Next Article in Journal
A 230-Year Summer Precipitation Variations Recorded by Tree-Ring δ18O in Heng Mountains, North China
Previous Article in Journal
Effect of Species Composition on Growth and Yield in Mixed Beech–Coniferous Stands
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 13
Issue 10
10.3390/f13101653
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Triggering Effect of Gaps on Seedling Germination of the Soil Seed Bank in Tropical Rain Forests, Hainan Island, South China

by
Lirong Yang
1,2,†,
Xiaobo Lv
1,3,†,
Xiaobo Yang
1,*,
Guofeng Zhang
4 and
Donghai Li
1
1
Institute of Ecology and Environment, Hainan University, Haikou 570228, China
2
Laboratory Management Center, Qingdao Agricultural University, Qingdao 266109, China
3
Hainan Academy of Forestry, Haikou 570110, China
4
Hainan Institute of Meteorological Sciences, Haikou 570203, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2022, 13(10), 1653; https://doi.org/10.3390/f13101653
Submission received: 15 September 2022 / Revised: 2 October 2022 / Accepted: 5 October 2022 / Published: 9 October 2022
(This article belongs to the Section Forest Soil)
Browse Figures
Review Reports Versions Notes

Abstract

:
Light, soil temperature, and soil moisture likely change when a gap or clearing is formed in closed-canopy forests, triggering seed germination in the soil seed bank. However, which factors induce such seed germination remains elusive. In this study, we explored the triggering mechanism of gaps on seed germination in the soil seed bank without felling trees. Power sources were supplied in the forest, and three types of lamps were used to simulate the photo-thermal, light, and temperature environments of gaps (i.e., photo-thermal separation in the field), respectively. The photo-thermal separation experiment was carried out in the tropical rain forests of Bawangling in Hainan Island, South China. Three common pioneers and one late-successional species of the Bawangling area were selected for an indoor photo-thermal separation experiment. The field experiment results showed a significant difference in the average seedling number between groups exposed to light and the control group (13.2 ± 4.0 and 1.4 ± 1.7, respectively; p < 0.01), indicating that light in gaps can initiate seed germination of some species in the soil seed bank. Further indoor validation experiments supported this conclusion. No significant difference was observed in the average seedling number between the thermal group (2.1 ± 1.6) and the control group. The indoor validation experiment showed that changes in temperature alone could not trigger the seed germination of the three pioneer species in darkness. However, a higher average seedling number was observed in the photo-thermal group (15.7 ± 5.6) compared to the light group, indicating that the combined effect of light and temperature can initiate seed germination in the soil seed bank, which was also supported by the indoor verification experiment. We further showed that the ratio of species requiring only light for seed germination to those requiring both light and temperature was 2:3. More case studies are necessary to determine if such outcomes are common in forest soil seed banks.

1. Introduction

Since the 1940s, scientists have gradually realized, based on a large number of field investigations and studies, that plant communities are mosaic complexes composed of different patches, and that forest gaps play important roles in the maintenance of forest structure, dynamics, and diversity [1,2,3,4,5,6,7,8,9]. After the gap is formed, the micro-habitat, including the light, temperature, and humidity, of the gap is expected to change (especially the light and soil surface temperature), and part of the dormant seeds in the soil seed bank begin to germinate under the stimulation of changing environments [10]. How does the change in environmental factors of the forest gap affect the seed germination of the soil seed bank? Which environmental factors play a decisive role? So far, these questions remain unexplored.
Seed germination is affected by an array of environmental factors [11,12,13,14,15]. In the soil seed bank of tropical rain forests, seed germination can be affected by light, such as increased light intensity and the high proportion of red light [1,16,17,18,19], or by high temperature and large temperature fluctuations [20]. These environmental factors vary with the formation of forest gaps and the changing light [21,22,23].
Therefore, light is one of the most considered environmental factors regarding forest gaps, as it triggers seed germination in the soil seed bank. Some indoor experiments conducted on target species indicated that seeds of many pioneer species only germinate under light conditions [10,24,25,26], whereas the seed germination of non-pioneer species does not require light [3,22]. In a forest gap, the increase in light radiation leads to an increment in the fluctuation of the daily temperature and soil surface temperature in the forest gap [23,27,28]. The seed germination of some pioneer tree species is not regulated by light but by temperature, and their seeds can only germinate under high-temperature or variable-temperature conditions [13,20,29,30]. Chen et al. (2013) [30] have shown that the seed germination of Ficus hispida and Ficus racemosa is regulated by both light and temperature in the forest gap. In previous studies, there were some cases in which collected seeds were placed in the forest gap or artificial shed to study the effect of the micro-environment of the forest gap on seed germination [16,31]. Other studies employed indoor artificial devices, such as artificial climate chambers and heating rods, to study the effects of light and temperature on the seed germination of forest trees [20,26,30]. The problem with studies using forest gaps or sheds is that the light and temperature factors are not separated, which makes it impossible to determine whether the light or the temperature triggers seed germination. Although the indoor experiment can separate light and temperature, the research material of the indoor experiment is usually the seeds of the target species, not the seeds in the soil seed bank. The factors affecting the collected seeds and the naturally formed seeds in the soil seed bank may be different. The results of indoor experiments can be used to verify the conclusions obtained from field experiments, but they cannot reflect the actual factors affecting seed germination in the soil seed bank. Therefore, we assume that, in tropical rain forest, the germination of part of the seeds in the forest soil seed bank is affected primarily by light; the process is also affected in part by temperature and partly by the interaction of light and temperature. However, to answer these questions through research on the forest soil seed bank, the method to separate the light and temperature factors in the forest gap environment must first be explored. At present, no study has reported the use of a photo-thermal separation method in the field to study the mechanism of seed germination in the forest soil seed bank.
In this study, investigations were conducted on the soil seed bank of the tropical montane rain forest in Bawangling, Hainan Island, China, and the photo-thermal separation method was employed to study the influence of the light and temperature of the forest gap on seed germination of the soil seed bank. Based on field experiments, three common pioneer species and one late-successional species in the Bawangling area were selected for the indoor verification experiment. Artificial climate chambers were used to simulate the environment of the forest gap and understory; dark treatment was used as the control to verify the results of the field experiment.

2. Material and Methods

2.1. Overview of the Study Site

The study site is located on the northeastern ridge of the Dong’er Station in the Bawangling Nature Reserve, Hainan Island, China (19°05′44″ N, 109°10′47″ E) (Figure 1). The altitude of the study site is 980–990 m, the slope is 20–30° with a north-east slope direction, and the soil is mountain yellow soil. In the 1970s, before the establishment of the nature reserve, this area was used as a forest farm for timber harvesting, and the vegetation was destroyed to a certain extent. After the nature reserve was established in 1980, the vegetation in this area began to recover. The vegetation is tropical montane rain forest dominated by Fagaceae plants and is in the middle of its succession [32]. This area has a tropical monsoon climate, with obvious dry and wet seasons. The rainy season is from May to October, and the dry season is from November to April. The annual average temperature is 23.6 °C, and the annual average rainfall is 1500–2000 mm [33].

2.2. The Photo-Thermal Separation Method Used in the Forest Understory

The photo-thermal separation method used in the forest understory has been developed by our team to study seed germination of the soil seed bank. The halogen lamp that emits a continuous light spectrum [34] is a kind of incandescent lamp. It provides illumination close to daylight and harbors both visible light and heat; thus, it can be used to simulate the photo-thermal environment of the forest gap. The energy-saving lamp is a cold-light-source lamp and emits a discontinuous light spectrum [35]. There is almost no heat in the light provided by the energy-saving lamp; thus, it can be used to simulate the light environment of the forest gap. The ceramic heating lamp uses far-infrared light to provide heat, which does not emit any visible light; thus, it can be used to simulate the temperature environment of the forest gap. The application of these three different lamps in the forest understory effectively separate the light and temperature factors that may affect seed germination of the soil seed bank. The photo-thermal environment, the light environment, and the temperature environment of the forest gap were simulated, and the specific combination experiments were as follows:
A 15 m × 15 m understory plot was selected as the study area, divided into nine squares (5 m × 5 m) to serve as replicates. A light group (LG), a temperature group (TG), a photo-thermal group (PTG), and a control group (CG) were set up in each square (Figure 2). As a light source, 85-w energy-saving lamps(Opple, Shanghai, China)were used; ceramic-heating lamps (Super reptile, Shanghai, China) were used in the TG as the heat source; and 35-w H3 halogen lamps (Sunca, China) were used in the PTG as the light and heat sources. In the understory, three wooden stakes were used to fix the halogen lamp at 1 m above the ground, and a plastic bag was applied to wrap the upper part of the lamp to prevent the rainwater from damaging the lamp. The lampshades were attached to both the energy-saving and the ceramic heating lamps before the lamps were hung on a fixed PVC pipe. The bottom of the PVC pipe, with a diameter of 20 cm, was about 10 cm above the ground; the height of the PVC pipe holding the energy-saving lamp was 40 cm, while that of the PVC pipe supporting the ceramic heating lamp was 20 cm. The PVC pipe was used for concentrating light and heat, and the lampshade was used to protect the light source from rainwater and the spreading of foreign seeds. The newly fallen litter on the surface of each plot was removed, and the PVC pipes were fixed in a circle with a diameter of 20 cm above the ground of each plot to form an experimental area, reducing the soil erosion of the plot by ground water. The sunlight time in the forest gap of the Bawangling area is from 8:00 a.m. to 4:00 p.m. [23]; therefore, the light was supplied from 8:00 a.m. to 4:00 p.m. in this study. An Em50 soil temperature and humidity recorder (Decagon Devices, Pullman, WA, USA) was used to record the temperature and humidity of the 0–5 cm soil layer at an interval of 30 min and a duration of 8 months. An LX-1010B digital illuminance recorder (Shuangxu Electronics Co., Ltd., Shanghai, China) was used to measure light intensity. All plots were watered every day to ensure proper soil moisture.

2.3. Indoor Verification Experiment

Seeds of three common pioneer species from the Bawangling area were selected for the indoor single-factor verification experiment, and the late-successional species Cryptocarya chinensis was used as the control [36,37,38]. The characteristics of each species [30] are shown in Table 1.
Three sets of PRX-250 intelligent artificial climate chambers (Haishusaifu Experimental Instrument Factory, Ningbo, China) were used for the indoor photo-thermal separation experiments. The three artificial climate chambers were all set to a photoperiod of 14 h light/10 h dark; one artificial climate chamber was set to 20–30 °C to simulate the gap environment, one was set to 20–25 °C to simulate the understory environment, and one was set to a constant temperature at 30 °C. The three light intensity gradients included the gap light (125 μmol m−2 s−1), the understory light (6 μmol m−2 s−1), and the dark area (<0.13 μmol m−2 s−1). The artificial climate chamber that simulated the gap environment was divided into three parts by transparent partitioning from top to bottom: the first part was under the original light, to simulate the light condition of the forest gap; black plastic bags were used to block the light source in the second part, to simulate the dark environment; and multi-layer shading nets were used to block the light source in the third part, to simulate the understory light conditions (Figure 3). A total of five different treatments were conducted, with three replicates for each treatment.
The seeds were collected in Bawangling, Hainan Island, one to two months prior to the experiment. The seeds were brought back to the laboratory and dried in the dark for later use. Before the experiment, the seeds or fruits of each tree species were soaked in distilled water for 72 h to ensure they fully absorbed water. Fine sand was obtained by sieving through a 0.2-mm sieve and used as the substrate for seed germination. The fine sand was placed in an oven at 80 °C for 24 h before use and was then placed in a Petri dish to reach a thickness of 1 cm. Twenty seeds each of Thysanolaena maxima and Melastoma sanguineum, ten seeds of Trema tomentosa, and eight seeds of Cryptocarya chinensis were used for each treatment. The seeds were buried in the surface layer of sandy soil with a water content of 20%. The Petri dish was sealed with a transparent plastic film and a rubber band to prevent rapid water loss. The seed germination situation was recorded every other day until no more new seeds germinated within a week. An LX-1010B digital illuminance recorder (Shuangxu Electronics Co., Ltd., Shanghai, China) was used for the light intensity measurements.
Forests 13 01653 g003 550
Figure 3. The design diagram for the seed germination experiments in artificial climate chambers.
Figure 3. The design diagram for the seed germination experiments in artificial climate chambers.
Forests 13 01653 g003

2.4. Data Analyses

The complete temperature records of each month obtained from the field experiment were used for statistical analyses. The maximum temperature, minimum temperature, average temperature, and variation in daily temperature were used to calculate the maximum daily temperature, minimum daily temperature, average daily temperature, and average daily temperature variations for each month. The number of germinated seeds and their species were recorded every three days once seed germination was observed. The seedling species were identified according to the Flora of China [39]. For those seedling species that could not be identified, only the number of germinated seeds was recorded. A total of nine indicators, including the time required for seed germination, the time required for seed germination in half of the plots, the time required for seed germination in all the plots, the total number of seedlings, the average number of seedlings in the plot, the maximum and minimum numbers of seedlings in the plot, and the seedling species, were compared to reveal the characteristics of seed germination in the understory soil seed bank under various light and heat conditions.
In each treatment, the final germination rate (FG), the germination starting time (GS), and mean time to germinate (MTG) were calculated [25] according to the following formulas:
(1)
FG = number of germinated seeds/total number of seeds × 100%;
(2)
GS = number of days from the start of the experiment to 1/6 of the FG;
(3)
MTG = Σ Ni. Di/Σ Ni.
where Ni represents the number of seeds germinated on the i-th day, and Di represents the number of days to germinate.
One-way analyses of variance (ANOVAs) were used to compare the differences in the number of germinated seeds between the treatments in the germination experiment of the understory soil seed bank; the non-parametric test was used to test for differences in the number of germinated seeds between the treatments in the indoor verification experiment. The geographic location map of the study site (Figure 1) was generated with ArcGIS v9.3 (ESRI, Redlands, CA, USA); Figure 4, Figure 7 and Figure 8 were created with SigmaPlot v12.0 (Systat, Chicago, IL, USA), and the remaining figures were created with Excel 2003 (Microsoft, Redmond, WA, USA); ANOVAs and the non-parametric test were conducted in SPSS v19.0 (IBM, Armonk, New York, NY, USA).

3. Results

3.1. Effect of Simulated Light and Soil Temperature on Seed Germination of the Soil Seed Bank

3.1.1. Light and Temperature Characteristics under Different Treatments in the Germination Experiment of the Understory Soil Seed Bank

Table 2 lists the light and temperature characteristics of the different treatments in the germination experiment of the understory soil seed bank. Results showed that the average light intensity of PTG was the highest (954 μmol m−2 s−1), and that of LG was 75 μmol m−2 s−1, which was lower compared to PTG but 20 times higher compared to the understory light intensity (Table 2). Based on the full light intensity of 1800 μmol m−2 s−1 [22], the light intensity of PTG was 50% that of the full light, the light intensity of LG was 4% that of the full light, the light intensity of TG was 0.07% that of the full light, and the light intensity of the understory was 0.34% that of the full light. Due to the shelter of the PVC pipes, the light intensity of TG was lower than that of the understory. The temperature characteristics of CG and LG were consistent; the average maximum daily temperatures of CG and LG were 20.5 °C and 20.8 °C, respectively, with daily temperature variations of <4 °C. The characteristics of the daily maximum temperature, daily temperature variation, and average daily temperature of TG and PTG were similar, which were significantly higher than those of CG and LG. The average maximum daily temperatures of PTG and TG were 31.6 °C and 32.2 °C, respectively, with daily temperature variations of >7 °C (Figure 4).
Forests 13 01653 g004 550
Figure 4. Temperature characteristics of the soil seed bank micro-environmentunder different photo-thermal treatments: (A) monthly average minimum daily soil surface temperature; (B) monthly average maximum daily soil surface temperature; (C) monthly average daily variation of the soil surface temperature; (D) monthly average soil surface temperature. Dec is December, Jan is January, Feb is February, Mar is March, Apr is April, Jun is June, and Jul is July.
Figure 4. Temperature characteristics of the soil seed bank micro-environmentunder different photo-thermal treatments: (A) monthly average minimum daily soil surface temperature; (B) monthly average maximum daily soil surface temperature; (C) monthly average daily variation of the soil surface temperature; (D) monthly average soil surface temperature. Dec is December, Jan is January, Feb is February, Mar is March, Apr is April, Jun is June, and Jul is July.
Forests 13 01653 g004

3.1.2. Seed Germination in the Understory Soil Seed Bank under Photo-Thermal Separation Conditions and Remaining Conditions

The germination characteristics of each treatment group are shown in Table 3. Results showed that the time required for seed germination, the time required for seed germination in half of the plots, and the time required for seed germination in all the plots of PTG were the shortest, while the number and species of emerged seedlings were the largest. In PTG, seed germination was observed in all nine plots at 142 d after the experiment began, and a total of 141 seedlings were obtained. Most of the seedlings died before the true leaves emerged; thus, the species could not be identified. Among the emerged seedlings, 29 seedlings were identified to belong to 12 species, including 6 pioneer species (Blechnum orientale, Melastoma affine, Evodia lepta, Trema tomentosa, Gynura crepidioides, and Melastoma sanguineum) and 6 non-pioneer species (Wendlandia uvariifolia, Rubus reflexus, Engelhardia roxburghiana, Lithocarpus corneus, Musa balbisiana, and Scleria biflora).
The time required for seed germination, the time required for seed germination in half of the plots, and the time required for seed germination in all the plots of LG were longer. Seed germination was observed in all nine plots after 192 d from the start of the experiment. The total number of emerged seedlings was 119, belonging to only six species. Among them, Evodia glabrifolia, Evodia lepta, and Melastoma sanguineum were pioneer species, while Smilax hypoglauca, Rubus reflexus, and Cayratia japonica were non-pioneer species.
The time required for seed germination and the time required for seed germination in half of the plots of TG and CG were even longer. By the end of the experiment, there were still four plots without seed germination observed. The numbers of emerged seedlings were 19 and 13, respectively. The emerged seedlings grew extremely slowly, and some seedlings died soon after emergence; therefore, their species could not be identified. However, it can be confirmed that none of the species that appeared in PTG and LG were present in TG or CG.
One-way ANOVA was carried out between four different treatments in the understory photo-thermal separation experiment. The results revealed significant differences in the number of seedlings among different photo-thermal treatments (p = 0.000067). The results of multiple comparisons showed that the differences in seedling numbers between PTG and TG, between PTG and CG, between LG and TG, and between LG and CG were extremely significant (p = 0.00012, respectively), while no significant difference was observed between PTG and LG and between TG and CG (p = 0.174 and p = 0.707, respectively). The relationship between light intensity and seedling number (Figure 5) showed that the number of emerged seedlings in LG was significantly higher than that in CG. However, the identified number of species in LG was lower by six relative to the number in PTG, indicating that the light in the gap can initiate the seed germination of some species in the soil seed bank, and that the combined effect of light and temperature can initiate the seed germination of more species. Figure 6 illustrates the soil temperature and the number of emerged seedlings. There was no significant difference in the number of emerged seedlings between TG and CG (Figure 6), which seemed to indicate that temperature alone cannot trigger seed germination in the soil seed bank.
Table
Table 3. Comparisons of the seed germination characteristics in the soil seed bank under different photo-thermal treatments.
Table 3. Comparisons of the seed germination characteristics in the soil seed bank under different photo-thermal treatments.
GroupA (Day)B (Day)C (Day)D (Seedling Number)E (Seedling Number)F (Seedling Number)G (Seedling Number)
PTG20 a38 a142 a141 a15.7 a22 a7 a
LG31 a50 b192 a119 a13.2 a21 a10 a
TG49 a197 c/ b19 b2.1 b4 b0 b
CG170 b200 c/ b13 c1.4 b5 b0 b
Note: A, days for the first seed germination; B, days for the seed germination in half of the plots; C, days for the seed germination in all the plots; D, total seedling number; E, average seedling number in the plot; F, maximum seedling number in the plot; G, minimum seedling number in the plot; /, seed germination did not occur in half of the plots or all the plots at the end of the experiment. Different lowercase letters indicate significant differences (p < 0.05).
Forests 13 01653 g005 550
Figure 5. Effect of light intensity on the number of emerged seedlings in the soil seed bank under different photo-thermal treatments.
Figure 5. Effect of light intensity on the number of emerged seedlings in the soil seed bank under different photo-thermal treatments.
Forests 13 01653 g005
Forests 13 01653 g006 550
Figure 6. Effect of soil surface temperature on the number of emerged seedlings in the soil seed bank under different photo-thermal treatments.
Figure 6. Effect of soil surface temperature on the number of emerged seedlings in the soil seed bank under different photo-thermal treatments.
Forests 13 01653 g006

3.2. Indoor Verification Experiments

The results of the indoor verification experiment showed that T. maxima, M. sanguineum, and T. tomentosa did not germinate under dark conditions, and they all germinated in the simulated light environment of the understory and forest gap (Figure 7). In contrast, C. chinensis germinated under the three light conditions, and the FG of C. chinensis under dark conditions was the same as that in the simulated understory light environment; both were 28%. The differences in the FG, MTG, and GS of T. maxima among the three light conditions were extremely significant (p = 0.004, p = 0.0056, p = 0.0074); the GS of T. maxima under simulated understory light conditions occurred later than under simulated gap light conditions, and the germination speed of T. maxima in the simulated understory light environment was slower than that in the simulated gap light environment (Table 4). The FG of M. sanguineum differed significantly (p = 0.0357) among the three light conditions, while extremely significant differences were observed in the MTG and GS of M. sanguineum among the three light conditions (p = 0.0032, p = 0.00026). The GS of M. sanguineum occurred slightly later in the simulated understory light environment than in the simulated gap light environment, but the germination speed of M. sanguineum was much slower in the simulated understory light environment (Table 4). The FG, MTG, and GS of T. tomentosa were significantly different among the three light conditions (p = 0.0256, p = 0.042, and p = 0.01). The GS of T. tomentosa was significantly later in the simulated understory light environment than in the simulated gap light environment, and the germination speed was also much slower in the simulated understory light environment (Table 4). The above results indicate that light intensity can significantly affect the seed germination of pioneer species T. maxima, M. sanguineum, and T. tomentosa. Under dark conditions, their seeds would not germinate, even if the moisture and temperature were appropriate.
Table
Table 4. The mean time to germinate (MTG) and germination starting time (GS) of the three representative species under different photo-thermal conditions of the indoor verification experiment.
Table 4. The mean time to germinate (MTG) and germination starting time (GS) of the three representative species under different photo-thermal conditions of the indoor verification experiment.
MTG (d)GS (d)
SpeciesDarkUnderstory LightGap LightDarkUnderstory LightGap Light
Thysanolaena latifolia/ a17.3 b9.2 b/ a9 b7.5 b
Melastoma sanguineum/ a22 b14.5 c/ a14 b11 c
Trema tomentosa/ a29 a21.8 b/ a25 a15 b
20/30 ℃30 ℃20/25 ℃20/30 ℃30 ℃20/25 ℃
Thysanolaena latifolia8.3 a7.6 a12 b7.5 a7 a9.5 b
Melastoma sanguineum12.8 a13.3 a20.3 b9.5 a8.5 a14 b
Trema tomentosa20 a/ b/ b15 a/ b/ b
/ means no seedling emerged from this species under this condition. Different lowercase letters indicate significant differences (p < 0.05).
Forests 13 01653 g007 550
Figure 7. Effect of light intensity on seed germination of species with different ecological forms. Germination curves of (A) Thysanolaena maxima, (B) Melastoma sanguineum, (C) Trema tomentosa, and (D) Cryptocarya chinensis under different light intensities.
Figure 7. Effect of light intensity on seed germination of species with different ecological forms. Germination curves of (A) Thysanolaena maxima, (B) Melastoma sanguineum, (C) Trema tomentosa, and (D) Cryptocarya chinensis under different light intensities.
Forests 13 01653 g007
T. maxima, M. sanguineum, and C. chinensis germinated under the three temperature conditions, and their FG values were similar. T. tomentosa only germinated in the simulated gap temperature environment (Figure 8). The difference in the FG of T. maxima among the three temperatures was not significant (p = 0.980), but the differences in the MTG and GS of T. maxima were significant (p = 0.0327, p = 0.0218). The GS of T. maxima in the simulated understory temperature environment was the latest, and the germination speed was the slowest. The difference in the FG of M. sanguineum among the three temperatures was not significant (p = 0.252). However, the differences in the MTG and GS of M. sanguineum were significant among the three temperature conditions (p = 0.018, p = 0.0287): the GS of M. sanguineum was the latest in the simulated understory temperature environment, with the lowest germination speed. The differences in the FG, MTG, and GS of T. tomentosa among the three temperatures were extremely significant (p = 0.0054, p = 0.0032, p = 0.0008). Seed germination was only observed in the simulated gap temperature environment, and the FG was 93% (Figure 7C and Table 4). In summary, the temperature had a significant effect on the FG of T. maxima and M. sanguineum seeds under suitable light and moisture conditions, and obviously affected the GS and germination speed. Temperature showed the most apparent effect on the germination of T. tomentosa seeds, which only germinated in the simulated gap temperature environment.
To sum up, light intensity had a significant effect on the seed germination of the three pioneer species. Temperature had no significant effect on the germination of T. maxima and M. sanguineum seeds, but it can increase the germination speed of these seeds. Temperature had a significant effect on the germination of T. tomentosa seeds, which required the gap photo-thermal conditions to germinate. Therefore, the seed germination of T. maxima and M. sanguineum is regulated by the light factor of the gap, while that of T. tomentosa is regulated by both the light and temperature factors of the gap. However, the seed germination of C. chinensis as a control is not regulated by the light or temperature factor of the gap. This conclusion further validates and refines the findings of the understory photo-thermal separation experiment: light is the main factor affecting seed germination of pioneer species in the soil seed bank of tropical rain forests, and appropriate temperature will promote seed germination. However, the seed germination of the late-successional species is not affected by light or temperature.

4. Discussion

The formation of forest gaps leads to increased light radiation, which carries heat to the soil in the gap, leading to soil temperature variations [23,40]. Zang [23] conducted a study on the gap environment of tropical montane rain forests at different cycle stages in Bawangling, Hainan Island, in April 2001. The results showed that the maximum light intensity in the center of the gap could reach up to 540 μmol m−2 s−1, while the maximum light intensity at the edge of the gap was 144 μmol m−2 s−1. A study by Chazdon and Pearcy [40] in Costa Rica showed that the photosynthetically active radiation of the understory light was generally 1%–2% that of the full light; it was 9% in the center of a 200 m2 forest gap and increased to 20%–35% in the center of a 400 m2 forest gap. In a stable understory habitat, the daily variation in soil temperature is small; however, the soil temperature may increase by 15 °C or much higher than the understory soil temperature in the presence of the gap [23,41]. Overall, in this study, the understory photo-thermal separation experiment showed that the photo-thermal environment in the halogen lamp treatment group was similar to that of the forest gap. The temperature characteristics in the ceramic heating lamp treatment group were close to those in the forest gap, while the light intensity of this group was close to that of the understory. The light intensity of the energy-saving lamp treatment group (75 μmol m−2 s−1) was close to that at the edge of the forest gap, and the average temperature was only 0.2 °C higher than that of the control group. In summary, the halogen lamp group simulated the photo-thermal environment of the forest gap, the energy-saving lamp simulated the light characteristics of the forest gap, and the ceramic heating lamp simulated the temperature characteristics of the forest gap. We successfully simulated the characteristics of individual environmental factors (i.e., light and temperature) in the forest gap using three kinds of lamps, without destroying the vegetation on the ground, and separated the light and temperature factors in the forest gap environment.
There are currently two main methods to study the soil seed bank. One is to collect the understory soil, which is used for seed germination experiments under natural light and temperature conditions [42,43,44]. This method is mainly used to study the species composition and distribution of the soil seed bank. The other method uses seeds of several plant species, which are placed under artificial light and temperature conditions for single-factor control experiments [30,31,45]. This method can obtain the effect of single factors (e.g., light and temperature) on the seed germination of test species and can verify whether the seed germination of test species is regulated by light, temperature, or the combination of light and temperature.
In fact, as early as at the end of the last century, the conclusion that light can regulate seed germination has been confirmed [4,46,47,48]. A large number of indoor simulation experiments have shown that many seeds from pioneer species can only germinate under light conditions [10,17,20,29,48], while seeds of some other pioneer species can germinate under temperature increments or alteration [20,29,30]. Chen et al. (2013) [30] studied the regulation of temperature on the photosensitivity seeds of four Ficus species in Xishuangbanna, and found that under 25/35 °C, a low R:FR (0.25) could not inhibit the seed germination of F. hispida and F. racemosa in the gap. However, under 22/23 °C, a low R:FR (0.25) could inhibit their seed germination, while the seed germination of the understory species F. altissima and F. auriculata was not inhibited. This indicates that seed germination of F. hispida and F. racemosa is regulated by two factors (i.e., light and temperature) in the forest gap. Pearson et al. (2003) believed that the germination of small seeds (<2 mg) was more photosensitive, while the germination of large seeds was mostly temperature-controlled [49,50]. However, different plants have different light-factor requirements. Among the four Piper species studied by Dows et al. (2002), only one required high-intensity light to reach the maximum germination value, while the remaining three species only needed medium- or low-intensity light to reach the maximum germination value [51]. These results indicate that the seed germination of some forest species may be regulated by light alone, the seed germination of some species may be regulated by temperature alone, and the seed germination of some species may be comprehensively regulated by both light and temperature. However, these studies were not conducted on the actual soil seed banks; thus, their results cannot reflect the true situation of the soil seed bank. This study successfully separated the light and temperature factors in the natural environment and carried out single-factor experiments that simulated the forest gap environment, without destroying the forest vegetation.
In this germination experiment of the understory soil seed bank, the supply of power sources and the application of different lamps successfully separated the light and temperature factors in the gap, realizing the independent simulation of the light or temperature factors of the natural forest gaps. The results of the indoor photo-thermal separation experiment obtained from a few target species verified and supplemented the conclusions of the photo-thermal separation experiment in the forest understory. The conclusions of this study and the photo-thermal separation method will provide a new starting point and new insights for future research on the seed germination mechanism of soil seed banks.

5. Conclusions

In this study, we demonstrated that in Hainan Island, China, the light factor alone in the gap could indeed initiate seed germination of some species in the soil seed bank, while the combination of the light and temperature factors can initiate seed germination of a larger number of species in the soil seed bank. With the indoor verification experiment, temperature alone cannot initiate seed germination in the soil seed bank. This study further showed that in Hainan Island, China, in the soil seed bank of the tropical rain forest, the ratio of the species that can germinate due to light only, and the species that require a comprehensive combination of light and temperature to germinate, was 2:3. Our experiment represents the first of such a case study; thus, the results obtained from studies in other different regions, different forests, or even different plots may be different. Therefore, more research is needed to verify whether there are common patterns in the forest soil seed bank.

Author Contributions

Conceptualization, X.Y.; methodology, L.Y. and X.L.; software, L.Y. and G.Z.; validation, L.Y.; formal analysis, L.Y.; investigation, L.Y., X.L. and G.Z.; data curation, L.Y.; writing and editing, L.Y. and X.Y.; visualization, X.Y.; supervision, X.Y.; project administration, D.L.; funding acquisition, D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Natural Foundation of China (31460120, 31760170) and the National Science and Technology Support Program Project (2012BAC18B04-3-1).

Institutional Review Board Statement

Not applicable for studies not involving humans or animals.

Informed Consent Statement

Not applicable.

Acknowledgments

Thanks to Qing Chen, Zengnan Xie, Lubiao Huang, and Yuhai Qiu of the Hainan Bawangling National Nature Reserve Administration for their help in seedling identification and field trials. Thanks to Chunhong Wan, Chu Tao, Wenqi Luo, and Yukai Chen of Hainan University for their excellent assistance in field trials and seedling identification.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Watt, A.S. Pattern and process in the plant community. J. Ecol. 1947, 35, 1–22. [Google Scholar] [CrossRef] [Green Version]
  2. Pickett, S.T.A.; White, P.S. The Ecology of Natural Disturbance and Patch Dynamics; Academic Press: New York, NY, USA, 1985. [Google Scholar]
  3. Whitmore, T.C. Canopy gaps and the two major groups of forest trees. Ecology 1989, 70, 536–538. [Google Scholar] [CrossRef]
  4. Whitmore, T.C. Changes over twenty-one years in the Kolombangara rain forests. J. Ecol. 1989, 77, 469–483. [Google Scholar] [CrossRef]
  5. Everham, E.M.; Brokaw, N.V. Forest damage and recovery from catastrophic wind. Bot. Rev. 1996, 62, 113–185. [Google Scholar] [CrossRef]
  6. Du, Y.J.; Mi, X.C.; Ma, K.P. Comparison of seed rain and seed limitation between community understory and gaps in a subtropical evergreen forest. Acta Oecologica 2012, 44, 11–19. [Google Scholar] [CrossRef]
  7. Feng, D.L.; Huang, X.H.; Geng, Y.H.; Zhu, H.X. Influence of forest gaps and litter on growth of Castanopsis fargesii and Castanopsis carlesii in the Pinus massoniana pure forest of the three gorges reservoir area. Appl. Mech. Mater. 2014, 692, 33–39. [Google Scholar] [CrossRef]
  8. Ren, J.Y.; Kadir, A.; Yue, M. The role of tree-fall gaps in the natural regeneration of birch forests in the taibai mountains. Appl. Veg. Sci. 2015, 18, 64–74. [Google Scholar] [CrossRef]
  9. Meiado, M.V.; Rojas-Aréchiga, M.; de Siqueira-Filho, J.A.; Leal, I.R. Effects of light and temperature on seed germination of cacti of brazilian ecosystems. Plant Species Biol. 2016, 31, 87–97. [Google Scholar] [CrossRef]
  10. Vàzquez-Yanes, C.; Smith, H. Phytochrome control of seed germination in the tropical rain forest pioneer trees Cecropia obtusifolia and Piper auritum and its ecological significance. New Phytol. 1982, 92, 477–485. [Google Scholar] [CrossRef]
  11. Bewley, J.D.; Black, M. Seeds: Physiology of Development and Germination; Plenum Press: New York, NY, USA, 1994. [Google Scholar]
  12. Gul, B.; Weber, D.J. Effect of dormancy relieving compounds on the seed germination of non-dormant Allenrolfea occidentalis under salinity stress. Ann. Bot. 1998, 82, 555–560. [Google Scholar] [CrossRef]
  13. Rosbakh, S.; Poschlod, P. Initial temperature of seed germination as related to species occurrence along a temperature gradient. Funct. Ecol. 2015, 29, 5–14. [Google Scholar] [CrossRef]
  14. Aghamir, F.; Bahrami, H.; Malakouti, M.J.; Eshghi, S.; Sharifi, F. Seed germination and seedling growth of bean (Phaseolus vulgaris) as influenced by magnetized saline water. Eurasian J. Soil Sci. 2016, 5, 39–46. [Google Scholar] [CrossRef] [Green Version]
  15. Carón, M.M.; Frenne, P.D.; Verheyen, K.; Quinteros, A.; Ortega-Baes, P. Germination responses to light of four Neotropical forest tree species along an elevational gradient in the southern Central Andes. Ecol. Res. 2020, 35, 550–558. [Google Scholar] [CrossRef] [Green Version]
  16. Orozco-Segovia, A.; Vàzquez-Yanes, C. Light effect on seed germination in Piper L. Acta Oecologica Oecologia Plant. 1989, 10, 123–146. [Google Scholar]
  17. Vàzquez-Yanes, C.; Orozco-Segovia, A. Ecological significance of light controlled seed germination in two contrasting tropical habitats. Oecologia 1990, 83, 171–175. [Google Scholar] [CrossRef] [PubMed]
  18. Valio, I.F.M.; Joly, C.A. Light Sensitivity of the Seeds on the Distribution of Cecropia glaziovi Snethlage (Moraceae). Z. Pflanzenphysiol. 1979, 91, 371–376. [Google Scholar] [CrossRef]
  19. Vázquez-Yanes, C. Germination of a pioneer tree (Trema guineensis Ficahlo) from Equatorial Africa. Turrialba 1977, 27, 301–302. [Google Scholar]
  20. Vàzquez-Yanes, C.; Orozco-Segovia, A. Seed germination of a tropical rain forest pioneer tree (Heliocarpusdonnell-smithii) in response to diurnal fluctuation of temperature. Physiol. Plant 1982, 56, 295–298. [Google Scholar] [CrossRef]
  21. Yu, Y.; Baskin, J.M.; Baskin, C.C.; Tang, Y.; Cao, M. Ecology of seed germination of eight non-pioneer tree species from a tropical seasonal rain forest in southwest China. Plant Ecol. 2008, 197, 1–16. [Google Scholar] [CrossRef]
  22. Zang, R.G. Measurement and analysis on light and temperature regimes in different patch types of forest cycle in a tropical mountain rain forest, Hainan Island. J. Beijing For. Univ. 2002, 24, 125–130. [Google Scholar]
  23. Vàzquez-Yanes, C.; Orozco-Segovia, A. Light gap detection by the photoblastic seeds of Cecropia obtusifolia and Piper auritum, two tropical rain forest trees. Biol. Plant. 1987, 29, 234–236. [Google Scholar] [CrossRef]
  24. Vàzquez-Yanes, C.; Orozco-Segovia, A.; Rincón, E.; Sanchez-Coronado, M.E.; Huante, P.; Toledo, J.R.; Barradas, V.L. Light beneath the litter in a tropical forest: Effect on seed germination. Ecology 1990, 7, 1952–1958. [Google Scholar] [CrossRef]
  25. Chen, H.; Zhang, S.; Cao, M. Effects of light and temperature on seed germination of Ficus hispida in Xishuangbanna, Southwest China. J. Plant Ecol. 2008, 32, 1084–1090. (In Chinese) [Google Scholar]
  26. Zang, R.G.; Tao, J.; Li, C. Within community patch dynamics in a tropical montane rain forest of Hainan Island, South China. Acta Oecologica 2005, 28, 39–48. [Google Scholar] [CrossRef]
  27. Duan, W.B.; Guo, Q.W.; Chen, L.X.; Feng, J.; Wang, L.X.; Du, S. Heterogeneity of soil surface temperature and shallow soil temperature in different size gaps of broadleaved Pinus koraiensis forest. J. Beijing For. Univ. 2019, 41, 108–121. [Google Scholar]
  28. Probert, R.J. The role of temperature in the regulation of seed dormancy and germination. In Seed: The Ecology of Regeneration in Plant Communities; Fenner, M., Ed.; CABI: London, UK, 2000; pp. 261–292. [Google Scholar]
  29. Vranckx, G.; Vandelook, F. A season and gap detection mechanism regulates seed germination of two temperate forest pioneers. Plant Biol. 2012, 14, 481–490. [Google Scholar] [CrossRef]
  30. Chen, H.; Cao, M.; Baskin, J.M.; Baskin, C.C. Temperature regulates positively photoblastic seed germination in four Ficus (moraceae) tree species from contrasting habitats in a seasonal tropical rainforest. Am. J. Bot. 2013, 100, 1683–1687. [Google Scholar] [CrossRef]
  31. Kyereh, B.; Swaine, M.; Thompson, J. Effect of light on the germination of forest trees in Ghana. J. Ecol. 1999, 87, 772–783. [Google Scholar] [CrossRef]
  32. Lv, X.B.; Yang, L.R.; Yang, M.; Yang, X.B.; Li, D.H.; Tao, C.; Wan, C.H. Study on the distribution patterns and dynamics of main tree population of Fagaceae dominance in tropical montane rain forest in Hainan Island. Chin. Agric. Sci. Bull. 2012, 28, 84–90. [Google Scholar]
  33. Liu, W.D.; Zang, R.G.; Ding, Y. Community features of two types of typical tropical monsoon forests in Bawangling Nature Reserve, Hainan Island. Acta Ecol. Sin. 2009, 29, 3465–3476. [Google Scholar]
  34. Ojanen, M.; Kärhä, P.; Ikonen, E. Spectral irradiance model for tungsten halogen lamps in 340–850 nm wavelength range. Appl. Opt. 2010, 49, 880–886. [Google Scholar] [CrossRef] [Green Version]
  35. Steigerwald, D.A.; Bhat, J.C.; Collins, D.; Fletcher, R.M.; Holcomb, M.O.; Ludowise, M.J.; Martin, P.S.; Rudaz, S.L. Illumination with solid state lighting technology. IEEE J. Sel. Top. Quantum Electron. 2002, 8, 310–320. [Google Scholar] [CrossRef]
  36. Gong, Q.; Zhou, J.S.; Liu, D.M.; Yi, W.; Xing, F.W.; Chen, H.F. Application of native plants in the ecological virescence of Guang-Wu Expressway. Ecol. Environ. 2007, 16, 486–491. [Google Scholar]
  37. Zhang, Z.D.; Zang, R.G. Predicting potential distribution of dominant woody plant keystone species in a natural tropical forest landscape of Bawangling, Hainan Island, South China. J. Plant Ecol. 2007, 31, 1079–1091. (In Chinese) [Google Scholar]
  38. Wang, Z.F.; Gao, S.H.; Tian, S.N.; Fu, S.L.; Ren, H.; Peng, S.L. Genetic structure of Cryptocarya chinensis in fragmented lower subtropical forests in China based on ISSR markers. Biodivers. Sci. 2005, 13, 324–331. [Google Scholar] [CrossRef] [Green Version]
  39. Editorial Committee of Flora Reipublicae Popularis Sinicae. Flora Reipublicae Popularis Sinicae; Sciences Press: Beijing, China, 1959–2004.
  40. Chazdon, R.L.; Pearcy, R.W. The importance of sunflecks for forest understory plants. BioScience 1991, 41, 760–766. [Google Scholar] [CrossRef]
  41. Ritter, E.; Dalsgaard, L.; Einhorn, K.S. Light, temperature and soil moisture regimes following gap formation in a semi-natural beech-dominated forest in Denmark. For. Ecol. Manag. 2005, 206, 15–33. [Google Scholar] [CrossRef]
  42. Daïnou, K.; Bauduin, A.; Bourland, N.; Gillet, J.F.; Fétéké, F.; Doucet, J.L. Soil seed bank characteristics in Cameroonian rainforests and implications for post-logging forest recovery. Ecol. Eng. 2011, 37, 1499–1506. [Google Scholar] [CrossRef]
  43. Han, A.R.; Sohng, J.E.; Barile, J.R.; Lee, Y.K.; Woo, S.Y.; Lee, D.K.; Park, P.S. Comparison of Soil Seed Banks in Canopy Gap and Closed Canopy Areas between a Secondary Natural Forest and a Big Leaf Mahogany (Swietenia macrophylla King) Plantation in the Mt. Makiling Forest Reserve, Philippines. J. Environ. Sci. Manag. 2012, 15, 47–59. [Google Scholar]
  44. Miller, G.; Cummins, R. Soil seed banks of woodland, heathland, grassland, mire and montane communities, Cairngorm Mountains, Scotland. Plant Ecol. 2003, 168, 255–266. [Google Scholar] [CrossRef]
  45. Liu, K.; Baskin, J.M.; Baskin, C.C.; Bu, H.; Du, G.; Ma, M. Effect of diurnal fluctuating versus constant temperatures on germination of 445 species from the eastern Tibet Plateau. PLoS ONE 2013, 8, e69364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Swaine, M.D.; Whitmore, T.C. On the definition of ecological species groups in tropical rain forests. Vegetatio 1988, 75, 81–86. [Google Scholar] [CrossRef]
  47. Vàzquez-Yanes, C.; Orozco-Segovia, A. Signals for Seeds to Sense and Respond to Gaps. Ecophysiological Processes above and below Ground; Academic Press: New York, NY, USA, 1994. [Google Scholar]
  48. Nishii, K.; Nagata, T.; Wang, C.N.; Mölle, M. Light as environmental regulator for germination and macrocotyledon development in Streptocarpus rexii. S. Afr. J. Bot. 2012, 81, 50–60. [Google Scholar] [CrossRef] [Green Version]
  49. Pearson, T.R.H.; Burslem, D.F.R.P.; Mullins, C.E.; Dalling, J.W. Germination ecology of neotropical pioneers: Interacting effects of environmental conditions and seed size. Ecology 2002, 83, 2798–2807. [Google Scholar] [CrossRef]
  50. Pearson, T.R.H.; Burslem, D.F.R.P.; Mullins, C.E.; Dalling, J.W. Functional significance of photoblastic germination in neotropical pioneer trees: A seed’s eye view. Funct. Ecol. 2003, 17, 394–402. [Google Scholar] [CrossRef] [Green Version]
  51. Daws, M.I.; Burslem, D.F.R.P.; Crabtree, L.M.; Kirkman, P.; Mullins, C.E.; Dalling, J.W. Differences in seed germination responses may promote coexistence of four sympatric Piper species. Funct. Ecol. 2002, 16, 258–267. [Google Scholar] [CrossRef]
Forests 13 01653 g001 550
Figure 1. Location of the Bawangling Mountain and the study site.
Figure 1. Location of the Bawangling Mountain and the study site.
Forests 13 01653 g001
Forests 13 01653 g002 550
Figure 2. Plot design for the photo-thermal separation experiment in the forest.
Figure 2. Plot design for the photo-thermal separation experiment in the forest.
Forests 13 01653 g002
Forests 13 01653 g008 550
Figure 8. Effect of temperature on seed germination of species with different ecological forms. Germination curves of (A) Thysanolaena maxima, (B) Melastoma sanguineum, (C) Trema tomentosa, and (D) Cryptocarya chinensis under different temperatures.
Figure 8. Effect of temperature on seed germination of species with different ecological forms. Germination curves of (A) Thysanolaena maxima, (B) Melastoma sanguineum, (C) Trema tomentosa, and (D) Cryptocarya chinensis under different temperatures.
Forests 13 01653 g008
Table
Table 1. Main characteristics of the species used in this study.
Table 1. Main characteristics of the species used in this study.
SpeciesFamilyLife FormEcological FormHabitatSeed Shape and Size
Thysanolaena maximaPoaceaeHPRoadside and sparse forestCircular with a diameter of 0.1 mm
Melastoma sanguineumMelastomataceaeSPRoadsideFlat semicircle with a length of 2 mm
Trema tomentosaUlmaceaeTPRoadsideCircular with a diameter of 2 mm
Cryptocarya chinensisLauraceaeTNPHidden forestCircular with a diameter of 10 mm
H, herb; S, shrub; T, tree; P, pioneer species; NP, non-pioneer species.
Table
Table 2. Soil surface temperature and light intensity under different photo-thermal treatments.
Table 2. Soil surface temperature and light intensity under different photo-thermal treatments.
GroupTmin (°C)Tmax (°C)T (°C)L (μmol m−2 s−1)
TG17.932.221.41.3
PTG17.831.621.0954
LG17.920.819.275
CG17.720.519.06.2
Tmin, average minimum soil surface temperature; Tmax, average maximum soil surface temperature; T, average soil surface temperature; L, average light intensity.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Yang, L.; Lv, X.; Yang, X.; Zhang, G.; Li, D. The Triggering Effect of Gaps on Seedling Germination of the Soil Seed Bank in Tropical Rain Forests, Hainan Island, South China. Forests 2022, 13, 1653. https://doi.org/10.3390/f13101653

AMA Style

Yang L, Lv X, Yang X, Zhang G, Li D. The Triggering Effect of Gaps on Seedling Germination of the Soil Seed Bank in Tropical Rain Forests, Hainan Island, South China. Forests. 2022; 13(10):1653. https://doi.org/10.3390/f13101653

Chicago/Turabian Style

Yang, Lirong, Xiaobo Lv, Xiaobo Yang, Guofeng Zhang, and Donghai Li. 2022. "The Triggering Effect of Gaps on Seedling Germination of the Soil Seed Bank in Tropical Rain Forests, Hainan Island, South China" Forests 13, no. 10: 1653. https://doi.org/10.3390/f13101653

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop