Article Interactive Effects of Intertidal Elevation and Light Level on Early Growth of Five Species under Sonneratia apetala Buch. Hamplantation Canopy: Turning Monocultures to Mixed Forests

Zhongmao Jiang, Wei Guan, Yanmei Xiong, Mei Li, Yujun Chen and Baowen Liao *

Key Laboratory of State Forestry Administration on Tropical Forestry, Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China; [email protected] (Z.J.); [email protected] (W.G.); [email protected] (Y.X.); [email protected] (M.L.); [email protected] (Y.C.) * Correspondence: [email protected]; Tel.: +86-186-6466-1496

 Received: 9 December 2018; Accepted: 20 January 2019; Published: 22 January 2019 

Abstract: The introduced Sonneratia apetala Buch. Hamplantation plantations have occupied more than 3800 ha in China. The prevalence, fast growth rate, and high seed production of S. apetala have raised concerns about the risks to native mangrove habitats. Efforts are required to convert these introduced monocultures to mixed or native forests. In this study, we examined native mangrove colonization in the introduced S. apetala plantations at the Qi’ao Island, Zhuhai, China. A 12-month field study was conducted to evaluate the effects of intertidal elevation and light level on the survival and early growth of five native mangrove species, viz., gymnorrhiza (L.) Savigny, obovata Sheue, Liu & Yong, Aegiceras corniculatum (L.) Blanco, Avicennia marina (Forssk.) Vierh., and Rhizophora stylosa Griff. Across intertidal elevations and light levels, the survival of B. gymnorrhiza was the highest. All the species had relatively higher survival rates under 30% canopy closure. Although the seedlings survived best at high intertidal elevation, the relative growth rate (RGR) was the highest at low intertidal elevation, and it was promoted by high light level. The stem height at low intertidal elevation was higher than that at high intertidal elevation, and it was the highest under 30% canopy closure. B. gymnorrhiza and R. stylosa at high intertidal elevation had relatively high leaf numbers, whereas K. obovata and A. marina showed a reverse tendency. The growth of stem diameter showed a decreasing trend initially and then increased with better performance at low intertidal elevations, and B. gymnorrhiza presented the best value under 30% canopy closure. Bruguiera gymnorrhiza showed the highest growth rate under similar conditions. Overall, intensive canopy thinning is an effective measure to promote native mangrove growth in S. apetala plantations. Additionally, increasing planting density especially at low intertidal elevations may improve native mangrove establishment and growth. Furthermore, Bruguiera gymnorrhiza is the best choice in the effort to native species in S. apetala plantations in the study area.

Keywords: intertidal elevation; light level; mangrove; restoration; survival

1. Introduction are the only forests bridging land and sea with a rich diversity of flora and fauna in the intertidal zones of tropical and subtropical coastlines [1,2]. Mangroves provide ecological services to humans, but they are also threatened by anthropogenic activities [3,4]. Mangrove habitats are becoming small or fragmented, which is attributable to anthropogenic activities, including aquaculture, agricultural reclamation, urbanization, and pollution explosion [5,6]. The mangrove forest area in

Forests 2019, 10, 83; doi:10.3390/f10020083 www.mdpi.com/journal/forests Forests 2019, 10, 83 2 of 13

China was 250,000 ha, but it was reduced to 42,000 ha by 1956, and further shrunk to 21,000 ha by the end of the 1980s and to 15,000 ha by the end of 1990s, according to the National Investigation of Forest Resource [6]. In the early 1990s, China launched a 10-year mangrove reforestation program in degraded mangrove areas, through which the mangrove forest areas have recovered to 22,000 ha [6]. However, the exotic mangrove species Sonneratia apetala replaced the main native species ( (Sheue, Liu & Yong) and Bruguiera gymnorrhiza (L.) Savigny) in this program, owing to its higher survival rate and faster growth [7]. Since 1998, S. apetala has been widely planted as a pioneer species in Guangdong, Guangxi, Fujian, and Zhejiang Provinces. The planting area of S. apetala has exceeded 3800 ha in China [8]. For example, Spartina alterniflora Loisel. began to invade the Qi’ao Island in the early 1990s [9], and expanded its coverage to up to 227 ha by 1995. In 1999, S. apetala was introduced to control S. alterniflora invasion, eventually eradicating S. alterniflora in 2011 (only 0.63 ha remained for experimental purpose) [10,11]. However, S. apetala covered approximately 600 ha on Qi’ao Island by 2008 [7]. Such a large area of S. apetala plantation and its prevalence, fast growth rate, and high seed production has raised the concern whether the introduced species threaten the survival and development of native mangrove species [12]. Peng et al. [13] explored the dynamic changes in mixed stands under naturally spreading condition of native species in S. apetala plantations. The planting density of S. apetala directly affects the canopy gaps, which can affect the density of tree seedlings and saplings. For example, Ren et al. [14] reported that the native mangrove species, namely K. obovata and Rhizophora stylosa Griff., could invade 4-year-old S. apetala plantations, but disappeared after 10 years in Leizhou Bay, Guangdong. However, in the Sanjiang River of Qiongshan, Hainan, the native mangrove species such as K. obovata, Aegiceras corniculatum (L.) Blanco, and Bruguiera sexangula (Lour.) Pior. were naturally diffused in a 12-year-old S. apetala plantation. Furthermore, compared with those of a 5-year-old S. apetala plantation, the number of species remained basically unchanged, and the diversity index and uniformity index increased marginally [15]. The planting density of S. apetala in these two plantations was 2500 and 833 /ha, respectively. Similarly, shading has been reported to significantly limit Xylocarpus granatum Koenig seedling growth and might affect the establishment of X. granatum under forest canopies [16]. In contrast, Rhizophora apiculata Blume, B. gymnorrhiza, and Xylocarpus moluccensis could have higher sapling and seedling densities under closed canopy than under open gaps [17]. Since 1999, S. apetala has been planted in approximately 600 ha in the Qi’ao Island, successfully controlling the further spread of S. alterniflora [7]. In addition to different canopy closures, this plantation also occupied high tide beaches and low tide beaches. Usually, Avicennia marina (Forssk.) Vierh., B. gymnorrhiza, and R. stylosa survived or grew the best at high intertidal elevation. Ceriops tagal (Perr.) C.B. Rob. reached the maximum abundance at low intertidal elevation [18]. Therefore, the objective of the present study was to compare the growth and physiological responses of five native mangrove species seedlings at different light levels and intertidal elevations. We also attempted to examine the interactive effect of light level and intertidal elevation on the early development of five native mangrove species seedlings. The results will provide a theoretical basis for afforestation in S. apetala plantations using native species.

2. Materials and Methods

2.1. Study Sites The study area is situated in the Qi’ao-Dangan Provincial Nature Reserve, located on the Qi’ao Island of Zhuhai in China. Its geographical location is 22◦2304000–22◦2703800 N and 113◦3604000–113◦3901500 E (Figure1). The region has south subtropical marine climate with an average annual rainfall of 1964.4 mm, annual sunshine duration of 1907.4 h, and annual average temperature of 22.4 ◦C. The tide pattern is irregular and semidiurnal, and the average salinity of sea water is 18 ± 2 . The average high tide level is 0.27 m, and the average low tide level is −0.24 m. The plantationh of 2.1. Study Sites The study area is situated in the Qi’ao-Dangan Provincial Nature Reserve, located on the Qi’ao Island of Zhuhai in China. Its geographical location is 22°23′40″–22°27′38″N and 113°36′40″–113°39′15″E (Figure 1). The region has south subtropical marine climate with an average annual rainfall of 1964.4 mm, annual sunshine duration of 1907.4 h, and annual average temperature of 22.4 °C. The tide pattern is irregular and semidiurnal, and the average salinity of sea water is 18 ± 2‰. The average high tide level is 0.27 m, and the average low tide level is −0.24 m. The plantation of S. apetala is fan-shaped in the tidal flat, and a small area of K. candel and A. corniculatum plantations was nearby. Five native species in Southern China (namely, K. obovata, A. corniculatum, A. marina, B. gymnorrhiza, and R. stylosa) were selected for the present study. The propagules of K. obovata and A. corniculatum were collected from Qi’ao Island. The propagules of A. marina, B. gymnorrhiza, and R. stylosa were collected from the Zhanjiang Mangrove National Nature Reserve (20°14′–21°35′N and 109°40′–110°35′E). The seeds of A. corniculatum and A. marina, and the hypocotyls of K. obovata, B. gymnorrhiza, and R. stylosa were collected from under the Forests 2019, 10, 83 3 of 13 canopy. The length of propagules (n = 50) of K. obovata, R. stylosa, and B. gymnorrhiza was 19.32 ± 2.72, 28.46 ± 3.48, and 15.49 ± 1.32, respectively, and their wet weight was 14.67 ± 3.75, S. apetala19.44 ±is 2.83, fan-shaped and 22.37 in the± 4.23 tidal g, flat,respectively. and a small The area mean of K.wet candel weightand ofA. A. corniculatum corniculatumplantations and A. wasmarina nearby. seeds was 0.008 ± 0.002 and 0.015 ± 0.004 g, respectively.

FigureFigure 1. Sketch. 1. Sketch map of map field of trial field sites trial in sites mangrove in mangrove plantation plantation at the Qi’ao at theIsland. Qi’ao The Island. abbreviations The of sitesabbreviations refer to 30% of canopysites refer closure to 30% (30% canopy CC), closure 60% canopy (30% CC), closure 60% (60% canopy CC) closure and 90% (60% canopy CC) closureand (90%90% CC), canopy respectively. closure (90% CC), respectively.

2.2.Five Experimental native species Design in Southern China (namely, K. obovata, A. corniculatum, A. marina, B. gymnorrhiza, and R. stylosa) were selected for the present study. The propagules of K. obovata and A. corniculatum were collectedWe measured from Qi’ao the Island. canopy The closure propagules using of fisheyeA. marina lens, B. camera gymnorrhiza (Nikon, and D750R. stylosa, Nikonwere collectedPrecision from Shanghai the Zhanjiang Co., MangroveLtd., Shanghai, National China Nature and Reserve SIGMA (20 ◦8mm140–21 F3.5◦350 N EX and DG 109 FISHEYE◦400–110◦, 350 E).Heshuo The seeds Optical of A. corniculatum Equipment andShanghaiA. marina Co.,, and Ltd the., Shanghai, hypocotyls China of K. obovata) at the, B. intersection gymnorrhiza , of and R. stylosadiagonalswere of collectedthe sample from plot under and selected the canopy. the plots The with length 30%, of propagules60%, and 90% (n =canopy 50) of closure.K. obovata , R. stylosaThe effects, and B. of gymnorrhiza wave actionwas (tidal 19.32 inundation± 2.72, 28.46 time± [18]3.48, and and wave 15.49 ± [19])1.32, on respectively, young mangrove and their wetspecies weight across was 14.67 the intertidal± 3.75, 19.44 zone± were2.83, different, and 22.37 a±nd4.23 the g, effects respectively. were relatively The mean significant wet weight in of A. corniculatumthe low intertidaland A. zone. marina Weseeds measured was 0.008 the water± 0.002 level and of 0.015 the low± 0.004 tide g,zone respectively. and high tide zone

2.2. Experimental Design We measured the canopy closure using fisheye lens camera (Nikon D750, Nikon Precision Shanghai Co., Ltd., Shanghai, China and SIGMA 8 mm F3.5 EX DG FISHEYE, Heshuo Optical Equipment Shanghai Co., Ltd., Shanghai, China) at the intersection of diagonals of the sample plot and selected the plots with 30%, 60%, and 90% canopy closure. The effects of wave action (tidal inundation time [18] and wave [19]) on young mangrove species across the intertidal zone were different, and the effects were relatively significant in the low intertidal zone. We measured the water level of the low tide zone and high tide zone using a water level logger (HOBO U20-001-0x, Onset computer corporation, Bourne, Massachusetts, America) at high tide; the average elevation difference of the tide zones was 0.87 ± 0.26 m. Quadrats of dimension 10 m × 10 m were created in the high tide beach and low tide beach with the canopy density of 30%, 60%, and 90%, respectively. Three repetitions per processing combination, a total of 18 sample plots, were performed. In April 2017, the hypocotyls of K. obovata and B. gymnorrhiza were planted, and the seeds of A. corniculatum and A. marina, and the hypocotyls of R. stylosa were planted in June in each plot. Fifty propagules were planted in each sample plot to examine the frequency and period of germination under six processing combinations. Forests 2019, 10, 83 4 of 13

2.3. Measurement of Seedling Survival and Seedling Growth From April 2017, a 12-month growth trial was set up, and seeding growth was measured once a month. The budding date of each propagule was recorded every 10 days, and the total number of propagules that survived was also counted in each sample plot. Other germination parameters, such as the stem height, stem basal diameter, and number of unfurled leaves, were measured at every 60 days after planting the propagules. The stem height and stem basal diameter of each seedling were determined directly using callipers. At the end of the trial, the seedlings were collected and separated into leaf, stem, and root components, and then dried at 65 ◦C to a constant mass to determine the biomass. The monthly relative growth rate (RGR) was determined, according to the method of Ye et al. [20].

2.4. Statistical Analyses For one-parameter statistical tests, the analysis of variance (ANOVA) was performed using SPSS 21.0 for Windows (SPSS Inc., New York, NY, USA). The differences in growth and physiological responses of seedlings among the five species and six habitats were analyzed with the two-way ANOVA. Significant differences among multiple means were determined by the SNK test.

3. Result

3.1. Seedling Survival During the 360-day trial, the number of seedlings that survived decreased gradually and differed significantly among the five species. There was a significant interactive effect of light level and intertidal elevation on the number of seedlings that survived among A. corniculatum, B. gymnorrhiza, K. obovata, and R. stylosa. There was no significant interactive effect of light level and intertidal elevation on A. marina (Table1).

Table 1. F values of two-way ANOVA tests indicating the differences of five mangrove species surviving in varying light level and intertidal elevation.

Sources of Variance Species Light Level Intertidal Elevation Light Level × Intertidal Elevation Ac 334 *** 9.21 *** 22.9 *** Am 455 *** 31.6 *** 1.69 NS Bg 31.7 *** 20.7 *** 12.3 *** Ko 116 *** 55.7 *** 84.2 *** Rs 85.2 *** 9.96 *** 14.2 *** Note: NS means not significant at p > 0.05 (n = 54). *** Statistical significance at p < 0.001. Ac = Aegiceras corniculatum, Am = Avicennia marina, Bg = Bruguiera gymnorrhiza, Ko = Kandelia obovata, Rs = Rhizophora stylosa.

The survival rate of the five mangrove species seedlings was different at different intertidal elevations. The survival rate of B. gymnorrhiza was the highest in each habitat, followed by K. obovata seedlings at low intertidal elevation. Conversely, the survival rate of A. marina, A. corniculatum, and R. stylosa was lower at the low intertidal elevation than at the high intertidal elevation. The number of A. corniculatum, A. marina, and R. stylosa seedlings that survived at the high intertidal elevation was higher than that at low intertidal elevation, whereas the number of B. gymnorrhiza and K. obovata seedlings that survived at low intertidal elevation was more than that at high intertidal elevation. The number of A. corniculatum and A. marina seedlings that survived decreased rapidly at low intertidal elevation, which may be dislodged by wave action. The number of R. stylosa seedlings that survived decreased rapidly in every habitat during 180 to 240 days (Figure2). The number of species that survived showed a marginal decreasing trend with time at high intertidal elevation, whereas the survival rate was stable from 240 days. With an increase in canopy closure, the number of seedlings that Note: NS means not significant at p > 0.05 (n = 54). *** Statistical significance at p < 0.001. Ac = Aegiceras corniculatum, Am = Avicennia marina, Bg = Bruguiera gymnorrhiza, Ko = Kandelia obovata, Rs = Rhizophora stylosa.

The survival rate of the five mangrove species seedlings was different at different intertidal elevations. The survival rate of B. gymnorrhiza was the highest in each habitat, followed by K. obovata seedlings at low intertidal elevation. Conversely, the survival rate of A. marina, A. corniculatum, and R. stylosa was lower at the low intertidal elevation than at the high intertidal elevation. The number of A. corniculatum, A. marina, and R. stylosa seedlings that survived at the high intertidal elevation was higher than that at low intertidal elevation, whereas the number of B. gymnorrhiza and K. obovata seedlings that survived at low intertidal elevation was more than that at high intertidal elevation. The number of A. corniculatum and A. marina seedlings that survived decreased rapidly at low intertidal elevation, which may be dislodged by wave action. The number of R. stylosa seedlings that survived decreased rapidly in every habitat during 180 to 240 days (Fig. 2). The number of species that survived showed a Forests 2019, 10, 83 5 of 13 marginal decreasing trend with time at high intertidal elevation, whereas the survival rate was stable from 240 days. With an increase in canopy closure, the number of seedlings that survivedsurvived among among the the five five mangrove mangrove species species was was also also different. different. In the In habitatsthe habitats of 60% of 60% and 90%and canopy90% closurecanopy with closure lower lightwith penetration,lower light thepenetration, average seedling the average survival seedling rate of survival mangrove rate species of mangrove decreased marginallyspecies decreased (Figure2). marginally Intertidal elevation (Fig. 2). hadIntertidal a higher elevation effect than had light a higher level effect on seedling than light survival. level on seedling survival. 55 55 50 50 45 45 40 40 35 35 30 30 25 25 20 20 15 15 0 60 120 180 240 300 360 0 60 120 180 240 300 360 A D 55 55 50 50 45 45 40 40 35 35 of seedlings seedlingsof

survivd 30 30 25 25 Number 20 20 15 15 Forests 2019, 10, 83 6 of 15 0 60 120 180 240 300 360 0 60 120 180 240 300 360 B E 55 55 50 50 45 45 40 40 35 35 30 30 Ac 25 Am 25 Bg 20 Ko 20 Rs 15 15 0 60 120 180 240 300 360 0 60 120 180 240 300 360 Time(day) Time(day) C F

FigureFigure 2.. The2. The number number of seedlings of seedlings of the of five the mangrove five mangrove species species surviving surviving (Bg = Bruguiera (Bg = Bruguiera gymnorrhiza , Acgymnor = Aegicerasrhiza, Ac corniculatum = Aegiceras, Kocorniculatum = Kandelia, Ko obovata = Kandelia, Rs = Rhizophoraobovata, Rs stylosa= Rhizophora, Am = stylosaAvicennia, Ammarina = ) (AAvicennia) 30% canopy marina closure) (A) 30% and highcanopy intertidal closure elevation, and high ( Bintertidal) 60% canopy elevation, closure (B) and 60% high canopy intertidal elevationclosure and (C) high 90% intertidal canopy closure elevation and (C high) 90% intertidal canopy closure elevation, and (highD) 30% intertidal canopy elevation, closure ( andD) low intertidal30% canopy elevation, closure (E )and 60% low canopy intertidal closure elevation, and low ( intertidalE) 60% canopy elevation, closure (F) 90%and canopylow intertidal closure and lowelevation, intertidal (F) elevation. 90% canopy closure and low intertidal elevation. 3.2. Seedling Morphological Features and Growth Rates 3.2. Seedling Morphological Features and Growth Rates Both intertidal elevation and light level had significant effects on the stem height, leaf number, and stemBoth diameter intertidal (Table elevation2). The and stem light height level differed had significant significantly effects among on the intertidal stem height, elevations leaf and lightnumber, levels and (Table stem2). diameter The annual (Table cumulative 2). The stem increase height in thediffered stem significantly height at low among intertidal intertidal elevation waselevations generally and high light at levels the same (Table light 2). level. The annual The stem cumulative height in increase the understory in the stem of 30% height canopy at low closure wasintertidal the highest elevation irrespective was generally of intertidal high elevation. at the sameWe found light that level. the stemThe stem height height of B. gymnorrhiza in the , A.understory corniculatum of, and 30%A. canopy marina under closure 30% was canopy the highest closure irrespective in high tide beachof intertidal was lower elevation. than that We under found that the stem height of B. gymnorrhiza, A. corniculatum, and A. marina under 30% canopy closure in high tide beach was lower than that under 60% canopy closure in low tide beach, respectively. Conversely, the stem height of R. stylosa under 30% canopy closure was higher than that under 60% canopy closure. The highest stem height of B. gymnorrhiza, K. obovata, R. stylosa, A. corniculatum, and A. marina under 30% canopy closure was 63.79, 56.32, 54.34, 42.13, and 41.67 cm, which was 36.22%, 85.31%, 30.21%, 53.62%, and 31.45% higher than that under 90% canopy closure at low intertidal elevation, respectively. The relative growth of B. gymnorrhiza decreased with time after 120 days, whereas the other species tended to grow steadily after 180 days (Figure 3).

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60% canopy55 closure in low tide beach, respectively.55 Conversely, the stem height of R. stylosa under 30% canopy50 closure was higher than that under 60%50 canopy closure. The highest stem height of B. gymnorrhiza45 , K. obovata, R. stylosa, A. corniculatum45, and A. marina under 30% canopy closure was 63.79,40 56.32, 54.34, 42.13, and 41.67 cm, which was 36.22%,40 85.31%, 30.21%, 53.62%, and 31.45% higher than that35 under 90% canopy closure at low intertidal35 elevation, respectively. The relative growth of 30 30 B. gymnorrhiza decreasedAc with time after 120 days, whereas the other species tended to grow steadily after 18025 days (FigureAm 3). 25 Bg The20 increaseKo in leaf number among the species20 was significantly different at different light Rs intensities,15 and A. corniculatum presented a significant15 difference in leaf number at different intertidal elevations (Table0 260). Bruguiera120 180 gymnorrhiza240 300and360R. stylosa at high0 intertidal60 120 elevation180 240 generally300 360 presented Time(day) Time(day) relatively high leaf numbers, whereas K. obovata and A. marina showed a reverse tendency. The number C F of A. corniculatum differed marginally between 30% and 60% canopy closure but declined sharply underFig 90%ure canopy. 2. The closurenumber irrespective of seedlings of of the intertidal five mangrove elevation. species The surviving relativegrowth (Bg = Bruguiera of K. obovata and B. gymnorrhizagymnorrhizadecreased, Ac = Aegiceras rapidly corniculatum with time after, Ko = 120 Kandelia days, obovat and thea, Rs other = Rhizophora species tended stylosa, toAm grow = steadily duringAvicennia the same marina period) (A (Figure) 30% 4 canopy). closure and high intertidal elevation, (B) 60% canopy Theclosure stem and diameter high intertidal of B. gymnorrhiza elevation (C, K.) 90% obovata canopy, and closureA. corniculatum and high intertidaldiffered elevation, significantly (D) between light level,30% canopy and high closure canopy and closure low intertidal decreased elevation, the increase (E) 60% in canopy stem diameter closure and at low low and intertidal high elevations. The stemelevation, diameter (F) 90% of canopyR. stylosa closurewas and generally low intertidal higher elevation. at high intertidal elevations, approximately 1.34 times higher than that at the low intertidal elevations. Furthermore, A. marina was not significantly 3.2. Seedling Morphological Features and Growth Rates affected by intertidal elevation and light level (Table2). The relative growth of B. gymnorrhiza was the highestBoth under intertidal 30% canopy elevation closure. and The light growth level had of all significant the species effects showed on a the decreasing stem height, trend leaf initially andnumber, then increasedand stem withdiameter better (Table performance 2). The stem at low height intertidal differed elevations significantly (Figure among5). intertidal elevations and light levels (Table 2). The annual cumulative increase in the stem height at low intertidalTable 2. elevationF values of was two-way generally ANOVA high tests at indicating the same the differences light level. in morphological The stem height parameters in the in understoryvarying light of 30% levels canopy and intertidal closure elevation was the among highest different irrespective mangrove of species. intertidal elevation. We

found that the stem heightLight Levels of B. gymnorrhiza, IntertidalA. corniculat Elevationum, and A. Light marina Levels under× Intertidal 30% Elevation canopy closureSpecies in high Stemtide beachLeaf was lowerSteam thanStem that underLeaf 60%Steam canopy Stemclosure in Leaflow tide Steambeach, respectively. Conversely,Height Number the stemDiameter heightHeight of R. stylosaNumber underDiameter 30% canopyHeight closureNumber wasDiameter higher than thatAc under 112 60% *** canopy 12.7 *** closure. 4.38 * The 63.6 highest *** 23.0 stem *** height 33.3 *** of B. 41.6 gymnorrhiza *** 2.83,NS K. obovata0.35 NS, R. Am 39.2 *** 30.3 *** 3.92 * 22.2 *** 1.63 NS 2.22 NS 50.9 *** 1.46 NS 2.42 NS stylosa, A.Bg corniculatum 85.2 ***, 51.5and *** A. marina3.13 NS under21.3 ***30% 0.24canopyNS 42.05closure *** was 30.6 63.79, *** 56.32,0.32 NS 54.34,1.45 42.13,NS and 41.67Ko cm, which 276 *** was 43.1 36.22%, *** 0.98 85.31%,NS 36.5 30.21%, *** 2.55 53.62%,NS 27.3 and *** 31.45% 65.8 ***higher0.19 thanNS that0.26 underNS Rs 26.7 *** 78.8 *** 13.0 *** 34.2 *** 5.32 NS 2.14 NS 21.1 *** 7.01 * 0.86 NS 90% canopy closure at low intertidal elevation, respectively. The relative growth of B. Note: NS means not significant at p > 0.05 (n = 54). *** Statistical significance at p < 0.001, * Statistical significance gymnorrhizaat p < 0.05. decreased Ac = Aegiceras with corniculatum time after, Am = 120Avicennia days, marina whereas, Bg = Bruguiera the other gymnorrhiza species, Ko tended = Kandelia to obovata grow , steadilyRs = Rhizophora after 180 stylosa days. (Figure 3).

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FigureFigure 3. . The3. The steam steam height height increment increment of seedlings of seedlings of the of five the mangrove five mangrove species species (Bg = Bruguiera(Bg = gymnorrhizaBruguiera, Ac gymnor = Aegicerasrhiza, Ac corniculatum = Aegiceras, Ko corniculatum = Kandelia obovata, Ko =, RsKandelia = Rhizophora obovata stylosa, Rs =, Am=RhizophoraAvicennia marinastylosa)(A, Am=) 30% Avicennia canopy closuremarina) and(A) 30% high canopy intertidal closure elevation, and high (B) intertidal 60% canopy elevation, closure (B and) 60% high intertidalcanopy elevation closure (andC) 90% high canopy intertidal closure elevation and high (C intertidal) 90% canopy elevation, closure (D) 30%and canopyhigh intertidal closure and lowelevation, intertidal ( elevation,D) 30% canopy (E) 60% closure canopy and closure low intertidal and low intertidalelevation, elevation, (E) 60% canopy (F) 90% closure canopy and closure andlow low intertidal intertidal elevation, elevation. (F) 90% canopy closure and low intertidal elevation.

Table 2. F values of two-way ANOVA tests indicating the differences in morphological parameters in varying light levels and intertidal elevation among different mangrove species.

Light levels × Intertidal Light levels Intertidal elevation elevation Species Steam Stem Leaf Steam Stem Leaf Steam Stem Leaf diamete height number diameter height number diameter height number r Ac 112*** 12.7*** 4.38* 63.6*** 23.0*** 33.3*** 41.6*** 2.83 NS 0.35 NS Am 39.2*** 30.3*** 3.92* 22.2*** 1.63 NS 2.22 NS 50.9*** 1.46 NS 2.42 NS Bg 85.2*** 51.5*** 3.13 NS 21.3*** 0.24 NS 42.05*** 30.6 *** 0.32 NS 1.45 NS Ko 276*** 43.1*** 0.98 NS 36.5*** 2.55 NS 27.3*** 65.8*** 0.19 NS 0.26 NS Rs 26.7*** 78.8*** 13.0*** 34.2*** 5.32 NS 2.14 NS 21.1 *** 7.01* 0.86 NS Note: NS means not significant at p > 0.05 (n = 54). *** Statistical significance at p < 0.001, * Statistical significance at p < 0.05. Ac = Aegiceras corniculatum, Am= Avicennia marina, Bg = Bruguiera gymnorrhiza, Ko = Kandelia obovata, Rs = Rhizophora stylosa.

The increase in leaf number among the species was significantly different at different light intensities, and A. corniculatum presented a significant difference in leaf number at different intertidal elevations (Table 2). Bruguiera gymnorrhiza and R. stylosa at high intertidal elevation generally presented relatively high leaf numbers, whereas K. obovata and A. marina showed a reverse tendency. The number of A. corniculatum differed marginally between 30% and 60% canopy closure but declined sharply under 90% canopy closure irrespective of Forests 2019, 10, 83 8 of 15

intertidal elevation. The relative growth of K. obovata and B. gymnorrhiza decreased rapidly Forests 2019, 10, 83 8 of 13 with time after 120 days, and the other species tended to grow steadily during the same period (Figure 4). 7 7 Bg Ko 6 6 Ac Am 5 5 Rs 4 4

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0 0 60 120 180 240 300 360 60 120 180 240 300 360 A D 7 7 6 6 5 5 4 4 3 3

Leaf number Leaf 2 2 1 1 0 0 60 120 180 240 300 360 60 120 180 240 300 360 B E 7 7 6 6 5 5 4 4 3 3 2 2 1 1 0 0 60 120 180 240 300 360 60 120 180 240 300 360 Time(day) Time(day) C F

FigureFigure 4. .The 4. The leaf number leaf number of seedlings of seedlings of the fiveof the mangrove five mangrove species (Bg species = Bruguiera (Bg = Bruguiera gymnorrhiza , Acgymnor = Aegicerasrhiza, corniculatum Ac = Aegiceras, Ko corniculatum = Kandelia obovata, Ko = Kandelia, Rs = Rhizophora obovata, Rs stylosa = Rhizophora, Am = Avicennia stylosa, Am marina = ) (A)Avicennia 30% canopy marina closure) (A) and 30% high canopy intertidal closure elevation, and high (B )intertidal 60% canopy elevation, closure ( andB) 60% high canopy intertidal elevationclosure ( Cand) 90% high canopy intertidal closure elevation and high(C) 90% intertidal canopy elevation,closure and (D high) 30% intertidal canopy elevation, closure and (D) low intertidal30% canopy elevation, closure (E) 60%and canopylow intertidal closure elevation, and low intertidal (E) 60% elevation,canopy closure (F) 90% and canopy low intertidal closure and lowelevation, intertidal ( elevation.F) 90% canopy closure and low intertidal elevation. A significant interactive effect of intertidal elevation and light intensity on the RGR was observed. The stem diameter of B. gymnorrhiza, K. obovata, and A. corniculatum differed significantly The RGR of all the species significantly decreased with the decrease in light intensity. Bruguiera between light level, and high canopy closure decreased the increase in stem diameter at low gymnorrhiza, K. obovata, and R. stylosa at high intertidal elevation presented higher RGR, whereas and high elevations. The stem diameter of R. stylosa was generally higher at high intertidal A. corniculatum and A. marina showed better performance at low intertidal elevation under 30% and elevations, approximately 1.34 times higher than that at the low intertidal elevations. 60% canopy closure. The RGR of K. obovata, A. corniculatum, and A. marina was significantly affected Furthermore, A. marina was not significantly affected by intertidal elevation and light level under 90% canopy closure at high and low intertidal elevations (Table3). (Table 2). The relative growth of B. gymnorrhiza was the highest under 30% canopy closure. The growth of all the species showed a decreasing trend initially and then increased with better performance at low intertidal elevations (Figure 5). Forests 2019, 10, 83 9 of 13

0.16 0.16

0.12 0.12

0.08 0.08

0.04 0.04

0 0 60 120 180 240 300 360 60 120 180 240 300 360 A D 0.16 0.16

） 0.12 0.12 mm （ 0.08 0.08

0.04 0.04 Stem diameter Stem

0 0 60 120 180 240 300 360 60 120 180 240 300 360 B E 0.16 0.16

0.12 0.12

0.08 0.08

Bg 0.04 Ko 0.04 Ac Am 0 Rs 0 60 120 180 240 300 360 60 120 180 240 300 360 Time(day) Time(day) C F

FigureFigure 5. .The 5. The stem stem diameter diameter of seedlings of seedlings of the offive the mangrove five mangrove species (Bg species = Bruguiera (Bg = Bruguiera gymnorrhiza , Acgymnor = Aegicerasrhiza, corniculatumAc = Aegiceras, Ko corniculatum = Kandelia, obovata Ko = Kandelia, Rs = Rhizophora obovata Rs stylosa = Rhizophora, Am = Avicenniastylosa Am= marina ) (A)Avicennia 30% canopy marina closure) (A) and30% high canopy intertidal closure elevation, and high (B )intertidal 60% canopy elevation, closure (B and) 60% high canopy intertidal elevationclosure (andC) 90% high canopy intertidal closure elevation and ( highC) 90% intertidal canopy elevation,closure and (D high) 30% intertidal canopy elevation, closure and (D) low intertidal30% canopy elevation, closure (E) 60%and canopylow intertidal closure elevation, and low intertidal(E) 60% canopy elevation, closure (F) 90% and canopy low intertidal closure and lowelevation, intertidal (F elevation.) 90% canopy closure and low intertidal elevation.

−1 -1−1 -1 TableTable 3. The 3. The relative relative growth growth rate (RGR,rate (RGR, mean mean± SE) ± (mg SE) g(mgday g day) of) fiveof five mangrove mangrove species species planted in varyingplanted lightin varying level andlight intertidal level and elevation. intertidal elevation.

Species HL andHL 30%and CC HLHL and and 60% CC HLHL and and 90% CC LL andLL and 30% CC LLLL and and 60% CC LLLL and and 90% CC Species Bg 223.230%± CC43.5a 184.660%± CC32.4b 144.390%± CC25.3c 207.630%± CC35.4a 190.360% ±CC26.3b 152.490% CC± 24.3c KoBg 172.3223.2±43.5a± 23.6a 184.6±32.4b 98.3 ± 18.5b 144.3±25.3c 54.7 ± 9.7c 207.6±35.4a 166.4 ± 21.3a 190.3±26.3b 102.3 ± 24.5b 152.4±24.3c 62.5 ± 12.6c AcKo 122.3172.3±23.6a± 31.2b 101.398.3±18.5b± 26.4c 64.454.7±9.7c± 15.4d 166.4±21.3a 142.3 ± 21.7a 102.3±24.5b 120.4 ± 21.2b 62.5±12.6c 87.3 ± 13.4d RsAc 167.4122.3±31.2b± 32.4a 143.4101.3±26.4c± 17.6b 103.464.4±15.4d± 20.3c 142.3±21.7a 151.3 ± 25.3b 120.4±21.2b 139.5 ± 19.4b 87.3±13.4d 87.3 ± 16.3d ± ± ± ± ± ± AmRs 87.32167.4±32.417.3ba 143.4±17.6 52.4 12.6cb 103.4±20.3c 40.5 8.3c 151.3±25.3 136.4 13.2ab 139.5±19.4b 125.4 26.3a 87.3±16.3 90.3 22.1bd AmNote: Values87.32±17.3b with different letters52.4±12.6c mean statistical40.5±8.3c significant differences136.4±13.2a at 0.05 level among125.4±26.3a treatments. 90.3±22.1bHL = High intertidal level, LL = Low intertidal level, 30% CC = 30% canopy closure, 60% CC = 60% canopy closure, 90% Note: Values with different letters mean statistical significant differences at 0.05 level among CC = 90% canopy closure, respectively. Ac = Aegiceras corniculatum, Am = Avicennia marina, Bg = Bruguiera gymnorrhizatreatments., Ko =HL=HighKandelia obovata intertidal, Rs = level,Rhizophora LL=Low stylosa intertidal. level, 30% CC=30% canopy closure, 60% CC=60% canopy closure, 90% CC=90% canopy closure, respectively. Ac = Aegiceras Forests 2019, 10, 83 10 of 13

4. Discussion

4.1. Seedling Survival in the Understory The survival rate of mangrove species seedlings in a mangrove forest is primarily driven by the habitat structure [21]. Mangroves have an interspecific difference in tolerance limits to shading and intertidal position at the early stage [22,23]. The survival rate of four mangrove species, namely, A. marina, B. gymnorrhiza, C. tagal, and R. stylosa, was higher at high intertidal elevation than at low intertidal elevation, irrespective of the light level, and the seedlings survived better in light gaps than under the canopy in the high intertidal position [18]. In the present study, A. corniculatum, A. marina, and R. stylosa were relatively more sensitive at low intertidal elevation, whereas K. obovata exhibited better performance at low intertidal elevation. Rhizophora stylosa, B. gymnorrhiza, and K. obovata survived better than the other two species during the first two months, which may be related to their bigger hypocotyls [24]. Bruguiera gymnorhiza and K. obovata presented higher survival rate under low light irradiance condition than A. corniculatum in S. apetala plantations [25]. We also found that B. gymnorrhiza and K. obovata had higher survival rates than the other species under 90% canopy closure. Overall B. gymnorrhiza performed best in low intertidal position and under low light irradiance condition throughout the study.

4.2. Early Growth Response of Seedlings to Light Level A 12-month study showed that B. gymnorrhiza was the most stable and exhibited an adaptive response to low light condition, followed by K. obovata and A. corniculatum in the understory of S. apetala plantations in China [25]. The height of R. apiculata and Bruguiera cylindrica (L.)Bl. in the gaps was more than 2 and 5 times higher than that in the canopy, respectively [26]. The seedlings of B. gymnorrhiza and K. obovata under the canopy had lower leaf number and stem basal diameter than those in the gaps [27,28]. Similarly, Chen et al. reported that the leaf number and stem basal diameter of A. marina were higher in the gaps than in the canopy, indicating that A. marina seedlings might be shade-intolerant [29]. The results of the present study conducted in S. apetala plantations grown at different light levels under field conditions confirm these previous findings. It has been reported that the RGR of R. apiculata and B. gymnorrhiza decreased with decrease in irradiance from full sunlight to canopy shade environment [30]. In the present study, the RGR of K. obovata, A. corniculatum, and A. marina was significantly affected by the low light level regardless of the intertidal elevation, indicating light level is the main limiting factor affecting early biomass accumulation in seedlings.

4.3. Responses to Intertidal Elevation High tidal inundations stimulated the early growth of seven mangrove species, especially the stem height [31]. It has been reported that the stem height of Laguncularia racemosa (L.) Gaertn. f. seedlings was considerably higher under tidal flooding than under no flooding condition [32]. Similarly, recent studies on growth and physiology have shown that A. marina seedlings are tolerant to low intertidal elevation, but not to canopy shade [29]. A growth trial with five native mangrove species also supported such a pattern. The leaf number of K. obovata [20] and A. marina [29] seedlings increased significantly with water level, which is consistent with the observations of the present study, mainly in K. obovata and A. marina seedlings. We also found the seedlings of K. obovata and A. marina at the low intertidal elevation improved their ability to capture light energy by increasing the stem height to adapt to flooding stimulation and increased leaf number to increase the ability to capture light energy. In a present study, all species presented higher stem height at the low intertidal position, and the stem height growth exhibited no particular trend with waterlogging from seedlings to 300-day-old Forests 2019, 10, 83 11 of 13 plants. This is similar to the findings of Hovenden et al. [33], who reported that the stem height of A. marina did not change significantly with flooding after the seedlings were 12-month old. The present study showed that the RGR of B. gymnorrhiza, K. obovata, and R. stylosa was significantly enhanced by high inundation elevation, especially at high light level, whereas A. corniculatum and A. marina showed better performance at low intertidal elevation under 30% and 60% canopy closure. In another study, the seedlings of A. marina presented higher RGR at lower intertidal elevation, and B. gymnorrhiza and R. stylosa seedlings showed negligible disparity between eight different tidal flat elevations [32]. A previous study in Hong Kong showed that K. obovata had stronger resilience to high intertidal elevation than B. gymnorrhiza [34].

4.4. Interactive Effects of Intertidal Elevation and Light Level Grime reported that morphological plasticity of plants is closely related to the individual’s ability to exploit habitats [35]. The relative growth of R. stylosa, A. marina, and C. tagal was higher at the high intertidal elevation than at the low intertidal elevation. Moreover, it was higher in gaps than in the canopy. The growth of B. gymnorrhiza was the highest under all conditions [18]. The specific leaf area of B. gymnorrhiza (71.0 ± 2.8 cm2 g−1) were significantly different from that of R. stylosa (45.4 ± 1.0 cm2 g−1) and K. obovata (48.6 ± 0.8 cm2 g−1), which may be related to the fact that B. gymnorrhiza can tolerate shaded conditions better than the other species [36]. The results showed that the survival of all five species studied and the growth of three species (A. corniculatum, A. marina, and R. stylosa) were high under adverse conditions. Moreover, B. gymnorrhiza showed the best performance in the six interactive treatments.

4.5. Turning Monocultures to Mixed Forests Species diversity and structural complexity are important factors that enhance both ecosystem productivity and stability [37]. A previous study showed successful recruitment of natural mangrove species into artificial mangrove monocultures in Kenya. Bosire et al. confirmed that mixed stands of plantations with natural mangrove species are achievable [38]. Furthermore, Ren et al. [14] reported that the native species A. marina, A. corniculatum, K. obovata, and R. stylosa can occupy the understory of 4 to 10-year old S. apetala plantations in Leizhou Peninsula of Southern China. These studies proved the possibility of establishing mixed forests using native species under introduced species. Our study results also demonstrated the adaptability of different mangrove species to intertidal elevation and light intensity. Light gaps in mangrove forests are often created by episodic events such as violent wind storms [39], lightning strikes [40], and single tree falls [41]. Two ways to achieve stable mixed forests are as follows: (1) planting propagules of A. corniculatum, A. marina, and R. stylosa two times at low intertidal position, and (2) choosing natural gaps or thinning the canopy of S. apetala plantations with tree pruners at high intertidal position.

5. Conclusions The adaptability to light levels and intertidal elevations of five native mangrove species in China was explored in a 12-month field experiment. Although the seedlings of all five native species survived better at high intertidal elevation, the stem height of all species at low intertidal elevation was higher than that at high intertidal elevation, and it was the highest under 30% canopy closure. The RGR was the highest at low intertidal elevation, and it was promoted by high light level. The survival rate and growth rate of B. gymnorrhiza were the highest across intertidal elevations and light levels. Bruguiera gymnorrhiza was the best acclimated native species in S. apetala plantations in the study area. Simultaneously, periodical thinning of canopy artificially in the dense canopies of S. apetala plantations is an effective measure. In addition, increasing the planting density of seedlings would promote the establishment and growth of native species especially at low intertidal elevations. Forests 2019, 10, 83 12 of 13

Author Contributions: B.L. conceived the idea and Y.X. designed the experiment; Z.J., W.G., M.L. and Y.C. carried out field and laboratory analyses; Z.J. wrote the manuscript and Y.X. helped with the revision. Acknowledgments: This work was supported by the National Natural Science Foundation of China (grant numbers 41676080, 41876094); the National Key Research and Development Program of China (2017YFC0506103). We are grateful to Shuping Ding for establishment of the experimental plots and for data collection in Qi’ao Island. Conflicts of Interest: The authors declare no conflict of interest.

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