Article Germination of cinnabari Balf.f. Seeds under Controlled Temperature Conditions

Lucie Bauerová 1, Shiferaw Alem Munie 1, KateˇrinaHoušková 2 and Hana Habrová 1,*

1 Department of Forest Botany, Dendrology and Geobiocoenology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemˇedˇelská 1, 613 00 Brno, Czech Republic; [email protected] (L.B.); [email protected] (S.A.M.) 2 Department of Silviculture, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemˇedˇelská 1, 613 00 Brno, Czech Republic; [email protected] * Correspondence: [email protected]; Tel.: +420-545134555; Fax: +420-545212293

 Received: 14 April 2020; Accepted: 4 May 2020; Published: 6 May 2020 

Abstract: Research highlights: This study is focused on the germination of Dracaena cinnabari seeds in order to discover the possibility of natural and artificial regeneration of this species. Background and Objectives: This study aimed to determine the optimal temperature for D. cinnabari seed germination, e.g., the temperature at which the germination percentage and germination rate (vitality) are the highest. The objectives of this study are to: (1) determine the optimal temperature for the germination of D. cinnabari seeds, (2) compare the suitability of different seed collection methods, and (3) compare the germination parameters of seeds that were collected from different localities. The results of this study will contribute to obtaining the highest number of seedlings from limited seed material for reforestation of the most endangered localities of D. cinnabari species. Materials and methods: Four seed sections were employed. These sections were directly collected from either the fruits of a cut panicle or the ground and were obtained from different localities that differ in altitude. The seeds were tested in a greenhouse while using Petri dishes at three different temperatures—22, 26, and 30 ◦C—with four replicates of 25 seeds of each section. ANOVA and the t-test were employed for data analysis. Results: The highest germination percentages (GPs) were achieved at 26 ◦C and 30 ◦C, which were 84.6% and 82.5%, respectively. The ANOVA and t-test results showed that the germination index (GI) of the species was relatively higher at a temperature of 30 ◦C relative to that at other temperatures in the study. Although seeds that were collected from the tree achieved a higher GP, the t-test result showed no significant differences in the GI of D. cinnabari seeds that were collected from the ground and from the tree (p > 0.05). Overall, the findings of this study show that temperature has substantial influence on the germination of seeds of D. cinnabari. Therefore, we recommend a temperature of 30 ◦C to facilitate the germination of D. cinnabari, as it achieved the highest GI at this temperature relative to that at the other temperatures (22 ◦C, 26 ◦C) applied in this study.

Keywords: dragon’s blood tree; ; regeneration; germination percentage; mean germination time; germination index

1. Introduction The Monocotyledonous Dracaena species, especially the members of the dragon tree group [1], are rare species with a limited and often scattered distribution, very limited natural regeneration, and usually very small populations. Among the different Dracaena species, Dracaena cinnabari Balf.f., which is endemic to Socotra Island, has a large population with an unbalanced age structure [2]. Eighty-thousand individuals are distributed along the eastern part of the island [3,4]; most of them have over mature individuals [5], according to previous studies.

Forests 2020, 11, 521; doi:10.3390/f11050521 www.mdpi.com/journal/forests Forests 2020, 11, 521 2 of 14

Some of the localities, such as Qatariyah, with the last few trees (localities number 11 and 16 according to Madˇeraet al. [4]) require urgent intervention to prevent the loss of genetic variability and unique genotype features, as well as other species that are associated with the trees [6,7]. The trees on the whole island do not have a problem of flowering or producing seeds when compared with, e.g., D. serrulata Baker, which flowers, according to observations, mainly after exceptional rain events [8]. D. cinnabari usually flowers each year, at least for the majority of the individuals. Artificial regeneration would be an important practice for supporting natural regeneration, which is lacking due to overgrazing and possibly climate change [9–13]. For successful regeneration, obtaining the highest number of seeds with the highest possible germination percentage is very important. Unfortunately, information regarding the collection of D. cinnabari or Draceana sp. seeds, their handling and processing, and the suitable conditions for germination are lacking [14]. Some researchers reached low germination percentage (35%) of D. cinnabari seeds [15], others described germinated D. cinnabari seeds only after some pre-sowing treatment [16]. These weak germination results prompt the question of whether seeds are dormant or not. Seed dormancy delays or inhibits germination, and some studies, for example, Marrero et Almeida [17] consider non-germinated seeds of D. tamaranae Marrero Rodr., R.S. Almeira and M. Gonzáles-Martin as probably dormant. However, some findings showed a relatively high germination percentage (77%) of D. draco L. seeds [16] or of D. cinnabari seeds (78% and 90%) [18] without any pre-sowing treatment. Using different growth hormones to facilitate seed germination might not also be successful, and some studies, for example Chan-Chin et Govinden-Soulange [19] did not obtain a higher germination percentage of seeds after gibberellic acid and butenolid application for D. concinna Kunth as compared with non-treated seeds. These findings indicate that any pre-sowing treatment might not be necessary. Seeds must be exposed to suitable conditions to germinate. Temperature is one of the most important external factors for seed germination under natural and laboratory conditions [20,21], which means that a suitable temperature range has to be identified. Some studies confirmed that temperature highly influences the seed germination of different species, including Dracaena sp. For example, Chan-Chin et Govinden-Soulange [19] compared the germination of D. concinna seeds under different temperature conditions (15–35 ◦C) and obtained the highest germination percentage for a temperature of 25 ◦C. A high germination percentage have been reached at 20 ◦C by Hubálková et al. [18] for D. cinnabari seeds, and by Monteiro et al. [22] and Adolt [16] for D. draco seeds. Conversely, the results of Adolt [16] and Chan-Chin et Govinden-Soulange [19] show a low germination percentage of D. cinnabari and D. concinna at the same temperature of 20 ◦C. None of the seeds of D. concinna germinated at 15 ◦C[19], and none of the seeds of D. draco germinated at alternating temperatures of 10 ◦C and 20 ◦C[22]. These and other similar studies show that each species requires a different temperature for the seeds to germinate. D. cinnabari belongs to the tropical species, for which 25–35 ◦C would be the optimum temperature for germination [23]. Therefore, studies on the impact of various temperatures on the germination of D. cinnabari are lacking. The results of previous studies are hardly ever comparable, not only due to the use of other Dracaena species but also to the different origins, times, and methods of collection; other methods of handling, processing, and storage of seeds; and, different media for the germination test. As a result, this study has focused on determining the optimal temperature for D. cinnabari seed germination, i.e., a temperature at which the germination rate, germination percentage, and germination index are the highest. The objectives of this study are to: (1) determine the optimal temperature for the germination of D. cinnabari seeds, (2) evaluate the effect of seed collection methods on the germination of D. cinnabari, and (3) compare the germination parameters of seeds of different origin. All of the results will contribute to obtaining the most seedlings from limited seed material from the most endangered localities of D. cinnabari. Forests 2020, 11, 521 3 of 14

2. Materials and Methods

2.1. Seed Collection The seeds were collected in three different localities by two different methods. (1) SB—the seeds were collected from the ground under 10 nearby trees (area of about 0.3 ha) in the Firmihin locality. Seeds without fruit pulp were collected from the ground in October 2014. The Firmihin locality has an elevation of approximately 650 m a.s.l. and is characterised by a mean annual temperature of 23.6 ◦C with a maximum daily mean of 27.4 ◦C at the end of April and beginning of May, as well as a decrease in the minimum daily mean of 21.4 ◦C at the end of January and beginning of February according to data from the Czech climatic station in the Firmihin locality at an altitude of 440 m a.s.l. between 2000 and 2009. (2) PL—seeds were directly collected from one tree by cutting one panicle of ripe fruits in Firmihin in the same locality as SB seeds in October 2014. Whole fruits (Figure1a) were taken to the laboratory, and the seeds (Figure1b) were removed from the fruit. We also counted the total number of fruits in Forests 2020, 11, x FOR PEER REVIEW 4 of 14 this panicle and the number of seeds in individual fruits (Figure2a).

(a) (b)

Figure 1. Fruits ( a)) and and seeds ( b) of Dracaena cinnabari.

(3) NN—seeds were collected directly from trees by picking individual ripe fruits (area of about 0.7 ha) in the Sirhin locality at an elevation of 850 m a.s.l. in September 2014. The mean annual temperature at the climate station with a similar altitude reaches 22.0 ◦C with a daily mean maximum temperature of 22.6 ◦C and a daily mean minimum temperature of 18.9 ◦C, according to our data. The fruits were carefully dried to make them lose their moisture for the purpose of reducing fungi attack and to increase their storability, and then, the seeds were removed. (4) PE—seeds were collected directly from trees by cutting more panicles (area of about 0.2 ha) in the Skant locality at an elevation of 1400 m a.s.l. in December 2014. The mean annual temperature from the climate station in Skant at an altitude of 1440 m a.s.l. reaches 17.5 ◦C with a daily mean maximum temperature of 22.2 ◦C and a daily mean minimum temperature of 12.6 ◦C, according to our data. The seeds were removed from the fruits a few days after the collection and then taken to the laboratory. All of the seeds were placed in plastic bags and stored in the laboratory at ordinary (not controlled) temperatures, that ranged between 20–25 ◦C, until the experiment was started.

(a) (b)

Figure 2. Example of three-seed fruit (a), and germinating seeds on cotton swabs (b).

2.3. Data Analysis For data analysis, the statistical software program SigmaPlot 13 (Systat Software, Inc., San Jose, CA, USA) was utilised. In the data analysis, a parametric method of analysis was performed, as all the germination data were normally distributed. One-way ANOVA was conducted for a comparison of the final mean seed germination percentage (GP), mean germination time (MGT), and mean germination index (GI) of the seeds collected from the different localities and evaluated for their germination at different temperatures. The t-test was also performed for the data analysis. When a significant difference was observed, mean separation was performed while using Fisher's least significant difference (LSD) test with a significance level of p = 0.05. GP, MGT, and GI for the different temperature treatments applied to evaluate the seed germination of D. cinnabari seeds were analysed while using the following formulas: germination percentage (GP) was calculated using the formula Forests 2020, 11, x FOR PEER REVIEW 4 of 14

(a) (b)

Forests 2020, 11, 521 Figure 1. Fruits (a) and seeds (b) of Dracaena cinnabari. 4 of 14

(a) (b)

Figure 2. ExampleExample of of three-seed three-seed fruit ( a),), and and germinating seeds on cotton swabs (b).

2.3.2.2. Data Germination Analysis Experiment ForThe data germination analysis, experiment the statistical was software performed prog inram a university SigmaPlot laboratory 13 (Systat in Software, air-conditioned Inc., San cabinet Jose, CA,Climacell USA) 707was EVO utilised. at stable In the and data controlled analysis, temperatures a parametric ofmethod 22 ◦C (October–Novemberof analysis was performed, 2015), 26as ◦allC (January–Februarythe germination data 2015), were andnormally 30 ◦C distributed. (November–December One-way ANOVA 2015). Eachwas conducted of the experimental for a comparison studies wasof the performed final mean at di seedfferent germination temperatures percentage for 33 days. (GP), The mean seeds germination were germinated time in (MGT), Petri dishes and mean while germinationusing pieces index of cotton (GI) swabs of the as seeds a substrate collected (Figure from2 b),the bothdifferent at the localities bottom ofand the evaluated dish and for the their top germinationof the dish. Theat different filter paper temperatures. seemed to beThe an t-test insu wasfficient also substrate, performed as for it did the not data provide analysis. a su Whenfficient a significantamount of moisturedifference to thewas seeds observed, (due to mean the round separa shapetion andwas size performed of the seeds). while Four using replications Fisher's wereleast significantemployed fordifference each treatment (LSD) test (i.e., with each a significance seed section level and temperature);of p = 0.05. each replication had 25 seeds (i.e., totalGP, MGT, of 100 seeds).and GI Unfortunately, for the different for thetemperatur PE locality,e treatments a seed germination applied studyto evaluate at 26 ◦ Cthe was seed not germinationperformed, as of the D. seedscinnabari were seeds collected were lateranalysed than while other seeds.using the Atotal following of 400 formulas: seeds were employed for the germinationgermination studypercentage at temperatures (GP) was calculated of 22 ◦C andusing 30 the◦C, formula while 300 seeds were employed for the 26 ◦C temperature germination study. The seeds were watered and counted at least three times per week (usually on Monday, Wednesday, and Friday), and germinating seeds (Figure2b) were removed. Only distilled water was applied to retain moisture in the seeds. After the experiment, the ungerminated seeds at 26 ◦C underwent a Tetrazolium Chloride test to realise the viability of the seeds.

2.3. Data Analysis For data analysis, the statistical software program SigmaPlot 13 (Systat Software, Inc., San Jose, CA, USA) was utilised. In the data analysis, a parametric method of analysis was performed, as all the germination data were normally distributed. One-way ANOVA was conducted for a comparison of the final mean seed germination percentage (GP), mean germination time (MGT), and mean germination index (GI) of the seeds collected from the different localities and evaluated for their germination at different temperatures. The t-test was also performed for the data analysis. When a significant difference was observed, mean separation was performed while using Fisher’s least significant difference (LSD) test with a significance level of p = 0.05. GP, MGT, and GI for the different temperature treatments applied to evaluate the seed germination of D. cinnabari seeds were analysed while using the following formulas: Forests 2020, 11, 521 5 of 14

germination percentage (GP) was calculated using the formula

GP (%) = total number of seeds germinated/total number of sown seeds 100 (1) × The mean germination time (MGT) was calculated using the formula X X MGT (days) = (T1 n1 + T2 n2 + ... + Tk nk)/ (n1 + n2 + ... + nk) (2) × × × where—n = no. of newly germinated seeds, T = time from the beginning of the experiment Germination Index (GI) was calculated while using the formula X GI = (N1 T1 + N2 T2 + ... + Nk Tk) (3) × × × where—N = no. of newly germinated seeds on the first, second, and subsequent days and T = the weight given to the number of germinated seeds on the first, second, and subsequent days. In the GI, the maximum weight is given to seeds germinated on the first day and less to those that were germinated at subsequent dates [24].

3. Results

3.1. Number of Seeds in Individual Fruits We counted the number of fruits and seeds in individual fruits, as we achieved one whole panicle cut from a tree at Firmihin. The panicle contained 427 fruits: 92 fruits contained one seed, 194 fruits contained two seeds, and 141 fruits contained three seeds (Figure2a). Therefore, the panicle contained a total of 903 seeds. Thus, approximately 21.5%, 45.5%, and 33% of the fruits had one seed, two seeds and three seeds, respectively.

3.2. Germination

3.2.1. Effect of Temperature on Seed Germination Figure3 presents the results for the GP of the D. cinnabari seeds that were collected from the different localities, which were evaluated at different temperatures for their germination. The ANOVA results showed significant differences among the different temperatures in the GP of the seeds that were collected in the Sirhin (NN) locality (Figure3, p = 0.001). However, the ANOVA results for the GP of the seeds collected in the Firmihin (PL) locality, and then treated for their germination at temperatures of 22 ◦C, 26 ◦C, and 30 ◦C showed no significant differences (p = 0.087, Figure3). Similarly, the statistical analysis results revealed no significant differences in the GP of the seeds collected in the Skant (PE) locality, which were treated at a temperature of 22 ◦C, 26 ◦C, and 30 ◦C(p = 0.445, Figure3). Figure4 shows the ANOVA results for the e ffect of temperature (22 ◦C, 26 ◦C, and 30 ◦C) on the MGT of the D. cinnabari seeds that were collected from the different localities. The statistical analysis results revealed that the temperature applied as a treatment for germination has a significant effect on the MGT of the D. cinnabari seeds collected from the NN locality (p 0.001, Figure4). Similarly, ≤ the ANOVA results revealed significant differences in the MGT for the seeds collected from the PL locality and treated for their germination at temperatures of 22 ◦C and 30 ◦C and temperatures between 26 C and 30 C(p 0.001, Figure4). The statistical analysis results also indicated significant di fferences ◦ ◦ ≤ in the MGT of the seeds collected in the PE locality and treated for germination in temperatures between 22 C and 30 C(p 0.01, Figure4). ◦ ◦ ≤ ForestsForests 20202020,, 1111,, xx FORFOR PEERPEER REVIEWREVIEW 66 ofof 1414

3030 °C°C (Figure(Figure 5).5). TheThe statisticalstatistical analysesanalyses resultresult furtfurtherher indicatedindicated significantsignificant differencesdifferences inin thethe GIGI ofof Foreststhethe treatmentstreatments2020, 11, 521 betweenbetween 2222 °C°C andand 3030 °C.°C. 6 of 14

120120 p = 0.087 SeedsSeeds SeedsSeeds fromfromp = 0.087 SeedsSeeds fromfrom PEPE p < 0.001 fromfrom NNNN p < 0.001 PLPL localitylocality localitylocality 100100 localitylocality BB pp == 0.4450.445

8080 CC AA AA 6060

A A 4040 A A AA A

Germination percentage Germination A Germination percentage Germination 2020

00 2222 °C°C 2626 °C°C3030 °C°C 22 22 °C°C 2626 °C°C 3030 °C°C 2222 °C°C 3030 °C°C Temperature Temperature FigureFigureFigure 3. ANOVA3.3. ANOVAANOVA results resultsresults for comparison forfor comparisoncomparison of the eofofffect thethe of effect temperatureeffect ofof temperaturetemperature on the final onon germination thethe finalfinal percentagegerminationgermination (%)percentagepercentage of seeds collected (%)(%) ofof seedsseeds in the collectedcollected Sirhin (NN), inin thethe Firmihin SirhinSirhin (( (PL),NN),NN), andFirmihinFirmihin Skant (PL),(PL), (PE) localities.andand SkantSkant Means (PE)(PE) localities.localities. with the sameMeansMeans letterwithwith are thethe not samesame significantly letterletter areare not dinotff erentsignificsignific fromantlyantly each differentdifferent other ( fromfromp = 0.05). eacheach otherother ((pp == 0.05).0.05).

3030 SeedsSeeds fromfrom SeedsSeeds fromfrom PLPL localitylocality SeedsSeeds fromfrom PEPE NNNN localitylocality localitylocality 2525 CC pp << 0.0010.001 pp << 0.0010.001 pp << 0.0010.001 BB 2020 AA BB

1515 AA AA AA 1010 BB Mean germination time (days) time Mean germination Mean germination time (days) time Mean germination 55

00 2222 °C°C 2626 °C°C 3030 °C°C 2222 °C°C 2626 °C°C 3030 °C°C 2222 °C°C 3030 °C°C Temperature Temperature FigureFigureFigure 4. 4.4.ANOVA ANOVAANOVA results resultsresults for forfor comparison comparisoncomparison of ofof the thethe eff effecteffectect of ofof temperature temperaturetemperature on onon the thethe mean meanmean germination germinationgermination time timetime (days)(days)(days) of ofof seeds seedsseeds of ofofD. D.D. cinnabari cinnabaricinnabaricollected collectedcollected in inin the thethe Sirhin SirhinSirhin (NN), (NN),(NN), Firmihin FirmihFirmihinin (PL), (PL),(PL), and andand Skant SkantSkant (PE) (PE)(PE) localities. localities.localities. MeansMeansMeans with withwith the thethe same samesame letter letterletter are areare not notnot significantly significantlysignificantly di ffdifferentdifferenterent from fromfrom each eacheach other otherother (p (=(pp 0.05).== 0.05).0.05). Forests 2020, 11, 521 7 of 14

Figure5 presents the results for the e ffect of different temperatures on the GI of D. cinnabari seeds, which were collected from the different localities (NN, PL and PE). The ANOVA results showed significant differences in the GI of the D. cinnabari seeds that were collected from the NN locality, which were treated for their germination at temperatures of 22 C, 26 C, and 30 C(p 0.001, Figure5). ◦ ◦ ◦ ≤ The ANOVA results revealed no significant differences in their GI, for the seeds collected in the PL locality and treated for their germination at temperatures of 22 ◦C and 26 ◦C (Figure5), and significant differences in the GI for the treatments between 22 ◦C and 30 ◦C and between 26 ◦C and 30 ◦C (Figure5). TheForests statistical 2020, 11, x analyses FOR PEER resultREVIEW further indicated significant differences in the GI of the treatments7 of 14 between 22 ◦C and 30 ◦C.

600 Seeds from NN locality Seeds from PL locality Seeds from PE locality 500 p < 0.001 p < 0.001 C p = 0.039 B B 400

A 300 A A B

Germination index Germination 200

A 100

0 22 °C 26 °C 30 °C 22 °C 26 °C 30 °C 22 °C 30 °C Temperature FigureFigure 5. 5.ANOVA ANOVA results results for for comparison comparison of the of etheffect effect of temperature of temperature on the on germination the germination index ofindex seeds of collectedseeds collected in the Sirhin in the (NN),Sirhin Firmihin(NN), Firmihin (PL), and (PL), Skant and (PE)Skant localities. (PE) localities. Means Means with thewith same the same letter letter are notare significantly not significantly different different from eachfrom othereach other (p = 0.05). (p = 0.05).

3.2.2.3.2.2. E Effectffect of of Seed Seed Collection Collection Locality Locality on on Seed Seed Germination Germination FigureFigure6 presents6 presents the the statistical statistical analysis analysis results results for for the the GP, GP, MGT, MGT, and and GI GI of ofD. D. cinnabari cinnabariseeds seeds collectedcollected from from the the di differentfferent localities localities ((Sirhin ((Sirhin (NN), (NN), Firmihin Firmihin (PL), (PL), and and Skant Skant (PE)), (PE)), which which were were evaluatedevaluated for for their their germination germination under under a a similar similar temperature temperature condition. condition. The The ANOVA ANOVA results results revealed revealed significantsignificant di differencesfferences in in the the GP GP of ofD. D. cinnabari cinnabariseeds seeds collected collected from from the the NN, NN, PL, PL, and and PE PE localities, localities, which were treated for their germination at temperatures of 22 C(p 0.001, Figure6H) and 30 C which were treated for their germination at temperatures of 22 ◦°C (p ≤ 0.001, Figure 6H) and 30 °C◦ (p (p= =0.007,0.007, Figure Figure 6I).6I). The The ANOVA ANOVA results results also also indicated indicated significant significant differences di fferences in the in MGT the MGT of the of seeds the seedsof D. of cinnabariD. cinnabari fromfrom the thelocalities localities of NN, of NN, PL, PL, and and PE, PE, which which were were treated treated for for their their germination germination at at temperatures of 22 C(p 0.001, Figure6J) and 30 C(p = 0.001, Figure6K). The ANOVA results temperatures of 22 °C◦ (p ≤≤ 0.001, Figure 6J) and 30 ◦°C (p = 0.001, Figure 6K). The ANOVA results showedshowed significant significant di differencesfferences in in the the GI GI of of the theD. D. cinnabari cinnabariseeds seeds that that were were collected collected from from di differentfferent localitieslocalities and and evaluated evaluated for for their their germination germination at at 22 22◦ C(°C p(p= =0.008, 0.008, Figure Figure6 L),6L), while while no no significant significant didifferencesfferences in in the the GI GI for for the the seeds seeds of ofD. D. cinnabari cinnabaricollected collected from from di differentfferent localities localities and and assessed assessed for for theirtheir germination germination at at a a temperature temperature of of 30 30◦ C(°Cp (p= =0.861, 0.861, Figure Figure6 M).6M). Forests 2020, 11, x FOR PEER REVIEW 8 of 14

Forests 2020, 11, 521 8 of 14

600 GP 22 °C GP 30 °C MGT 22 °C MGT 30 °C GI 22 °C GI 30 °C a 500 p < 0.001 p = 0.007 p < 0.001 p < 0.001 p = 0.008 a

H I J K L 400 a a 300 a p = 0.861

200 b 100 b a c Germination percentage percentage Germination Mean time (days)germination index Germination M c c d b d a b a a b a 0 a

PL NN PE PL NN PE PL NN PE NN PE PL NN PE PL NN PE PL

Seed collection localities FigureFigure 6. 6.ANOVA ANOVA results results for comparisonfor comparison of the of e fftheects effects of seed of collectionseed collection localities localities/sources/sources (Sirhin (NN),(Sirhin Firmihin(NN), Firmihin (PL), and (PL), Skant and (PE)) Skant on the(PE)) germination on the germination percentage percentage (GP), mean (GP), germination mean germination time (MGT), time and(MGT), germination and germination index (GI) index of D. cinnabari(GI) of D.seeds. cinnabari Means seeds. with Means the same with letter the are same not significantlyletter are not disignificantlyfferent from eachdifferent other from (p = each0.05). other Figure (p 6= H0.05). and Figure I represent 6 H and GP atI represent 22 ◦C and GP 30 at◦ C22 temperature, °C and 30 °C respectively.temperature, Figure respectively.6 J and K representFigure 6 MGTJ and at K 22 re◦Cpresent and 30 MGT◦C temperature, at 22 °C and respectively. 30 °C temperature, Figure6L andrespectively. M represent Figure GI at 6 22 L ◦andC and M 30represent◦C temperature, GI at 22 °C respectively. and 30 °C temperature, respectively.

3.2.3. Germination of Seeds Collected from the Ground and Tree Crown 3.2.3. Germination of Seeds Collected from the Ground and Tree Crown Figure7, Figure8, and Figure9, present the t-test analysis results of the GP, MGT, and GI for Figure 7, Figure 8, and Figure 9, present the t-test analysis results of the GP, MGT, and GI for seeds of D. cinnabari collected in the Firmihin locality, from the ground (SB) and the tree crown seeds of D. cinnabari collected in the Firmihin locality, from the ground (SB) and the tree crown (PL), (PL), and subsequently evaluated for their germination at temperatures of 22 C, 26 C, and 30 C, and subsequently evaluated for their germination at temperatures of 22 °C,◦ 26 ◦°C, and 30◦ °C, respectively. The t-test analysis results revealed significant differences in the GP of seeds that were respectively. The t-test analysis results revealed significant differences in the GP of seeds that were collected from the ground and tree crown and subsequently evaluated for their germination at a collected from the ground and tree crown and subsequently evaluated for their germination at a temperature of 22 C(p = 0.04, Figure7). Similarly, the t-test results showed a significant difference in temperature of 22◦ °C (p = 0.04, Figure 7). Similarly, the t-test results showed a significant difference the GP of seeds collected from the ground and tree crown and then assessed for their germination in the GP of seeds collected from the ground and tree crown and then assessed for their germination at temperatures of 26 C(p = 0.015, Figure7) and 30 C(p = 0.020, Figure7). The results showed no at temperatures of 26◦ °C (p = 0.015, Figure 7) and 30◦ °C (p = 0.020, Figure 7). The results showed no significant differences in the MGT of the seeds that were collected from the ground and directly from significant differences in the MGT of the seeds that were collected from the ground and directly from the crown and evaluated for their germination at temperatures of 22 C(p = 0.19, Figure8), 26 C the crown and evaluated for their germination at temperatures of 22 °C◦ (p = 0.19, Figure 8), 26 °C◦ (p = (p = 0.996, Figure8) and 30 C(p = 0.096, Figure8). Similarly, the statistical analysis results showed 0.996, Figure 8) and 30 °C◦ (p = 0.096, Figure 8). Similarly, the statistical analysis results showed no no significant differences in the GI of seeds that were collected from the ground and the tree crown significant differences in the GI of seeds that were collected from the ground and the tree crown and and subsequently evaluated for their germination at temperatures of 22 C(p = 0.262, Figure9), 26 C subsequently evaluated for their germination at temperatures of 22 °C◦ (p = 0.262, Figure 9), 26 °C◦ (p = (p = 0.182, Figure9), and 30 C(p = 0.230, Figure9). 0.182, Figure 9), and 30 °C ◦(p = 0.230, Figure 9). Forests 2020, 11, x FOR PEER REVIEW 9 of 14 Forests 2020, 11, x FOR PEER REVIEW 9 of 14 Forests 2020, 11, 521 9 of 14

120 p = 0.04 p = 0.015 p = 0.020 120 22 °C 26 °C 30 °C p = 0.04 22 °C p = 0.015 26 °C p = 0.020 30 °C 100 B A B 100 B A B A 80 A 80 60

60 A B 40 A B

Germination percentage Germination 40

Germination percentage Germination 20 20 0 Seeds Seeds Seeds Seeds Seeds Seeds 0 in the in the in the in the in the Seeds Seeds Seeds Seeds Seeds inSeeds the ground tree ground tree ground in the in the in the in the in the intree the ground tree ground tree ground tree Seed Collection Method Seed Collection Method Figure 7. T-test results for the germination percentage of D. cinnabari seeds collected from the ground FigureandFigure directly 7. 7.t-test T-test from results results the forcrown for the the germinationand germination evaluated percentage percentagefor their germination of ofD. D. cinnabari cinnabari at seedstemperatures seeds collected collected of from 22from °C, the the26 ground °C,ground and and30and °C. directly directly Means from from with the thethe crown crownsame letter andand evaluated are not si gnificantlyfor thei theirr germination germination different from at at temperatures temperatureseach other (p of = of 220.05). 22 °C,◦ C,26 26°C,◦ andC, and30 30°C.◦ MeansC. Means with with the the same same letter letter are are not not significantly significantly different different from from each each other other (p (=p 0.05).= 0.05). 25 25 22 °C 26 °C 30 °C 22 °C 26 °C A 30 °C p = 0.19 p = 0.996 p = 0.096 20 A p = 0.19 p = 0.996 p = 0.096 20 A A 15 A 15 A A A A A A A 10 10

Mean germination time (days) time germination Mean 5

Mean germination time (days) time germination Mean 5

0 Seeds Seeds Seeds Seeds Seeds Seeds 0 inSeeds the inSeeds the inSeeds the inSeeds the in the in the ground tree ground tree Seeds Seeds in the in the in the in the groundin the intree the ground tree ground tree Seed Collection Method ground tree

Seed Collection Method Figure 8. t-test results for the mean germination time (MGT) of D. cinnabari seeds collected from the Figure 8. T-test results for the mean germination time (MGT) of D. cinnabari seeds collected from the ground and directly from the crown and evaluated for their germination at temperatures of 22 ◦C, groundFigure 8.and T-test directly results from for the the crown mean andgermination evaluated time for (MGT)their germination of D. cinnabari at temperatures seeds collected of 22from °C, the 26 26 ◦C, and 30 ◦C. Means with the same letter are not significantly different from each other (p = 0.05). °C,ground and 30and °C. directly Means from with thethe crownsame letter and evaluated are not significantly for their germination different from at temperatures each other (p of = 220.05). °C, 26 °C, and 30 °C. Means with the same letter are not significantly different from each other (p = 0.05). Forests 2020, 11, x FOR PEER REVIEW 10 of 14 Forests 2020, 11, 521 10 of 14

600 p = 0.262 p = 0.182 p = 0.182

500 30 °C A 22 °C 26 °C A 400

300 A A A A

Germination index Germination 200

100

0 Seeds Seeds Seeds Seeds Seeds Seeds in the in the in the in the in the in the tree ground tree ground tree ground

Seed Collection Method

Figure 9. t-test results for the germination index (GI) of D. cinnabari seeds collected from the ground Figure 9. T-test results for the germination index (GI) of D. cinnabari seeds collected from the ground and directly from the crown and evaluated for their germination at temperatures of 22 ◦C, 26 ◦C, and directly from the crown and evaluated for their germination at temperatures of 22 °C, 26 °C, and and 30 ◦C. Means with the same letter are not significantly different from each other (p = 0.05). 30 °C. Means with the same letter are not significantly different from each other (p = 0.05). 3.3. Viability of the Seeds 3.3. Viability of the Seeds The seeds that did not germinate at 26 ◦C underwent a Tetrazolium Chloride test to determine their viabilityThe seeds after that finishing did not thegerminate germination at 26 experiment.°C underwent From a Tetrazolium 300 seeds, 46 Chloride seeds did test not to germinate, determine oftheir which viability seven after seeds finishing were dead, the andgermination the remaining experi 39ment. seeds From alive. 300 Therefore, seeds, 46 seeds the percentage did not germinate, of dead seedsof which in the seven whole seeds dataset were was dead, only and 2.3%, the accordingremaining to39 this seeds test. alive. Therefore, the percentage of dead seeds in the whole dataset was only 2.3%, according to this test. 4. Discussion 4. Discussion 4.1. Number of Seeds in Individual Fruits 4.1. TheNumber natural of Seeds regeneration in Individual of FruitsDracaena cinnabari is limited by overgrazing and climate change; therefore, artificial regeneration can help to keep this species in their habitats [13]. Successful regeneration The natural regeneration of Dracaena cinnabari is limited by overgrazing and climate change; will be influenced by the quantity and quality of seeds and conditions for seed germination and seedlings therefore, artificial regeneration can help to keep this species in their habitats [13]. Successful emergence. The fruit of D. cinnabari is a berry that contains 1–3 seeds. The highest proportion of fruits regeneration will be influenced by the quantity and quality of seeds and conditions for seed contained two seeds, while the lowest proportion of fruits contained one seed, based on our results from germination and seedlings emergence. The fruit of D. cinnabari is a berry that contains 1–3 seeds. The one panicle cut in Firmihin. This finding contradicts the findings of Adolt [16], who reported the highest highest proportion of fruits contained two seeds, while the lowest proportion of fruits contained one proportion of one-seeded fruits and the lowest proportion of three-seeded fruits, and unpublished seed, based on our results from one panicle cut in Firmihin. This finding contradicts the findings of results obtained by one of the authors in 2003 with the same ratio (refer to Table1). For a generalisation Adolt [16], who reported the highest proportion of one-seeded fruits and the lowest proportion of of results, it would be necessary to analyse more panicles from more trees in time, but these results three-seeded fruits, and unpublished results obtained by one of the authors in 2003 with the same show the probable activity of pollinators (insect) within different seasons. ratio (refer to Table 1). For a generalisation of results, it would be necessary to analyse more panicles A lower amount of seeds in fruits and panicles can be caused by deficient pollination or other from more trees in time, but these results show the probable activity of pollinators (insect) within factors, such as adverse weather, attacks by insects and other pests, and deficiencies of carbohydrates, different seasons. mineral nutrients, and hormones [25]. In some species, the fruits from self-pollinated flowers are more likely to be shed prematurelyTable 1. Number than areof fruits fruits with from one, cross-pollinated two, and three seeds flowers, in one according panicle. to these authors. The differences of the present results with other findings could also be associated with differences in the age structure ofFruits the trees with: where the seeds 1 were Seed collected. 2 Seeds Madera 3 Seeds et al. [4], in Total their Fruits study,/Seeds showed a big variationNo. in the of fruits/seeds age structure 2014 of D. cinnabari 92/92throughout 194/388 Socotra 141/423 Island. 427/903 No. of fruits/seeds (Adolt 2001) 156/156 81/162 16/48 253/366 No. of fruits/seeds 2003 699/699 141/282 30/90 870/1071 Forests 2020, 11, 521 11 of 14

Table 1. Number of fruits with one, two, and three seeds in one panicle.

Fruits with: 1 Seed 2 Seeds 3 Seeds Total Fruits/Seeds No. of fruits/seeds 2014 92/92 194/388 141/423 427/903 No. of fruits/seeds (Adolt 2001) 156/156 81/162 16/48 253/366 No. of fruits/seeds 2003 699/699 141/282 30/90 870/1071

4.2. Germination Results For successful regeneration, it is crucial to assure suitable conditions for seed germination. In nature, the germinated seeds of D. cinnabari are often digested by birds, probably endemic Onychognathus frater [26], which can improve the germinating parameters of seeds [27]. Producers of ornamental species recommend soaking D. cinnabari seeds in water for three to five days, which can increase the vitality of the seeds [28]. Furthermore, Adolt [16] worked with D. cinnabari seeds with minimal ability to germinate and increased their GP by soaking in vinegar or hydrogen peroxide. In his experiment, Beyhl [15] achieved a 35% GP, but did not provide any details regarding the conditions, locality, or seed collection methods, and only provided information about the substrate, which was soil. Marrero et Almeida [16] described 10–16% of tested D. tamaranae seeds as dormant. From these publications, we can deduce that D. cinnabari seeds may need some pre-sowing treatment or some pre-sowing treatment could increase their germination parameters. However, as our study and a study by Hubálková et al. [18] indicate, D. cinnabari seeds do not demand any pre-sowing treatment. The differences between the two findings are mainly in MGT, their seeds of D. cinnabari germinated after 2–3 months’ period [18] as compared to 33 days within our experiment. The results of Adolt [16] confirm acceptable results of GP (77%) without pre-sowing treatment and for germination also using whole fruits for D. draco from Tenerife Island. The substrate properties can also influence the success of germination. E.g., Marrero et Almeida [17] germinated D. tamaranae in a more nutritious soil substrate and achieved GP of 45–96%, while GP in a less nutritious substrate did not exceed 62%. On the other hand, light conditions were not detected to have an influence within Chan-Chin et Govinden-Soulange [19] experiment. They did not observe differences in the germination of D. concinna seeds between dark conditions and diurnal light conditions. The quality of seeds depends, among others, on the method of seed collection. Our results showed certain differences between seeds that were collected from the ground and seeds removed from the tree (panicle of ripe fruits). Although the seed vitality (MGT and GI) was comparable, the GP of seeds that were collected from trees was higher (92%) than those collected from the ground (79%). This result could be associated with the conditions in the soil and the presence of fungi and microorganisms, which can obviously negatively affect seeds. Collecting seeds from standing lively trees with fruits seems better and more favourable, but the results should be confirmed by some repeated research to analyse seeds from more trees and verify diversity within a population. Moreover, some authors, e.g., Hubálková et al. [18], reached an acceptable germination percentage (84%) for seeds that were collected from the ground and, on the contrary, Adolt [16] germinated seeds from a panicle cut from a tree in Dixam locality reaching zero germination percentage in the case of no pre-sowing treatment. He stated that one of the possible reasons could be a collection of non-ripe fruits, while the collection of seeds from the ground provides a certainty of ripe seeds. GI appears to be the most comprehensive measurement parameter that combines both the germination percentage and speed (spread, duration and ‘high/low’ events) [29]. The findings of this study revealed that the GI of seeds collected from different localities and the GI of seeds collected from the ground and directly from the tree crown were relatively higher at a temperature of 30 ◦C than at temperatures of 22 ◦C and 26 ◦C in the germination experiment study. This finding shows that temperature has a substantial influence on the germination of seeds of D. cinnabari; the results of a previous study [22] indicate similar findings for Dracaena sp. seeds. Yet, Chan-Chin et Govinden-Soulange [19] obtained the best results for Forests 2020, 11, 521 12 of 14

the germination of D. concinna seeds at 25 ◦C (92% of GP); seeds that germinated at 30 ◦C and 35 ◦C had a lower GP (80%). Moreover, Monteiro et al. [22] germinated D. draco seeds in Petri dishes with: (1) a constant temperature of 20 ◦C and (2) combined temperatures of 10 ◦C and 20 ◦C changed every 12 h. Their results show 91% GP for the constant temperature and 0% for the combined temperature. However, GP do not give us a complex idea about seed germination, as written above. The GP of the seeds in our study in two of the tree localities (PL and PE) did not differ at the study temperatures, but the MGT of the seeds for all of the variants was the highest at a temperature of 30 ◦C. Temperature does not always influence the GP of D. cinnabari seeds, but seeds at different temperatures differ in the speed of germination. This fact agrees with the results of the experiment of Hubálková et al. [18], who reached similar GP but very different MGT. Germination parameters are usually under strong genetic control, which has been confirmed, e.g., at Pseudotsuga menziesii [30], Eucalyptus globulus [31], or other trees species [32], but our study based on seeds from three different localities show no differences in results (i.e., the seeds from all the localities had the best MGT and GI at 30 ◦C), therefore an influence of maternal effects seems minimal. This is also a reason why we consider the diversity within the populations to be sufficiently covered. Quite interesting are the results of different germination percentage (GP) and vitality (MGT and GI) at different temperatures of D. cinnabari seeds with different origins. Seeds from the lowest altitude (Firmihin locality, 650 m a.s.l., PL) with the highest mean annual temperature reach the highest GP. Conversely, seeds from the highest altitude (Skant locality, 1400 m a.s.l., PE) with the lowest mean annual temperature reach a lower GP. Hubálková et al. present similar results [18] for the same localities. We discovered that seeds from the lowest altitude (Firmihin locality PL) with the highest mean annual temperature reach the lowest vitality (MGT), and vice versa. A larger number of seeds from mild climates can germinate, but they germinate more slowly than seeds in harsh climates. However, these results should be confirmed by the subsequent research within time to eliminate maternal effects and assure diversity within the population at each locality. Our results combined with information from previous studies extend knowledge regarding threatened D. cinnabari species; they bring information beneficial for D. cinnabari regeneration. The results can also serve as a basis of further studies that can help to preserve populations of this flagship species.

5. Conclusions Overall, the present study results could show that, despite different authors who have carried out different germination studies on D. cinnabari and found variable results, the current findings showed that the 30 ◦C temperature used as a treatment enhanced the seed germination percentage in a shorter period of time. D. cinnabari seeds can reach a lower GP when the seeds are collected from the ground than from the tree. Therefore, we recommend collecting ripe fruits from standing trees, followed by seed extraction. A pre-sowing treatment to break seed dormancy for the species is not necessary. Rather, temperature highly influences the germination of seeds of D. cinnabari. This study showed that a temperature of 30 ◦C applied as a treatment for germination achieved a higher GI relative to the other temperatures (22 ◦C and 26 ◦C) in the study. Therefore, we recommend applying this temperature to enhance the germination of the species.

Author Contributions: L.B., field data harvesting, data analysis, and writing—original draft preparation; S.A.M., methodology, data analysis, and writing—original draft preparation; K.H., field data harvesting, and writing—original draft preparation; H.H., conceptualisation, methodology, and writing—original draft preparation. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by Czech Development Agency, grant number 22/2015/10. Acknowledgments: The authors are grateful to the Environment Protection Authority, Socotra Branch who arranged us the permission on seed collection. The authors are also grateful to Pavel Hanáˇcekand his team, who supported us in providing an air-conditioned cabinet for the experiment, to Petr Nˇemec,who collected seeds in Skant, and Abdulwahab Saad who collected seeds in Sirhin. Forests 2020, 11, 521 13 of 14

Conflicts of Interest: The authors declare no conflict of interest.

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