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DO LEAF FUNCTIONAL TRAITS DIFFER BETWEEN 20-35-YEAR-OLD TRANSPLANTED AND WILD SOURCE POPULATIONS? A CASE STUDY INVOLVING FIVE ENDANGERED TREE SPECIES
Shitong Wang12 3, Yaozhan Xu12 3, Xinzeng Wei12 3 * , Mingxi Jiang12 3
1 Wuhan Botanical Garden, Chinese Academy of Sciences, China 2Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, China 3University of Chinese Academy of Sciences, China *e-mail: [email protected]
Received: 22.11.2021. Revised: 21.03.2022. Accepted: 28.03.2022.
Conservation of threatened species through translocation has become an effective way to combat species extinction worldwide. Plant functional traits are good predictors of plant performance and can reflect the adaptation strategies of plants to the environment. However, it is still unclear whether transplanted populations have comparable levels of leaf functional traits to their wild source populations. To assess the effectiveness of conservation-based translocation of long-living endangered tree species, we investigated the long-term (20-35 years) population dynamics of five co-existing endangered tree species (Davidia involucrata, Dipteronia sinensis, Pterostyrax psilophyllus, Tapiscia sinensis, and Tetracentron sinense) in transplanted populations, and compared the leaf functional traits between the transplanted and their wild source populations. We found that the survival rates of the five species in the transplanted populations ranged from 42.86% to 73.81%, and most of these species could blossom and yield fruit. All species had significant differences in some leaf functional traits between transplanted and wild populations. The intraspecific traits variation of some species in the transplanted populations was decreased compared with that in the wild populations on the whole. We conclude that after a long period of translocation, these species in transplanted populations were able to grow normally and most species become more efficient in resource acquisition or utilisation and more resources were available for growth. However, the intraspecific traits variation of some species in transplanted populations may lead to competitive exclusion, affect species coexistence, and thus affect their performance.
Key words: conservation-based translocation, intraspecific trait variation, long-living tree species, long-term monitoring, population dynamics
Introduction
The rate of extinction caused by human activities is approximately 1000 times the rate of environmental background extinction, and the rate of extinction will continue to rise in the future (Dirzo & Raven, 2003; Pimm et al., 2014). At present, approximately 20% of plants are at risk of extinction, and since plants are crucial to the maintenance of ecological processes and the survival of life (Newton, 2008), the conservation of plants becomes extremely urgent. Conservation of threatened species by transplanting them to new, safe locations has become an effective way to address the worldwide extinction of endangered plant species (Havens et al., 2006; Mounce et al., 2017), and now, it may be a major approach for ensuring their long-term survival (Oldfield, 2009).
However, when plants were transplanted to a new habitat, they may exhibit maladaptation due to the change in selection pressure, such
as climate, soil, and competition (e.g. Ensslin et al., 2015; Cho et al., 2019). Therefore, long-term monitoring of the transplanted population is needed. One criterion for the success of translocation is the formation of a self-sustaining and self-renewing population (Griffith et al., 1989; Reiter et al., 2016). So, we need to monitor the population dynamics and life history of transplanted populations, such as survival and reproduction, to evaluate the effectiveness of translocation (Ren et al., 2016; Izuddin et al., 2018). Current studies about the population monitoring are mainly focusing on herbs or shrubs with relatively short growth cycles (Wendelberger et al., 2008; Gomes et al., 2018), but monitoring the long-term population dynamics of trees species under transplanted conservation are still scarce.
Plant functional traits are a series of physiological and ecological indicators closely related to their survival, growth and reproduction (Ackerly, 2004; Violle et al., 2007), and they are
useful predictors of plant performance (Westo-by et al., 2002; Poorter & Bongers, 2006). For instance, species with high traits value of specific leaf area (SLA) and leaf nitrogen content (LNC), tend to have higher individual growth and fecundity (Adler et al., 2014). When transplanted to a new habitat, plants may cope with the changes through the plasticity of leaf functional traits (Agrawal, 2001; Zhu et al., 2020). Therefore, comparison of leaf functional traits between transplanted and wild collections may useful to reflect the plant performance and adaptation strategies on the translocation site.
Intraspecific trait variation is a major component of biodiversity (Mimura et al., 2017). Populations with higher trait variation are more stable and better able to adapt to rapid changes in the environment (Albert et al., 2011). A study on intraspecific trait variation of invasive species showed that the higher variation of intraspecific traits was related to the stronger resource utilisation ability (Heberling et al., 2016). Therefore, it is useful to determine whether transplanted populations harbour similar levels of intraspecific trait variation to their wild source populations. However, current studies about the comparison of phenotypic traits between transplanted and wild populations have mainly focused on herbs with relatively short growth cycles (Cho et al., 2019; Rauschkolb et al., 2019; Ensslin & Gode-froid, 2020), studies on long-living tree species are still scarce (Li et al., 2012).
Since the 1980s, the Jiugongshan National Nature Reserve has undertaken the conservation-based translocation of endangered plants within and around central China (Wang et al., 1988; Ye et al., 2000). More than 30 endangered species have been transplanted here for conservation. In this study, we investigated the population dynamics of five dominant endangered tree species (Davidia involucrata Baill., Dip-teronia sinensis Oliv., Pterostyrax psilophyllus Diels ex Perkins, Tapiscia sinensis Oliv., and Tetracentron sinense Oliv.) approximately 2035 years after their establishment on the translocation site, and compared leaf functional traits between transplanted and wild populations, to assess the conservation effectiveness of long-living endangered tree species. Specifically, we put forth the following questions: 1) What are the survival and reproductive statuses of the five endangered tree species after 20-35 years of translocation? 2) Do leaf functional traits dif-
fer between transplanted and wild source populations of the five endangered tree species after a long-term translocation?
Material and Methods
Study sites
This study was carried out at the Houhe National Nature Reserve (Wild site; 30.071833° N, 110.542753° E) and the Jiugongshan National Nature Reserve (Translocation site; 29.364911° N, 114.568081° E) (Fig. 1). The two regions have similar climates, with a subtropical monsoon climate. The mean annual temperature and precipitation of these two sites are 11.5 °C and 1776 mm, and 10 °C and 1512 mm, respectively (Table 1).
The Houhe National Nature Reserve is located in Wufeng Tujia Autonomous County, in the southwest of Hubei Province, China. There exists a special type of plant community, in which a variety of ancient, relict, and endangered plants naturally grow together. These endangered species have survived from a long-term natural selection, in addition to the unique environmental conditions; the overall advantage of the special community composition may also be an important reason. Inspired by this, Ye et al. (2000) proposed the idea of simulating plant communities to protect endangered plants at translocation sites, and put it into practice in Jiugongshan National Nature Reserve.
The Jiugongshan National Nature Reserve is located in Tongshan County, in the southeast of Hubei Province, China. The conservation-based translocation of endangered species has been carried out here since 1986. Seedlings of endangered species were first transplanted in 1986 and again in 1997. A total of 35 species of endangered plants are preserved there, covering an area of 3000 m2. The species distribution pattern was referenced to the community at the wild site, and the plant arrangement and density in transplantation sites was designed according to the actual distribution status in the wild site. The five endangered tree species often appeared in the same community as dominant species or co-dominant species, according to the number of individuals of each species in the wild community, we designed the transplant number of each species ranged from 20 to 70. The total density of trees in the wild community was 0.22 trees/m2, so the plant row spacing was designed 2-4 m in transplanted site (Ye et al., 2000).
Fig. 1. Location of the two study sites, namely Houhe National Nature Reserve (HH), Jiugongshan National Nature Reserve (JGS), China.
Table 1. Climate and soil condition of the two study sites
Site Population MAT (°C)* MAP (mm)* Soil C (mg/g) Soil N (mg/g) Soil P (mg/g) Soil C:N
Houhe Wild 10.0 1512 97.34 ± 52.04a 7.55 ± 3.16a 0.70 ± 0.19a 9.26 ± 1.78a
Jiugongshan Transplanted 11.5 1776 69.41 ± 7.48a 6.46 ± 0.63a 0.59 ± 0.06a 10.71 ± 0.19a
Note: * - Climate data were obtained from the global climate database (WorldClim, http://www.worldclim.org/). The same lowercase letter (a) indicates that there was no significant difference in soil element content between the two study sites.
Study species
We selected five endangered species in the community as the study subjects, namely Davidia involucrata, Dipteronia sinensis, Pterostyrax psilo-phyllus, Tapiscia sinensis, and Tetracentron sinense (Table 2). All these five species are deciduous trees or small trees that are endemic to China or East Asia. Among them, Davidia involucrata, T. sinensis, and T. sinense are tertiary relict species. The five species are mainly distributed in moist evergreen deciduous broad-leaved mixed forests or evergreen broad-leaved forests in the subtropical mountains. The main threats to these species are human disturbance or poor natural regeneration, or both. At present, D. involucrata and T. sinense are classified as national key protected wild plants in China. Pterostyrax psilophyllus and D. sinensis are listed as vulnerable and rare species, respectively, according to the China Plant Red Data Book (Fu & Jin, 1992).
original records of retired colleagues and our field investigations. Data between 1987 and 2001 were obtained from previous records, except that the data for the year 2000 were missing. Data in 2017 were obtained by field investigation, while the data from 2002 to 2016 were missing or incomplete. Finally, we obtained fifteen survey datasets for Davidia involucrata, Pterostyrax psilophyllus, Tapiscia sinensis and Tetracentron sinense with a span of 31 years and five survey datasets for Dipteronia sinensis with a span of 21 years. From June 2017 to August 2018, we investigated the number of survivors and the flowering, fruiting, and regeneration statuses of the five endangered tree species in transplanted populations. The survival rate is the ratio of the current survival number to the original cultivated number of each species. The current survival number was recorded during the field investigation in 2017 and the original cultivated number were obtained from previous records.
Population survey and data collection
We collated the population dynamics data during the period of translocation conservation from the
Sample collection and trait measurements
In August 2018, leaf and soil samples were collected in both the transplanted and wild popula-
tions. Five individuals of each species were randomly selected from both transplanted and wild populations (Table 2). Thirty healthy, intact and fully matured leaves were collected from the sun-exposed branches of each individual. The positions (i.e. aspect and height) of the sampled leaves are similar for transplanted and wild populations. In order to avoid the decrease of leaf fresh mass during the daytime by the vigorous transpiration, all leaf samples were collected in the morning. Finally, we collected a total of 1500 leaf samples from 50 individuals from the transplanted and wild populations. Leaf fresh masses were measured in the field, and then leaf samples were stored separately and immediately brought back to the laboratory. Soil sample collections were performed using a five-point sampling method, and the surface soil (0-30 cm) was collected after the removal of litter. As the five species grow together in both the transplanted and wild populations, three soil samples were randomly taken from each site and returned to the laboratory.
Leaf samples were scanned separately using a colour image scanner (CanoScan LiDE 110), and the images were used to measure the leaf length, width and leaf area. Then they were placed in an oven, dried at 60 °C to a constant weight, and used for the measurement of the leaf dry mass. Soil samples were air-dried to a constant weight. All samples were ground and sieved through a 100-mesh sieve to determine the element content of nitrogen and phosphorus.
The fresh and dry masses of leaf samples were determined with an electronic balance that was accurate to 0.001 g. The leaf area was measured by using «Digimizer» (https://www.digimizer.com/). The SLA was calculated as the one-sided leaf area per leaf dry mass, expressed as m2 x kg-1. The leaf dry matter content (LDMC) was calculated as the ratio of the leaf dry mass to the leaf fresh mass, expressed as mg x g-1. LNC, soil C and soil N were measured with an elemental analyser (Vario EL
cube), and leaf phosphorus content (LPC) and soil P were measured via the molybdenum-antimony anti-spectrophotometric method (UV-755B).
Data analysis
An independent-samples t-test was used to compare the mean values of leaf functional traits between transplanted and wild populations. All data were LN- or SQRT-transformed to satisfy the normality and homogeneity of residuals. Data analysis and mapping were performed using SPSS 21.0 (IBM, Armonk, NY, USA) and Origin 8.5 (OriginLab, Northampton, USA).
Results
Soilfactors
There was no significant difference in soil C, N and P contents between the wild and translocation site (p > 0.05). The range of soil C and N contents of the wild site is higher than on the transplanted site, but there was no significant difference in Soil C:N ratio between wild and transplanted site (p > 0.05) (Table 1).
Population dynamics and reproductive status
From 1987 to 2017, the overall population dynamics of the five endangered species at the translocation site fluctuated in the early stages of transplantation, then decreased and gradually became stable in the later stage (Fig. 2). However, the population of Tetracentron sinense declined only after the second planting, while it increased during the first five years after the first planting, caused by continuous artificial replant.
The final survival rates of the five species on the translocation site ranged from 42.86% to 73.81%. All surviving individuals could grow normally. Apart from Tetracentron sinense, blooming and fruiting have been observed in all the other four species. In addition, Pterosty-rax psilophyllus seedlings were observed near its large trees (Table 2).
Table 2. Characteristics, survival rate (transplanted population), and sample size of the five endangered species
Species Family Endangered Endemic Reproductive Survival rate Sample size
category status (%) Wild Transplanted
Davidia involucrata Nyssaceae Rare China Flower and fruit 42.86 5 5
Dipteronia sinensis Aceraceae Rare China Flower and fruit 73.81 5 5
Pterostyrax psilophyllus Styracaceae Vulnerable East Asia Flower, fruit and seedling 56.25 55
Tapiscia sinensis Staphyleaceae Rare China Flower and fruit 67.67 55
Tetracentron sinense Tetracentraceae Rare East Asia Vegetative growth 55.56 55
70
60
^ 50 о
a
I40'
.a
3 30
>
20 10 0
—•—D. involucrata
—•— D. sinensis
—•— P. psilophyllus
—•— T. sinensis
—*— T. sinense
^ л -—_
1 1 1 1 1 1 1
1985 1990 1995 2000 2005 2010 2015 Year
2020
Fig. 2. Population dynamics of the five endangered tree species in transplanted populations from 1987 to 2017.
Leaf functional traits
We found that all species had significant differences in some leaf functional traits between transplanted and wild populations (Fig. 3). Dip-teronia sinensis showed a significantly lower SLA (p < 0.05) but significantly higher LDMC (p < 0.01) in the transplanted population, while both Ptero-styrax psilophyllus and Tapiscia sinensis had a significantly higher SLA (p < 0.05) in transplanted populations. Davidia involucrata and Tetracentron sinense had significantly higher LNC (p < 0.05) and LPC (p < 0.01 or p < 0.05) in transplanted populations than in the wild populations. Compared with the wild population, the LNC and/or LPC values of the five species were all changed significantly in the transplanted population (p < 0.01 or p < 0.05). However, there was no significant difference in leaf N:P (p > 0.05) between transplanted and wild populations except T. sinensis (p < 0.01). There was no significant difference in leaf area between the transplanted and wild populations (p > 0.05) either.
Intraspecific trait variation
We found the changes in intraspecific trait variation between wild and transplanted populations were different among species. The trait CV-values of the five tree species were ranged from 0.49% to 12.79% in the transplanted population and 0.98% to 13.95% in the wild populations. Intraspecific traits variation of Davidia involucrata and Pterostyrax psilophyl-lus in the transplanted populations was similar or decreased compared with that in the wild populations. Compared with wild populations, Dipteronia sinensis and Tapiscia sinensis showed higher CV-values only in LPC and leaf N:P, and Tetracentron sinense showed higher CV-values in leaf area, SLA and LDMC in the transplanted populations (Fig. 4).
Fig. 3. Mean values (± SE) of leaf functional traits of the five endangered tree species in the transplanted and wild populations. Designations: SLA - specific leaf area; LDMC -leaf dry matter content; LNC - leaf nitrogen content; LPN -leaf phosphorus content; p-value designations: * -p < 0.05; ** -p < 0.01; n.s. - not significant.
[I I Wild 1Ш Transplanted)
1
(b) L | Wild | Transplanted]
Ir, i irl
(e) Il I Wild
Transplanted)
i
a
to
j Wild
И Transplanted)
D. involúcrala D. sinensis P. psilophyllus T. sinensis T. si
y Hi m m
D. involucrata D. sinensis P. psilophyllus T. sinensis T. sinense
Fig. 4. Coefficients of variation of the functional traits of the five endangered tree species in the transplanted and wild populations. Designations: SLA - specific leaf area; LDMC -leaf dry matter content; LNC - leaf nitrogen content; LPN -leaf phosphorus content; CV - coefficient of variation.
Discussion
Population dynamics and reproductive statuses
A high survival rate is important for species to become established and persist in new environments (Wendelberger et al., 2008; Gomes et al., 2018). According to the standard of Roman-Danobeytia et al. (2012), the survival rate of Da-vidia involucrata (42.86%) can be classified as «moderate» (26-50%), and the other four species (56.25-73.81%) can be classified as «good» (5175%). The relatively high survival rates observed in our study can be explained by the climate similarity theory (Mayr, 1906) because the two sites are both located in subtropical areas of China with similar climate and soil conditions (Table 1).
One criterion for the success of translocation is the formation of a self-sustaining and self-renewing population (Griffith et al., 1989; Reiter et al., 2016). In our study, after a long period of translocation, Pterostyrax psilophyllus could produce naturally regenerated seedlings, while Davidia involucrata, Dipteronia sinensis and Tapiscia sinensis were only able to blossom and yield fruit, basically meeting the «from seed to seed» criteria for successful conservation (He, 2002). Tetracentron sinense could grow normally, but no flowers or fruit was observed on this species. Two potential explanations for this disparity are proposed. First, the cultivation time (20-35 years) was not long enough for some species to become mature. For example, D. involu-crata usually requires 30-40 years to blossom and produce fruit. Secondly, a high rate of self and low viability of seeds in transplanted populations with small population sizes (Fig. 2).
Changes in leaf functional traits
In our study, Pterostyrax psilophyllus and Tapi-scia sinensis had a higher SLA in transplanted populations compared to the wild ones. Davidia involucrata and Tetracentron sinense had a higher LNC and LPC in transplanted compared to the wild population. However, the SLA, LNC, and LPC of Dip-teronia sinensis were all lower or similar in transplanted compared to the wild population. The SLA is positively correlated with relative growth rates. The LNC tends to be closely correlated with photo-synthetic rate, and the LNC and LPC are often correlated with each other (Perez-Harguindeguy et al., 2013). Thus, the results indicated that the efficiency of resource acquisition or utilisation of all species expect D. sinensis in transplanted populations increased and more resources were available for
growth (Aerts & Chapin, 2000; Vance et al., 2003; Adler et al., 2014). This may be due to the reduction of interspecific competition in the transplanted populations, because only endangered species were transplanted there, the number of species decreased in the translocation site (Plein et al., 2016).
However, Dipteronia sinensis presented the opposite trend with a lower SLA, LNC and a higher LDMC in the transplanted population. The LDMC can represent the proportion of resources invested in these structures, and plants with a higher LDMC are more resistant to physical damage (Cornelissen et al., 2003). That is, the investment in growth decreased while the investment in structure increased, which may be due to the increased intraspecific competition (Rol-hauser et al., 2019). On the wild site, there are many species of Aceraceae in the endangered species community, but most of them are non-endangered species. Thus, when simulated the community in the translocation site, a large number of the endangered species D. sinensis was transplanted to the translocation site to serve as the main substitute of Aceraceae species (Ye et al., 2000). The large individual number of the same species, D. sinensis, may contribute to an intense interspecies competition on the translocation site. Therefore, we should pay attention to the number of species and individuals in the future translocation.
It was worth noting that although all species showed a significant difference in the LNC and/ or LPC values between transplanted and wild populations, there was no significant difference in leaf N:P except for Tapiscia sinensis. According to the homeostasis hypothesis, the relatively active plant organs need to maintain a certain nutrient level to ensure the material production and energy utilisation efficiency (Zhang et al., 2018). Therefore, most of these species still maintained their original nitrogen and phosphorus homeosta-sis on the translocation site, which may be due to the similar community structure and microhabitat to that on the wild site.
Changes in intraspecific trait variation
Intraspecific trait variation can enhance plant resistance to environmental changes and conducive to species co-existence (Carlucci et al., 2015). The intraspecific variation in certain traits of Dip-teronia sinensis, Tapiscia sinensis and Tetracentron sinense was different. Dipteronia sinensis and T. sinensis showed lower CV-values in leaf area,
SLA, LDMC and LNC, but higher ones in LPC and leaf N:P, while T. sinense showed lower CV-values in LNC, LPC and leaf N:P, but higher ones in leaf area, SLA and LDMC, in the transplanted population than in the wild population. That may be due to the different heterogeneity of light and soil condition of different species on the wild and the translocation site (Boucher et al., 2013).
However, the habitat filter causes the functional traits of plants to become more similar, which will lead to a reduction in the intraspecific variation of traits (Liu et al., 2018). In our study, the intraspecific traits variation of Davidia involucra-ta and Pterostyrax psilophyllus in the transplanted population was lower than or similar to that in the wild population; that is, leaf traits of these two species tended to be similar, which might be related to the similar microhabitats within species on the translocation site (Boucher et al., 2013; Karbstein et al., 2020). Davidia involucrata and P. psilophyllus are both tall, fast-growing trees located at the top layer of the community, so the microhabitats of different individuals, such as light conditions, were similar in the translocation site. Similar leaf traits may lead to competitive exclusion and affect species co-existence, which is detrimental to their performance (Adler et al., 2013; Li et al., 2018). Sides et al. (2014) suggested that the larger the local distribution area of a species, the higher its traits variation will be. Therefore, we propose to expand the planting area appropriately in future translocation.
Phenotypic plasticity and genetic adaptation play very important roles in shaping leaf functional traits (Bresson et al., 2011; Vitasse et al., 2014; de Villemereuil et al., 2016). In our study, species in the transplanted population had covered the genetic diversity present in their original population (Xiao et al., 2021). In addition, individuals in transplanted populations were directly transplanted from wild populations, so the leaf traits were probably similar between the two populations immediately after the transplantation. Therefore, changes in leaf traits in this study were mainly caused by phenotypic plasticity.
Conclusions
After a long period of translocation, these five endangered tree species in transplanted populations were able to grow normally and four of the five species (Davidia involucrata, Pterostyrax psilophyllus, Tapiscia sinensis and Tetracentron sinense) become more efficient in resource
acquisition or utilisation and more resources were available for growth. However, the intraspecific trait variation of some species (D. involucrata and P. psilophyllus) in the translocation site was decreased as a whole, which may lead to a competitive exclusion and affect species coexistence, and affect their performance.
Acknowledgments
We thank M.T. Liu, J.M. Liu, D. Wan, Z.Q. Xiao, and H.J. Meng for their assistance during fieldwork. We are also grateful to the staffs of both Houhe National Nature Reserve and Jiugongshan National Nature Reserve. This work was supported by the National Natural Science Foundation of China (Grants No. 31870510 and 31770572) and the National Key Research and Development Program of China (2016YFC0503105).
References
Ackerly D. 2004. Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecological Monographs 74(1): 25-44. DOI: 10.1890/03-4022 Adler P.B., Fajardo A., Kleinhesselink A.R., Kraft N.J.B. 2013. Trait-based tests of coexistence mechanisms. Ecology Letters 16(10): 1294-1306. DOI: 10.1111/ele.12157 Adler P.B., Salguero-Gómez R., Compagnoni A., Hsu J.S., Ray-Mukherjee J., Mbeau-Ache C., Franco M. 2014. Functional traits explain variation in plant life history strategies. Proceedings of the National Academy of Sciences of the United States of America 111(2): 740-745. DOI: 10.1073/pnas.1315179111 Aerts R., Chapin F.S. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1-67. DOI: 10.1016/s0065-2504(08)60016-1 Agrawal A.A. 2001. Phenotypic plasticity in the interactions and evolution of species. Science 294(5541): 321-326. DOI: 10.1126/science.1060701 Albert C.H., Grassein F., Schurr F.M., Vieilledent G., Violle C. 2011. When and how should intraspecific variability be considered in trait-based plant ecology? Perspectives in Plant Ecology, Evolution and Systematics 13(3): 217-225. DOI: 10.1016/j.ppees.2011.04.003 Boucher F.C., Thuiller W., Arnoldi C., Albert C.H., Lavergne S. 2013. Unravelling the architecture of functional variability in wild populations of Polygonum viviparum L. Functional Ecology 27(2): 382391. DOI: 10.1111/1365-2435.12034 Bresson C.C., Vitasse Y., Kremer A., Delzon S. 2011. To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiology 31(11): 1164-1174. DOI: 10.1093/treephys/tpr084
Carlucci M.B., Debastiani V.J., Pillar V.D., Duarte L.D.S. 2015. Between- and within-species trait variability and the assembly of sapling communities in forest patches. Journal of Vegetation Science 26(1): 21-31. DOI: 10.1111/jvs.12223 Cho Y.C., Kim H.G., Koo B.Y., Shin J.K. 2019. Dynamics and viability analysis of transplanted and natural lady's slipper (Cypripedium japonicum) populations under habitat management in South Korea. Restoration Ecology 27(1): 23-30. DOI: 10.1111/rec.12835 Cornelissen J.H.C., Lavorel S., Garnier E., Diaz S., Buchmann N., Gurvich D.E., Reich P.B., ter Steege H., Morgan H.D., van der Heijden M.G.A., Pausas J.G., Poorter H. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51(4): 335-380. DOI: 10.1071/BT02124 de Villemereuil P., Gaggiotti O.E., Mouterde M., Till-Bottraud I. 2016. Common garden experiments in the genomic era: new perspectives and opportunities. Heredity 116(3): 249-254. DOI: 10.1038/hdy.2015.93 Dirzo R., Raven P.H. 2003. Global state of biodiversity and loss. Annual Review of Environment and Resources 28: 137-167. DOI: 10.1146/annurev.en-ergy.28.050302.105532 Ensslin A., Godefroid S. 2020. Ex situ cultivation impacts on plant traits and drought stress response in a multi-species experiment. Biological Conservation 248: 108630. DOI: 10.1016/j.biocon.2020.108630 Ensslin A., Tschöpe O., Burkart M., Joshi J. 2015. Fitness decline and adaptation to novel environments in ex situ plant collections: Current knowledge and future perspectives. Biological Conservation 192: 394-401. DOI: 10.1016/j.biocon.2015.10.012 Fu L.K., Jin J.M. 1992. China Plant Red Data Book: rare and endangered plants. Beijing: Science Press. 741 p. Gomes V.M., Negreiros D., Fernandes G.W., Pires A.C.V., Silva A.C.D.R., Le Stradic S. 2018. Long-term monitoring of shrub species translocation in degraded Neotropical mountain grassland. Restoration Ecology 26(1): 91-96. DOI: 10.1111/rec.12537 Griffith B., Scott J.M., Carpenter J.W., Reed C. 1989. Translocation as a species conservation tool: status and strategy. Science 245(4917): 477-480. DOI: 10.1126/science.245.4917.477 Havens K., Vitt P., Maunder M., Guerrant E.O., Dix-on K. 2006. Ex Situ Plant Conservation and Beyond. BioScience 56(6): 525-531. DOI: 10.1641/0006-3568(2006)56[525:ESPCAB]2.0.CO;2 He S.A. 2002. Fifty years of botanical gardens in China.
Acta Botanica Sinica 44(9): 1123-1133. Heberling J.M., Kichey T., Decocq G., Fridley J.D. 2016. Plant functional shifts in the invaded range: a test with reciprocal forest invaders of Europe and North America. Functional Ecology 30(6): 875-884. DOI: 10.1111/1365-2435.12590
Izuddin M., Yam T.W., Webb E.L. 2018. Specific niche requirements drive long-term survival and growth of translocated epiphytic orchids in an urbanised tropical landscape. Urban Ecosystem 21(3): 531-540. DOI: 10.1007/s11252-018-0733-2 Karbstein K., Prinz K., Hellwig F., Römermann C. 2020. Plant intraspecific functional trait variation is related to within-habitat heterogeneity and genetic diversity in Trifolium montanum L. Ecology and Evolution 10(11): 5015-5033. DOI: 10.1002/ece3.6255 Li T., Wu J., Chen H., Ji L., Yu D., Zhou L., Zhou W., Tong Y., Li Y., Dai L. 2018. Intraspecific functional trait variability across different spatial scales: a case study of two dominant trees in Korean pine broad-leaved forest. Plant Ecology 219(8): 875-886. DOI: 10.1007/s11258-018-0840-4 Li Y.Y., Tsang E.P.K., Cui M.Y., Chen X.Y. 2012. Too early to call it success: an evaluation of the natural regeneration of the endangered Metasequoia glyptostro-boides. Biological Conservation 150(1): 1-4. DOI: 10.1016/j.biocon.2012.02.020 Liu R., Liang S., Long W., Jiang Y. 2018. Variations in Leaf Functional Traits Across Ecological Scales in Riparian Plant Communities of the Lijiang River, Guilin, Southwest China. Tropical Conservation Science 11(1). DOI:10.1177/1940082918804680 Mayr H. 1906. Fremdländische Wald-und Parkbäume für
Europa. Berlin: P. Parey. 622 p. Mimura M., Yahara T., Faith D.P., Vázquez-Domínguez E., Colautti R.I., Araki H., Javadi F., Nunez-Farfan J., Mori A.S., Zhou S.L., Hollingsworth P.M., Neaves L.E., Fukano Y., Smith G.F., Sato Y.I., Tachida H., Hendry A.P. 2017. Understanding and monitoring the consequences of human impacts on intraspecific variation. Evolutionary Applications 10(2): 121-139. DOI: 10.1111/eva.12436 Mounce R., Smith P., Brockington S. 2017. Ex situ conservation of plant diversity in the world's botanic gardens. Nature Plants 3(10): 795-802. DOI: 10.1038/s41477-017-0019-3 NewtonA.C. 2008. Conservation oftree species through sustainable use: how can it be achieved in practice? Oryx 42(2): 195-205. DOI: 10.1017/S003060530800759X Oldfield S.F. 2009. Botanic gardens and the conservation of tree species. Trends in Plant Science 14(11): 581583. DOI: 10.1016/j.tplants.2009.08.013 Pérez-Harguindeguy N., Diaz S., Garnier E., Lavorel S., Poorter H., Jaureguiberry P., Bret-Harte M.S., Cornwell W.K., Craine J.M., Gurvich D.E., Urcelay C., Veneklaas E.J., Reich P.B., Poorter L., Wright I.J., Ray P., Enrico L., Pausas J.G., de Vos A.C., Buchmann N., Funes G., Quétier F., Hodgson J.G., Thompson K., Morgan H.D., ter Steege H., van der Heijden M.G.A., Sack L., Blonder B., Poschlod P. et al. 2013. New handbook for standardised measurement of plant functional traits worldwide. Aus-
tralian Journal of Botany 61(3): 167-234. DOI: 10.1071/BT12225 Pimm S.L., Jenkins C.N., Abell R., Brooks T.M., Gittleman J.L., Joppa L.N., Raven P.H., Roberts C.M., Sexton J.O. 2014. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344(6187): 1246752. DOI: 10.1126/science.1246752 Plein M., Bode M., Moir M.L., Vesk P.A. 2016. Translocation strategies for multiple species depend on interspecific interaction type. Ecological Applications 26(4): 1186-1197. DOI: 10.1890/15-0409 Poorter L., Bongers F. 2006. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87(7): 1733-1743. DOI: 10.1890/0012-9658(2006)87[1733:LTAGP0]2.0.C0;2 Rauschkolb R., Szczeparska L., Kehl A., Bossdorf O., Scheepens J.F. 2019. Plant populations of three threatened species experience rapid evolution under ex situ cultivation. Biodiversity and Conservation 28(14): 3951-3969. DOI: 10.1007/s10531-019-01859-9 Reiter N., Whitfield J., Pollard G., Bedggood W., Argall M., Dixon K., Davis B., Swarts N. 2016. Orchid reintroductions: an evaluation of success and ecological considerations using key comparative studies from Australia. Plant Ecology 217(1): 81-95. DOI: 10.1007/s11258-015-0561-x Ren H., Wang J., Liu H., Yuan L., Xu Y., Zhang Q., Yu H., Luo J. 2016. Conservation introduction resulted in similar reproductive success of Camellia changii compared with augmentation. Plant Ecology 217(2): 219-228. DOI 10.1007/s11258-015-0515-3 Rolhauser A.G., Nordenstahl M., Aguiar M.R., Pucheta E. 2019. Community-level natural selection modes: a quadratic framework to link multiple functional traits with competitive ability. Journal of Ecology 107(3): 1457-1468. DOI: 10.1111/1365-2745.13094 Román-Dañobeytia F.J., Levy-Tacher S.I., Aronson J., Rodrigues R.R., Castellanos-Albores J. 2012. Testing the performance of fourteen native tropical tree species in two abandoned pastures of the Lacandon Rainforest Region of Chiapas, Mexico. Restoration Ecology 20(3): 378-386. DOI: 10.1111/j.1526-100x.2011.00779.x Sides C.B., Enquist B.J., Ebersole J.J., Smith M.N., Henderson A.N., Sloat L.L. 2014. Revisiting Darwin's hypothesis: does greater intraspecific variability increase species' ecological breadth? American Journal of Botany 101(1): 56-62. DOI: 10.3732/ajb.1300284 Vance C.P., Uhde-Stone C., Allan D.L. 2003. Phosphorus acquisition and use: critical adaptations by plants
for securing a nonrenewable resource. New Phy-tologist 157(3): 423-447. DOI: 10.1046/j.1469-8137.2003.00695.x Violle C., Navas M.L., Vile D., Kazakou E., Fortunel C., Hummel I., Garnier E. 2007. Let the concept of trait be functional! Oikos 116(5): 882-892. DOI: 10.1111/j.0030-1299.2007.15559.x Vitasse Y., Lenz A., Kollas C., Randin C.F., Hoch G., Körner C. 2014. Genetic vs. non-genetic responses of leaf morphology and growth to elevation in temperate tree species. Functional Ecology 28(1): 243-252. D0I:10.1111/1365-2435.12161 Wang S., Zheng Z., Peng F., Zhao Z. 1988. The present state of preservation of the precious, rare and threatened plants in Hubei, as well as the proposition for studying further these plants. Journal of Wuhan Botanical Research 6(3): 285-298. Wendelberger K.S., Fellows M.Q.N., Maschinski J. 2008. Rescue and Restoration: Experimental Translocation of Amorpha herbacea Walter var. crenulata (Rybd.) Isley into a Novel Urban Habitat. Restoration Ecology 16(4): 542-552. DOI: 10.1111/j.1526-100x.2007.00325.x Westoby M., Falster D.S., Moles A.T., Vesk P.A., Wright I.J. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33(1): 125-159. DOI: 10.1146/annurev.ecolsys.33.010802.150452 Xiao Z.Q., Yang T., Wang S.T., Wei X.Z., Jiang M.X. 2021. Exploring the origin and genetic representation of ex situ living collections of five endangered tree species established for 20-35 years. Global Ecology and Conservation 32: e01928. DOI: 10.1016/j. gecco.2021.e01928 Ye Q.G., Wang C., Wang S.Y. 2000. A preliminary study on the design of a community for ex situ conservation of the rare and endangered plants in the Three Gorge reservoir area. Journal of Wuhan Botanical Research 18(1): 33-41. Zhang J.H., Zhao N., Liu C.C., Yang H., Li M.L., Yu G.R., Wilcox K., Yu Q., He N.P. 2018. C:N:P stoichiom-etry in China's forests: From organs to ecosystems. Function Ecology 32(1): 50-60. DOI:10.1111/1365-2435.12979
Zhu Y., Chen C., Guo Y., Fu S., Chen H.Y.H. 2020. Linking leaf-level morphological and physiological plasticity to seedling survival and growth of introduced Canadian sugar maple to elevated precipitation under warming. Forest Ecology and Management 457: 117758. DOI: 10.1016/j.foreco.2019.117758
ОТЛИЧАЮТСЯ ЛИ ФУНКЦИОНАЛЬНЫЕ ПРИЗНАКИ ЛИСТА МЕЖДУ
20-35-ЛЕТНИМИ ТРАНСЛОЦИРОВАННЫМИ И ПРИРОДНЫМИ ПОПУЛЯЦИЯМИ? ТЕМАТИЧЕСКОЕ ИССЛЕДОВАНИЕ ПЯТИ ВИДОВ ДЕРЕВЬЕВ, НАХОДЯЩИХСЯ ПОД УГРОЗОЙ ИСЧЕЗНОВЕНИЯ
Ш. Ван12 3, Я. Сюй12 3, С. Вэй12 3 * , М. Цзян12 3
1 Уханьский ботанический сад Академии наук Китая, Китай 2Центр биологии сохранения Центральных ботанических садов Академии наук Китая, Китай
3Университет Академии наук Китая, Китай *e-mail: [email protected]
Сохранение видов, находящихся под угрозой исчезновения, посредством транслокации стало эффективным способом противодействия исчезновению видов во всем мире. Функциональные признаки растений являются хорошими предикторами продуктивности растений и могут отражать стратегии адаптации растений к окружающей среде. Однако до сих пор неясно, имеют ли трансплантированные популяции сопоставимые уровни функциональных признаков листа с таковыми в популяциях в дикой природе. Чтобы оценить эффективность природоохранной транслокации деревьев-долгожителей, находящихся под угрозой исчезновения, мы исследовали многолетнюю (20-35 лет) популяционную динамику пяти сосуществующих исчезающих видов деревьев (Davidia involucrata, Dipteronia sinensis, Pterostyrax psilophyllus, Tapiscia sinensis и Tetracentron sinense) в транслоцированных популяциях и сравнили функциональные признаки листьев между транслоцированными и исходными (природными) популяциями. Мы обнаружили, что выживаемость пяти видов в транслоцированных популяциях колебалась от 42.86% до 73.81%, и большинство этих видов могли цвести и плодоносить. Все виды имели статистически значимые различия в некоторых функциональных признаках листьев между транслоцированными и природными популяциями. В целом, внутривидовая изменчивость некоторых видов в транслоцированных популяциях была снижена по сравнению с таковой в природных популяциях. Мы пришли к выводу, что после длительного периода транслокации эти виды в транслоцированных популяциях были способны нормально расти, и большинство видов характеризовались более эффективным приобретением или использованием ресурсов, и для их роста стало доступно больше ресурсов. Однако внутривидовая изменчивость некоторых видов в транслоцированных популяциях может привести к конкурентному исключению, повлиять на сосуществование видов и, таким образом, повлиять на их продуктивность.
Ключевые слова: внутривидовая изменчивость признака, деревья-долгожители, динамика популяции, долговременный мониторинг, природоохранная транслокация
