures at different modular levels in Acer barbinerve in Jiaohe Modular level
Gender
2010
2011
2012
Male
-0.365
-4.665***
-58.473***
Female
-0.018
-0.447***
-21.603***
Shoot Foliage Branch Foliage New Shoots
Male
0.071
0.115***
0.507***
Female
0.001
0.084***
0.415***
Male
0.294
0.436**
Female
0.037
2.027***
Shrub Foliage
Intra-annual trade-off at shoot level New Shoots
The intra-annual trade-off between reproductive structure and foliage biomass was statistically significant at the shoot level in both genders in 2011 and 2012; this trade-off was more pronounced in males than in females. However, the intra-annual trade-off was not significant in either gender in 2010 (Table 2). At the shoot level, females had higher foliage biomass than males in 2010 and 2011, and higher flower biomass in 2011 and 2012 (Fig. 2A, D).
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Male
0.002***
0.002***
0.009***
Female
0.004***
0.001***
0.020***
Male
0.010***
0.047***
Female
0.004***
0.067***
The regression coefficients are the slopes of linear relationships *** p \ 0.001; ** p \ 0.01; * p \ 0.05
Intra-annual trade-off at branch level There was no intra-annual trade-off at branch level in either gender in the three successive years. Foliage biomass was positively correlated with the
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Fig. 2 Comparison of foliage biomass, flower biomass and fruit biomass between males and females in three successive years at different levels in Acer barbinerve in Jiaohe. White indicates female; gray indicates male. Graph A, B, C were about the foliage biomass in both sexes at three different modular level; graph D, E, F were about the flower biomass in both sexes at three different modular level; and
graph G, H, I were about the fruit biomass in female at three different modular level. Letters denote significant differences (p \ 0.05), in multiple comparisons (LSD). The bottom and top of the box indicate the first and third quartiles, and the band inside the box is the median. Data which were not included between the dotted lines were plotted as outliers with small circles
reproductive structure in both genders in 2011 and 2012, and the same result was found for the new shoot biomass in 2012 (Table 2). Males had higher flower biomass and lower foliage biomass than females in 2011, while the inverse was observed in 2012 (Fig. 2E). Males had higher new shoot biomass than females in 2012 at the branch level (Online Resource 1).
Intra-annual trade-off at shrub level There was no intra-annual trade-off in the three successive years at the shrub level. The biomass of both foliage and new shoots were all positively correlated with the reproductive biomass in both genders in the three successive years (Table 2). Although males and females allocated resources differently to reproduction, both had similar
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resource allocation in foliage biomass in each of the 3 years and similar allocations in new shoot growth in 2012 (Fig. 2C, Online Resource 1). Inter-annual trade-off at shoot level An inter-annual reproductive trade-off was not detected in either gender in the three successive years at shoot level (Table 3). Females reduced their resource allocation in fruit biomass over the 3 years (Fig. 2G). Both genders showed a decreased allocation to foliage biomass and flower biomass in the 3 years (Fig. 2D). Males and females showed lower vegetative growth in 2012 at shoot level (Fig. 2A) and higher reproductive biomass in 2010 at shoot level (Fig. 2D, G). Inter-annual trade-off at branch level An inter-annual trade-off was observed during 2011 and 2012 in female shrubs. The female reproductive biomass in 2012 was negatively correlated with the reproductive biomass in 2011 (Table 3). Reproduction fluctuated in both genders, while the amounts of foliage biomass and new shoot biomass were reduced over the 3 years (Fig. 2B, E, H, Online Resource 1). Inter-annual trade-off at shrub level Inter-annual trade-off was barely detected in females in 2010 and 2011 at the shrub level. The reproductive biomass in 2012 was negatively correlated with the reproductive biomass in 2010 and 2011 (Table 3). Both genders had reduced vegetative biomass and reproductive biomass in 2012 at this level (Fig. 2C, F, I, Online Resource 1). Table 3 Results of GLM examination of the inter-annual trade-off in reproductive structures at different modular levels in Acer barbinerve in Jiaohe Modular level Shoot Branch Shrub
Gender
2010
2011
2010 9 2011
Male
10.224
0.530
-6.660
Female
10.224
0.530
-6.660
Male
-1.966
1.694
0.958
Female
-0.106
-0.221*
0.087
Male
-0.110
Female
-0.016**
0.040***
0.000
-0.007***
0.000
The biomass of reproductive structures in 2010 and 2011 was explanatory variables, and the biomass of reproductive structure in 2012 was response variable. 2010 indicates the relation between reproductive biomass of 2010 and 2012; 2011 indicates the relation between reproductive biomass of 2011 and 2012; and 2010 9 2011 indicates the interaction of reproductive biomass in 2010 and 2011 to the reproductive biomass in 2012 *** p \ 0.001; ** p \ 0.01; * p \ 0.05
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Variation in gender ratios and mortality The reproductive status of all Acer barbinerve shrubs was assessed in the study area during the three successive years. The gender ratios were male biased in these 3 years. The number of flowering male shrubs was far greater than the number of flowering and fruit bearing female shrubs in each DBH class and in each year (Table 4). The number of non-reproductive shrubs in each DBH class was highest in 2010 and lowest in 2011 (Table 4). The relatively high number of reproducing individual shrubs in 2011 and 2012 is difficult to explain. Rainfall was much higher than in 2010, but the rainy season usually starts in June, well after the flowering season which starts in early May. Female mortality was higher in the bigger DBH classes than male mortality, but lower in the smaller DBH classes (Fig. 3). Females had higher mortality in the [4 cm DBH in both 2011 and 2012, while the mortality of males was slightly higher than that of females in the 0–2 cm DBH class (Fig. 3). The size-dependent mortality of males, shown in Fig. 3 for 2 years, differs from that of females. Males show a higher mortality in the small DBH classes, but lower mortality than females in the bigger size classes. Larger females are likely to be older ones, and it is possible that the accumulated cost of reproduction during their life span may have affected their survival. Accordingly, we may assume that the greater the number of accumulated fruits produced by a female year after year, the lower is her chance of survival. This observation confirms the findings by Obeso (2002).
Discussion Intra-annual trade-off at different modular levels The intra-annual trade-off between reproduction and vegetative growth which was detected at shoot level confirms the observations by Matsuyama and Sakimoto (2008) who also detected a trade-off at shoot level in Rhus trichocarpa. In our study, this trade-off was considerably reduced, both at branch and whole plant level. This reduction from shoot to whole plant again corroborates Matsuyama and Sakimoto (2008). At the same sampled branch, not every shoot has flowers, or flowers and fruits, in the same year. Some shoots carry only flowers, or flowers and fruits, on a sampled branch, but some shoots do not carry any reproductive organs. Therefore, some nonreproductive shoots may reduce the cost of reproduction at branch level. This appears to be a likely reason for the positive slopes in Table 2. Our findings thus suggest that the autonomy of the different modular levels affects the potential to detect trade-offs between reproduction and vegetative growth (see also Obeso et al. 1998).
Plant Reprod (2015) 28:111–119 Table 4 Number of reproducing shrubs and gender ratios of Acer barbinerve in Jiaohe in three DBH classes during three successive years in the study area
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Year
2010
2011
2012
Gender
DBH classes (cm)
Total
0–2
2–4
[4
Male
168
90
13
271
Female
13
10
2
25
Non-reproduction
325
89
8
422
Male/female
12.9
9.0
6.5
10.8
G(P)
157.40***
73.61***
9.01**
238.94***
Male
311
116
17
444
Female
125
50
4
179
Non-reproduction
47
4
1
52
Male/female
2.5
2.3
4.2
2.5
G(P)
81.95***
26.98***
8.66**
116.39***
Male Female
205 52
79 24
16 2
300 78
G tests were used to analyze deviations from a 1:1 sex ratio
Non-reproduction
158
23
1
182
Male/female
3.9
3.3
8.0
3.9
*** p \ 0.001; ** p \ 0.01; * p \ 0.05
G(P)
97.42***
30.95***
12.40***
139.16***
Fig. 3 Mortality of females (white columns) and males (gray columns) in Acer barbinerve in Jiaohe in three DBH classes in 2011 and 2012
Although both genders showed intra-annual trade-offs between reproduction and vegetative growth at shoot level, the negative correlation between reproduction and vegetative growth was of greater magnitude in the male shrubs (Table 2). Acer barbinerve is a phenophase overlapper, simultaneously producing leaves and flowers, followed by fruiting. When resources from the environment are limited, and if Acer barbinerve would allocate the available resource equally to vegetative growth and reproduction, then the intra-annual trade-off will be easily detected. Wang et al. (2013a, b) did not detect intra-annual tradeoffs between reproduction and vegetative growth in two dioecious Rhamnus species which are phenophase sequencers, where leafing is followed by flowering and fruiting. These phenophase types differ between Rhamnus species and Acer barbinerve which suggests that phenophase types may also affect the detection of trade-off (Matsuyama and Sakimoto 2008). In 2010 and 2011, females allocated more resources to reproduction than males
in Acer barbinerve, while they also had higher foliage biomass than males. It is likely that females have some compensatory mechanisms. For example, Tozawa et al. (2009) suggested that females allocate more biomass to photosynthetic organs and have higher photosynthetic rates than males. Inter-annual trade-off at different modular levels Questions related to inter-annual trade-offs must deal with the effects of reproduction that extend beyond one vegetation period. Our study includes observations collected during three successive years. When females are fruiting, they allocate more resources to reproduction than males. When this happens during several years in succession, the cumulative effect of reproduction may reduce vegetative growth or reproduction or even increase the chance of mortality (Pianka 2000). This cumulative effect of reproduction will not be detected immediately, but probably only after a long period of time, and perhaps only at old age of a plant.
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Males and females showed reduced vegetative growth in 2012 at the three modular levels (Fig. 2A–C). They also showed higher reproductive biomass in 2010 at shoot level and in 2011 at branch and shrub level (Fig. 2D–I). This observation suggests that both males and females experienced an inter-annual trade-off involving previous reproduction and subsequent vegetative growth. The female reproductive biomass in 2012 was negatively correlated with that in 2011 at branch level. This negative correlation was also detected at shrub level (Table 3), which is an indication that the reproductive behavior in previous years affected the reproduction in subsequent years. This presumed delay in the cost of reproduction was only observed on females. Similar findings were also reported for other species (Vaughton and Ramsey 2011; Fox and Stevens 1991; Cipollini and Whigham 1994). Cumulative reproduction and survival of females A number of studies found that gender ratios in dioecious plant populations deviate from the normal ratio of 1:1 (Wheelwright and Bruneau 1992; Morellato 2004; Andrew 2010; Wang et al. 2013a, b). The gender ratio in our study was male biased during the three consecutive years (Table 4). Zhang et al. (2010) found a male-biased gender ratio in Fraxinus mandshurica in old-growth forests in northeastern China. Ortiz et al. (2002) studying Juniperus communis subsp. alpina reported that the gender ratio (male: female) increased significantly with increasing elevation and was significantly male biased above 2600 m. Several authors reported that male-biased gender ratios often occur in stressful environments (Delph 1999; Obeso 2002; Rau´l and Numa 2002; Graff et al. 2013). In our field study, female mortality was found to be higher than that of males in the larger DBH classes (Fig. 3). This may have been caused by the higher accumulated allocation of resources to reproduction in females over their lifetime, an observation that agrees with Lovett and Lovett (1988) and Allen and Antos (1993). Interestingly, such a result may also apply to some animal species. For example, Orell and Belda (2002) found a significant decline in the survival of Parus montanus females after age 5 (see also McCleery et al. 1996). However, results are not always very clear because this is a complex problem involving competition, microsite effects and compensatory mechanisms.
Conclusion The most important result of our study is the finding that the degree of autonomy of the different modular levels
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affects the trade-offs between reproduction and vegetative growth. Although both genders of Acer barbinerve revealed intra-annual trade-offs between reproduction and vegetative growth at shoot level, the negative correlation between reproduction and vegetative growth was greater in males. Females may have compensatory mechanisms which need to be explored in future studies. The high accumulated allocation of resources to reproduction is more obvious in females than in males. Author contribution statement CZ and JW conceived and designed research. YC and XZ conducted experiments. CZ and JW analyzed data. JW and KG wrote the manuscript. All authors read and approved the manuscript. Acknowledgments This work is supported by the 12th five-year National Science and Technology plan of China (2012BAD22B0203), the Program for New Century Excellent Talents in University of Ministry of Education of China (NCET-12-0781), the National Basic Research Program of China (973 Program; 2011CB403203) and the National Natural Science Foundation of China (31200315). Conflict of interest of interest.
The authors declare that they have no conflict
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