Effects of submergence in water on seed germination and vigor of the Copaifera lucens (Fabaceae) see

Journal of Forestry Research (2014) 25(4): 903- 908DOI 10.1007/s1 1676-014-0537-zORIGINAL PAPEREffects of submergence in water on seed germination and vigor of theCopaifera lucens (Fabaceae) seedlingsDaniela Baldez Vidal●Isis Leite Andrade●Eusinia Louzada Pereira AndradeMarcelo Schramm MielkeReceived: 2013-03-01;Acepted: 2013-12-03◎Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2014Abstract: We analyzed the tolerance of Copaifera lucens seeds to sub-mersion in water to assess the use of this species for direct seeding inriparian forest restoration programs. Seeds were submerged in water forIntroduction2, 4, 8, 16 and 32 days or not submerged (control = 0 days of submer-gence). For the control and at the end of each period of submersion,Riparian forests occur along waterways and function as regula-germination and seedling vigor tests were carried out. For germination tors of water flow, sediment and nutrients between the uppertests, seeds were sown in plastic pots containing sand and kept in labora-parts of the watershed and the aquatic ecosystems (Kozlowskitory conditions. The percentage of seed germination, the germination rate2002). Because riparian forests are located near watercourses,and the average germination time were analyzed. For seedlings, totalthese ecosystems are highly unstable forest formations and sus-biomass, leaf area, leaf mass per area and leaf area ratio were analyzed.ceptible to periodic flooding (Budke et al. 2008). Although pro-Submersion time drastically affected the dissolved oxygen content andtected by law, most of the riparian forests of the Brazilian Atlan-seed germination. Between 4 and 8 days of submersion there was a de-tic Rainforest are degraded and require the results of scientificcrease from 83.8% to 15.6% in the germination percentage. No seedstudies to provide basic information applicable to forest restora-germination occurred after 16 days of submersion. Although there was ation programs (Mielke et al. 2005; Lavinsky et al. 2007).significant decrease in the percentage of seed germination between 4 andKnowledge of the environmental requirements for tree species8 days of submersion, seedling vigor was not affected. Seeds of thisto be used for restoration of degraded riparian forests can assistin developing strategies that enhance the establishment of seed-lucens is a promising species for direct seeding in riparian forest restora-lings, reduce costs and increase the success of restoration. Con-tion projects.sidering expense, convenience, and ease of planting, direct seed-ing is a promising technique that has been tested for restorationKeywords: Copaiba, Brazilian Atlantie Forest, forest restoration, germi-of forest ecosystems (Engel and Parotta 2001; Camargo et al.nation, vigor2002; Woods and Elliot 2004; Doust et al. 2008; Bonilla-Morenoand Holl 2010; Cole et al. 201 1), including riparian forests (San-tos Jr et al. 2004; Ferreira et al. 2009). Studies of the viability ofseeds of forest species subjected to submersion in water can beuseful for the planning and success of projects to recover de-graded riparian forests.The online version is available at http:// www .springerlink.comSeed germination is one of the main factors affecting theDepartment of Agricultural and Environmental Sciences, State Universityfor production of seedlings in forest nurseries (Schmidt 2007). .of Santa Cruz, BR 415, km 16, lheus 45662 -300, Bahia. Brazil.The effectiveness of seed germination is closely related to seedrequirements such as water availability, gas composition, andIsis Leite Andrade●Marcelo Schramm Mielke )Department of Biological Sciences, State University of Santa Cruz, BRiting factor for the germination of non-dormant seeds, and affects415, km 16. Iheus 45662300, Bahia, Brazil.the rate, speed and uniformity of the process. Adequate supply ofEmail: msmielke@ uesc.brwater to the seed is associated with the mohilization of reservesCorresponding editor: Zhu Hongand release of中国煤化工: stimulates thefYHCNMHG包Springer904Journal of Forestry Research (2014) 25(4): 903- -908activity of enzymes and plant hormones (Baskin and Baskin998).remove surface water. After drying, measurements were takenEven though most seeds do not require oxygen concentrationsfor length, width, thickness, the weight of 1,000 seeds and theabove 10% for germination, lower levels can cause problemsseed moisture content. Biometrics (length, width and thickness)(Bewley and Black 1994; Baskin and Baskin 1998). In case offlooding, respiration of aerobic organisms associated with the1,000 seeds was determined by eight replicates of 100 seedslow diffusion of oxygen in water leads to a rapid decline in(Brazilian Ministry of Agriculture and Food Supplies 2009).available oxygen resulting in hypoxia or anoxia (Bailey-SerresSeed moisture content was determined by drying the mass ofand Voeseneck 2008). Limited oxygen supply to seeds during allseeds in an oven at 105 °C for 24 hours, with four replications ofstages of germination induces changes in aerobic respiratory10 seeds (Brazilian Ministry of Agriculture and Food Suppliesrates, causing increased fermentation, or anaerobic pathway,2009).producing lactic acid and ethanol (Crawford 1992; Lobo and JolySeeds were submerged in distilled water for 2, 4, 8, 16, and 32days or not submersed (0 days of submergence for controls). Sixdeath and loss of seed viability.1,000 ml beakers containing 186 seeds and 400 ml of distilledlPlants of the genus Copaifera are popularly known as‘co-water each were used. For the submersion treatments, the seedspaibeiras' or 'pau-d"'leo', as they produce an oil-resin of me-were incubated in a germinator at 25。C in the dark. During in-dicinal and commercial importance (Veiga-Junior and Pintocubation periods, dissolved oxygen (DO) was monitored using a2002; Rigamonte-Azevedo et al. 2004). Copaibeiras grow to multiparameter water quality analyzer HI 9828 (Hanna, Woon-10-40 meters tall and have dense foliage consisting of compositesocket, Rhode Island, USA) at0, 1, 2, 3, 4,5,6, 7, 8, and 24pinnate leaves, in alternate form, with coriaceous leaflets of 3-6hours, and 2, 4, 8, 16, 21, and 32 days after the beginning ofcm in length (Pio Correa 1984). Costa (2007) reported 38 speciestreatments. For the control, seeds were sown immediately afterin the genus Copaifera, 22 of which are restricted to Brazil.biometric measurements were carried out. At the end of eachThese species occur naturally in a variety of ecosystems, such assubmergence period, four replications of 40 seeds were subjectedupland forests, wetlands, lake shores and steams of the Amazonto germination tests. Seeds were sown in plastic containers (19Basin, in the forests of Central Brazilian vegetation and Atlanticcm X 45 cm x 14 cm) with washed and sterilized sand as sub-Forest (Rigamonte-Azevedo et al. 2004). Costa (2007) reportedstrate and kept under laboratory conditions. A Hobo H8 Pro Se-that Copaifera lucens Dwyer occurs exclusively in the easternries (Onset Computer, Bourne, Massachusetts, USA) sensor wasportion of Brazil, in areas of the Atlantic Rainforest in the statesused to monitor the environmental conditions inside the labora-of Bahia, Espirito Santo, Minas Gerais, Rio de Janeiro and Saotory, and the average temperature and relative humidity duringPaulo. In southern Bahia, this species has been found in the experiment were 26.3 °C and 66%, respectively. Germinatedrainforests and semideciduous forests, primary and secondaryseeds were counted every two days from the beginning of eachformations, and riparian forests, and is recommended for use ingermination test. The germination rate was expressed by theforest restoration programs because the seed aril provides foodgermination velocity index (GVI) (Maguire 1962) and averagefor animals (Sambuichi 2009).germination time (AGT) was calculated according to EdmondDespite the potential of direct seeding (Campbell et al. 2002;and Drapala (1958).Santos Jr et al. 2004; Moreno-Bonilla and Holl 2010) and theTo evaluate the effects of seed submersion on the vigor ofindications for the use of species in the genus Copaifera for theseedlings, at 23 days after the end of each germination test threerestoration of degraded riparian forests (Sambuichi 2009) to datenormal seedlings per container were collcted to have leaf areano information is available in the literature about the viability of(LA), total biomass, leaf mass per area (LMA) and the leaf areaseeds of these species after submersion in water. Thus, this studyratio (LAR) measured. LA was estimated using an automatic leafwas carried out to investigate the effect of submersion in water area meter LI-3100 (LI-COR, Lincoln, Nebraska, USA). Seed-on seed germination and seedling vigor of C. lucens.ling biomass was obtained after drying plant material at 70°Cuntil a constant mass was reached. LMA and LAR were calcu-lated by the ratios between dry mass of leaves and leaf area, andMaterials and methodsbetween leaf area and total biomass per plant, respectively.The experimental design was completely randomized with sixFruits of C. lucens were collected in August 2010 from treestreatments (submersion periods) and four replications. For ger-located on "Terra Vista' Setlement, Arataca, Bahia, Brazil. Aftemination tests, each experimental unit consisted of 40 seeds andcollection, the fruits were taken to the laboratory of Plant Sci- for seedling vigor analysis each experimental unit consisted ofence, Universidade Estadual de Santa Cruz (UESC), Iheus, Ba-three seedlings. The results expressed as percentages were trans-hia, Brazil. Seeds were manually extracted and those damaged informed into arcsin (x/100)05. The results were analyzed usingthe mechanical process or by pests, diseases or impurities wereANOVA followed by Tukey's test at a 5% probability level.discarded. Seeds were then sterilized in 70% ethanol for 1 min-ute, rinsed in distlledl water, submerged in a commercial bleachsolution for 10 minutes, washed again with distilled water andtreated with the fungicide Nystatin for one minute. After sterili-中国煤化工MHCNMH G包SpringerJoumal of Forestry Research (2014) 25(4): 903-908905ter immersing the seeds in water, falling from approximatelyResults70% to 20% within 8 hours of immersion (Fig. 1a). Approxi-mately 16 hours after immersing seeds in water, DO reached 0%and thickness (CV<10%), (Table 1), with a tendency to be longer the beginning of the experiment (Fig. 1b). Thus, only the seedsthan wide or thick. The results also indicated that 1,000 seeds of of the control treatment (0 days of submergence) were in an en-C. lucens weighed approximately 25 kg with a moisture contentvironment with adequate oxygen levels to start the germinationabove 30%.For the control and for the treatments of submersion for 2, 4Table 1: Biometric variables, weight of 1,000 seeds and moisture contentand 8 days, seed germination began at 9, 7, 5, and 5 days after .of C. lucens seeds.sowing, respectively (Fig. 2). No seed germination occurred after16 days of submersion. Although only the control was at ade-Variables Length Width Thickness Weight of 1000Moisturequate levels of oxygen availability to start the germination proc-(mm)_ (mm)__ (mm)seeds (g)content (%)ess, anoxia did not affect seed germination for up to 4 days ofMinimum 13.3 10.110.0248732submersion in water, since no significant differences were ob-Maximu30.34.814.727073Sserved for the control and treatments of 2 and 4 days of submer-Average_2567.3.sion in water for G40 and AGT (Table 2)._CV (%)18.73 7.347.463.013.76Notes: ! Ceoffcient of variation.70 [y= 53.72e-0.16x503020 t1028001.000Time (hours)Fig. 1: Dissolved oxygen content in water as a function of submersion time of C. lucens seeds. Measurements taken every hour until 8 hours (a) and 24,48, 96, 192, 384, 504 and 768 hours (1, 2, 4, 8, 16, 21 and 32 days, respectively) after the sinking of the seeds (b).GVI after 4 days of submersion was significantly higher thanfor the other treatments. The control seeds and seeds submergedfor 2 days did not differ significantly in terms of GVI, but GVIwas lower for the 8 day submergence treatment. There was nosignificant difference in AGT between untreated seeds and allother treatments. Although the mean AGT values did not differ-32between submersion periods, radicle protrusion for submersionAYYof 4 and 8 days started at the same time (5 days after sowing),but immersing the seeds for 8 days significantly affected germi-▲MMAnation (Fig. 2). Submersion of seeds for 8 days led to significant.◆◆◆.◆⑥⑥◆increase in the number of dead seeds at end of the test (82%) and40reduced the germination rate (Table 2, Fig. 2).Time (days)At 23 days after the end of germination tests (Table 3), whenthe seedlings had two fully expanded leaves, there were no sig-Fig. 2: Germination of C. lucens seeds as a function of the time of sub-nificant differences between treatments for total dry biomass, LA,mersion in water.LMA and LAR.中国煤化工MYHCNMHG包Springer906Journal of Forestry Research (2014) 25(4): 903- -908activity. In dry seeds, the amount of adenosine triphosphate(ATP) is extremely low but increases rapidly during imbibitionDiscussiondue to aerobic respiration that is the main source of ATP beforethe emergence of the radicle. However, when seeds are deprivedmoisture in seeds of about 27.6%, a value approximating that the block of oxidation in the mitochondria terminal (Baskin andobserved in this study. However, the weight of 1,000 seedsBaskin 1998). Thus, the rapid decline of dissolved oxygen, char-measured in our study was over three times higher than the valueacterizing hypoxia and anoxia around 8 and 16 hours after im-obtained by Guerra et al. (2006) for C. langsdoffi. This differ-mersing the seeds, respectively, may have been a consequence ofence may have been caused by seed biometrics since accordingtheir high respiration rate.to Guerra et al. (2006) seeds of C. langsdorffi were 13.23 mmNoleto et al. (2010) reported that germination of C. lang-long, 8.46 mm wide and 8.81 mm thick, smaller than C. lucenssdoffti began six days after sowing, approximating our results.seeds (Table 1). Moreover, Brum et al. (2009) reported that seedsHowever, for the controls, the values of G40 were lower thanof C. multjuga were on average 20 mm long, 13 mm wide andthose obtained by Noleto et al. (2010) for C. langsdorffi, who11 mm thick, very close to the results of our study for C. lucens.reported germination rates of 83% 25 days after sowing.Information on seed biometrics and weight of 1000 seeds is im-Cust6dio et al. (2002) reported a decrease of approximatelyportant for direct seeding in forest restoration projects, providing50% in germination and vigor of Phaseolus vulgaris L. (Fa-information on the amount of seeds that each worker can take to baceae) seeds after 8 hours of immersion in water. Moreover, anthe planting areas, as well as to calculate the amount of seedincrease in the number of dead seeds and inhibition of rootneeded for the planting area.growth was observed as the submersion time increased. After 48hours 80-90% of the seeds died and after 16 hours of immersionTable 2: Percentages of germinated seeds at fften (G15) and forty days the length of the root and hypocotyl and the dry weight of the(G40) after starting germination tests, germination speed index (GVI)shoot decreased more than 90%. On the other hand, Okamotoand average seed germination time (AGT) at the end of the germinationand Joly (2000) found that seeds of Inga sessilis (Vell) Mart.test (40 days) of C. lucens a function of time of submersion in water.(Fabaceae) when subjected to anoxia for four days showed aValues are means土standard deviation. (n =4).decrease of about 30% in germination. When seeds were sub-jected to anoxia for 10 days there was practically no germination._Time (days)G15(%)__ G40(%)GVIAGT (days)_Considering that P. vulgaris is intolerant to flooding15.0+8.2c 76.3+8.3a1.8+0.6b22.0+1.3(Schravendijk and van Andel 1985) and I. sessilis is partially28.13.8b 76.3+12.6a 1.9+0.4b20.3+1.8tolerant, the results obtained in our study indicate that seeds of C.46.9+8.5a 83.8+3.2a 2.8+0.1a25 4+4.3.lucens can tolerate short periods of flooding.13.8.._.._ 15.649.4..... 0.6+0.3c24.9+14.8LA, LMA and LAR are very important attibutes associatedCV(%)259.0912.5833.71with photosynthetic activity and growth in tropical tree seedlings_p (ANOVA)(Poorter and Bongers 2006; Houter and Pons 2012). Also, ahigher LMA is related to greater allocation of carbon to supportNotes: Means followed by the same ltter are not sigificantly different ac-and defense (Castro-Diez et al. 2000), enhancing seedling sur-cording to a Tukey test (p <0.05). *p <0.05; ** p <0.01; ns p >0.05.vival and growth when subjected to environmental stressTable 3: Biomass, leaf area (LA), specific leaf mass (LMA), leaf area(Poorter and Bongers 2006). Therefore, the lack of significantdifferences between treatments for total dry biomass, LA, LMAratio (LAR) of C. lucens seedlings originated from the untreated seeds (0and LAR at 23 days after the end of the germination tests showeddays of submergence) and for the treatments of submersion for 2, 4 and 8that, although there were differences between treatments for thedays. Values are means土standard deviation. (n =4)。germination tests, the submersion of seeds in water did not affetTimeBiomassLALMALARseedling vigor. Even though field tests are still necessary, these(days)(gm2)results have shown that seedlings of C. lucens from seeds sub-0.94+0.05 51.5+3.6 .98.7+4.1 55.0+3.5merged in water could have the same chance of survival and0.99+0.08 48.9+4.5102.2+9.5 50.0+7.5establishment as seedlings from non- submerged seeds.0.94+0.18 48.8+3.598.1+8.252 9+7.1Studies of temperate and tropical trees have shown that seed0.90+0.14 49.3+11.498.9+4.854.1+4.7weight is an important trait associated with seedling survival andCV (%)13.1713.347.0611.23establishment (Khan 2004; Baraloto et al. 2005; Metz et al. 2010;p(ANOVA)nsPerez-Ramos et al. 2010). Seed weight can also be related toseedling vigor after relatively long periods of submergence inNotes: Means followed by the same letter are not significantly different ac-water (Perez- Ramos and Maranon 2009). Thus, the similar vigorcording to a Tukey test (0 <0.05). *p <0.05; ** p <0.01; nsp≥>0.05.of seedlings of control seeds in comparison with treatments of 2,4 and 8 days of submersion may be related to the size and weightThe beginning of the imbibition of water by the seed occursof C. lucens seeds. Even though. immersing seeds in water re-due to the formation of the water potential gradient between theduced germinatio中国煤化工germination andseed and the substrate, followed by a rapid increase in respiratoryYHCNMH G包SpringerJourmal of Forestry Research (2014) 25(4): 903- -908907seedling establishment of this species are possible even after theoccurrence of occasional flooding. This supports the option ofareas of Central Amazonia using direct sowing of forest tree seeds. Re-using direct sowing as a technique (Santos Jr. et al. 2004) for thestor Ecol, 10: 636 -644.use of C. lucens in restoration projects of degraded riparian for-Castro-Diez P, Puyravaud JIP, Comelissn JHC. 2000. Leaf structure andests.anatomy as related to leaf mass per area variation in seedlings of a wideWe conclude that the time of submergence drastically affectedrange of woody plant species and types. Oecologia, 124: 476- -486.the dissolved oxygen content and the germination of C. lucens,Cole RI, Holl KD， Keene CL, Zahawi RA. 2011. Direct sceding ofand that between 4 and 8 days of immersion subsequent germi-lt-cssional trees to restore tropical montane forest. Forest Ecolnation declined from 83.8 to 15.6%. On the other hand, althoughManag, 261: 1590-1597.there was a significant decrease in the percentage of seed germi-Costa JAS. 2007. Taxonomic, biosystematic and phylogenetic studies in Co-nation between 4 and 8 days of submersion, seedling vigor waspaifera species with emphasis on the extra-Amazonian Brazil. Feira denot affected. Although further studies on the metabolism of C.Santana: State University of Feira de Santana, p. 266. (Portuguese withlucens seeds under anoxic conditions and field tests must still beabstract in English)performed, our results indicate that seeds of this species are par-Crawford RMM. 1992. Oxygen availability as an ecological limit to planttially tolerant to submersion in water, suggesting that C. lucens isdistrbution. Adv Ecol Res, 23: 93-185.a promising species for direct seeding in riparian forests restora-Custodio CC, Machado Neto NB, Ito HM, Vivan MR.2002. The foodingtion projects.effects on the bean seed germination and vigor of bean seeds. Rev BrasSemenes, 24: 49 -54. (Portuguese with abstract in English)AcknowledgementsDoust SI, Erskine PD, Lamb D.2008. Restoring rainforest species by directDaniela B. Vidal was master s degree scholarship student at theseeding: Tree seedling estabishment and growth performance on deFoundation for Research Support of theState of Bahiagraded land in wet tropics of Australia. Forest Ecol Manag, 25(FAPESB). The authors acknowledge the Terra Vista settlement1178-1188.and biologists Jose Lima da Paixao and Michaele Pessoa forEdmond JB, Drapala WJ.1958. The efects of temperature, sand and soil, andproviding the seed lot used in this study. Marcelo S. Mielkeacetone on germination of okra seed. P Am Soc Hortic Sci, 71: 428- 434.thanks the Brazilian National Council for Scientific and Techno-Engel VL, Prrota JA. 2001. An evaluation of diret seeding for reforesationlogical Development (CNPq) for a productivity fellowship. Weof degraded lands in central Sao Paulo state, Brazil. Foresi Ecol Manag,also thank Dr. Carter R. Miller, Dr. Janisete G. Silva and the152: 169-181.anonymous reviewers for constructive comments to help im-Ferreira RA, Santos PL, Aragio AG, Santos TIS, Santos Neto EM, Rezendeprove the manuscript.AMS. 2009. Direct sowing for the implantaion of a riparian forest at thelower San Francisco River in Sergipe State, Brazil. Scientia Forestalis,37: 37-46. 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