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Key factors affecting seed germination of Copaifera langsdorffii, a Neotropical tree

Abstract

In natural conditions biotic and abiotic factors interact, synergistically affecting seed germination. In this study, we experimentally simulated natural conditions that occur during seed dispersal that can affect the germination of Copaifera langsdorffii. Specifically we evaluated the effect of aril removal by different dispersal agents (birds and ants) and fire on germination. The seeds were submitted to the following treatments: Control (seeds placed to germinate with aril intact); Acid (simulation of passage through the digestive tract of a bird); Aril removal (simulation of aril removed by ants); Fire (seeds exposed to fire). Germination percentage and time varied among treatments (X²=89.735, P<0.001; X²=16.225, P<0.001, respectively). None of the control seeds (intact aril) germinated. Treatments that simulated dispersal (Acid, Aril removal) did not differ in germination percentage, with about 50% of the seeds germinating, however, the acid treatment accelerated seed germination. Fire also had a positive effect on seed germination with about 80% of the seeds germinating. Our results demonstrate the importance of dispersal agents to the population dynamics of C. langsdorffii. Furthermore, the capacity of seeds of C. langsdorffii to tolerate high temperatures is an important attribute for the occurrence of this species in the Cerrado.

Cerrado; Copaifera langsdorffii; fire; plant-disperser interaction; seed germination


Introduction

Seed germination is a critical phase of the plant life cycle, influencing the distribution and abundance of species in plant communities (Wulff 1986Wulff RD. 1986. Physiological performance seed size variation in Desmodium paniculatum. Journal of Ecology 74: 99-114. ; Armstrong & Westoby 1993Armstrong DP, Westoby M. 1993. Seedlings from large seeds tolerated defoliation better: a test using phylogeneticaly independent contrasts. Ecology 74: 1092-1100.). Biotic factors, intrinsic to the seed and/or interactions with other organisms and abiotic factors, such as light, temperature, humidity and fire, affect germination differently (Baskin & Baskin 1998Baskin CC, Baskin JM. 1998. Seeds - ecology, biogeography, and evolution of dormancy and germination. New York, Academic Press. ). Zoochorous seeds have fleshy structures that attract and reward their dispersers (Christianini et al. 2007Christianini AV, Mayhé-Nunes AJ, Oliveira PS. 2007. The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a Neotropical savanna. Journal of Tropical Ecology 23: 343-351.) and often have substances that inhibit germination (Cipollini & Levey 1997Cipollini ML, Levey DJ. 1997. Secondary metabolites of fleshy vertebrate dispersed fruits: adaptive hypotheses and implications for seed dispersal. The American Naturalist 150: 346-372.; Yagihashi & Miyamoto 1998Yagihashi T, Hayashida M, Miyamoto T. 1998. Effects of bird ingestion on seed germination of Sorbus commixta. Oecology 114: 209-212.; Robertson et al. 2006Robertson AW, Trass A, Ladley JJ, Kelly D. 2006. Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Functional Ecology 20: 58-66.). Thus, in addition to transporting seeds away from the mother plant, seed dispersers can be important to the successful germination of some species by removing compounds that inhibit germination (Robertson et al. 2006; Silveira et al. 2012Silveira FAO, Mafia PO, Lemos-Filho JP, Fernandes GW. 2012. Species-specific outcomes of avian gut passage on germination of Melastomataceae seeds. Plant Ecology and Evolution 145: 350-355.; Lessa et al. 2013Lessa LG, Geise L, Costa FN. 2013. Effects of gut passage on the germination of seeds ingested by didelphid marsupials in a neotropical savanna. Acta Botanica Brasilica 27: 519-525.). Birds and ants are important groups that mutually interact as seed dispersers and can remove inhibitors, thus promoting germination (Meyer & Witmer 1998Meyer GA, Witmer MC. 1998. Influence of seed processing by frugivorous birds on germination success of three north American shrubs. The American Midland Naturalist Journal 140: 129-139.; Christianini & Oliveira 2010; Guerta et al. 2011Guerta RS, Lucon LG, Motta-Junior JC. 2011. Bird frugivory and seed germination of Myrsine umbellata and Myrsine lancifolia (Myrsinaceae) seeds in a Cerrado fragment in southeastern Brazil. Biota Neotropica 11: 59-65.; Lima et al. 2013Lima MHC, Oliveira EG, Silveira FAO. 2013. Interactions between ants and non-myrmecochorous fruits in Miconia (Melastomataceae) in a neotropical Savanna. Biotropica 45: 217-223.), however, this influence is not uniform among zoochorous species (Barnea et al. 1991Barnea A, Yom-Tov Y, Friedman J. 1991. Does ingestion by birds affect seed germination? Functional Ecology 5: 394-402.; Figueroa & Castro 2002Figueroa JÁ, Castro SA. 2002. Effects of bird ingestion on seed germination of four woody species of the temperate rainforest of Chiloé Island, Chile. Plant Ecology 160: 17-23.).

Fire can interfere in many aspects of plant development, especially in the biology of seeds (Paula et al. 2009Paula S, Arianoutsou M, Kazanis D, et al. 2009. Fire-related traits for plant species of the Mediterranean basin. Ecology 90: 1420.). The effects of fire on the seeds include loss of viability (Schmidt et al. 2005Schmidt IB, Sampaio AB, Borghetti F. 2005. Efeitos da época de queima sobre a reprodução sexuada e estrutura populacional de Heteropterys pteropetala (Adr. Juss.), Malpighiaceae, em áreas de Cerrado sensu stricto submetidas a queimas bienais. Acta Botanica Brasilica 19: 927-34.), dormancy break (Ribeiro et al. 2013Ribeiro LC, Borghetti F. 2014. Comparative effects of desiccation, heat shock and high temperatures on seed germination of savanna and forest tree species. Austral Ecology 39: 267-278.), and the activation of genes important to germination by the presence of smoke (Moreira et al. 2010Moreira B, Tormo J, Estrelles E, Pausas JG. 2010. Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Annals of Botany 105: 627-635.). These effects depend mainly on the degree of tolerance a seed and the species life history has to high temperatures (Luna et al. 2007Luna B, Moreno JM, Cruz A, Fernández-González F. 2007. Heat-shock and seed germination of a group of Mediterranean plant species growing in a burned area: an approach based on plant functional types. Environmental and Experimental Botany 60: 324-33.). The Cerrado is an environment in which fire has been a recurrent factor for thousands of years (Salgado-Laboriau et al. 1997Salgado-Labouriau ML, Cassetti V, Ferraz-Vicentini KR, et al. 1997. Late Quaternary vegetational and climatic changes in cerrado and palm swamp from Central Brazil. Palaeogeography, Palaeoclimatology, Palaeoecology 128: 215-226.). In fact, recent studies have shown that seeds of plants of the Cerrado tend to be more tolerant to high temperatures than seeds of forest plants (Ribeiro et al. 2013; Ribeiro & Borghetti 2014). Despite these recent efforts, studies assessing the effects of fire on the germination of native Cerrado plant species remain scarce, especially investigations involving species that are not endemic to this biome.

Copaifera langsdorffii (Fabaceae) is a species of tropical tree of 7-30 m in height (Carvalho 2003Carvalho PER. 2003. Espécies arbóreas brasileiras. Embrapa Informação Tecnológica. Brasília, Colombo: Embrapa Florestas. ). The species is widely distributed in South America (Carvalho 2003). In Brazil the species occurs in the physiognomies of Cerrado, Atlantic Forest and gallery forest, from the north to the south (Almeida et al. 1998Almeida SP, Proença CEB, Sano SM, Ribeiro JF. 1998. Cerrado: espécies vegetais úteis. Brasília, Embrapa. ). Copaifera langsdorffii presents supra-annual fruiting, with alternating years of high and low or no fruit production (Pedroni et al. 2002Pedroni F, Sanchez M, Santos AM. 2002. Fenologia da copaíba (Copaifera langsdorffii Desf. - Leguminosae, Caesalpinioideae) em uma floresta semidecídua no sudeste do Brasil. Revista Brasileira de Botânica 25: 183-194.; Fagundes et al. 2013Fagundes M, Maia MLB, Queiroz ACM, Fernandes GW, Costa FV. 2013. Seed Predation of Copaifera langsdorffii Desf. (Fabaceae: Caesalpinioideae) by Rhinochenus brevicollis Chevrolat (Coleoptera: Curculionidae) in a Brazilian Cerrado Fragment. Ecología Austral 23: 218-221.). Flowering occurs from November to January and fruits mature in July to September, coinciding with the period of greatest deciduousness (Pedroni et al. 2002; Fagundes et al. 2013). There are many types of dispersers of the seed of Copaifera langsdorffii, but the primary seed dispersers are birds (see Rabello et al. 2010Rabello A, Ramos FN, Hasu E. 2010. Efeito do tamanho do fragmento na dispersão de sementes de Copaíba (Copaifera langsdorffii Delf.). Biota Neotropica 10: 47-54.), and the secondary dispersers are ants (see Leal & Oliveira 1998Leal IR, Oliveira PS. 1998. Interactions between fungus-growing ants (Attini), fruits and seeds in Cerrado vegetation in southeast Brazil. Biotropica 30: 170-178.; Silva & Souza 2014Silva A, Souza DJ. 2014. Interação entre Atta sexdens e espécie arbórea Copaifera langsdorfii Desf. em remanescente florestal de Cerrado. Revista Verde 9: 182-189.). The seeds of C. langsdorffii have orthodox behavior (Bezerra et al. 2002Bezerra AME, Medeiros SF, Moreira MG, Moreira FJC, Alves TTL. 2002. Germinação e desenvolvimento de plântulas de copaíba em função do tamanho e da imersão da semente em ácido sulfúrico. Revista Ciência Agronômica 33: 5-12.) and pre-germination treatments of scarification can accelerate the germination process (Perez & Prado 1993Perez SCJGA, Prado CHBA. 1993. Efeitos de diferentes tratamentos pré-germinativos e da concentração de alumínio no processo germinativo de sementes de Copaifera langsdorfii Desf. Revista Brasileira de Sementes 15: 115-118.). In addition, Souza & Fagundes (2014) showed that seed size as key factor in germination of C. langsdorffii.

In natural conditions, biotic and abiotic factors interact synergistically directly affecting time to germination and the percentage of successful seed germinations. Thus, the objective of this study was to evaluate seed dispersal of C. langsdorffii, in laboratory situations simulating field conditions, in order to determine the effects of biotic and abiotic factors on the process of seed germination. Specifically we seek to answer the following questions: (i) What influence does aril removal have on seed germination of C. langsdorffii? (ii) Knowing that birds and ants can disperse the seeds of C. langsdorffii and that they remove the aril differently, do they have differing affects on germination? (iii) Does fire affect seed germination of C. langsdorffii?

Materials and methods

Study area

Fieldwork was conducted in a Cerrado (Brazilian savanna) area located in the Floresta Nacional de Paraopeba (FLONA-PARAOPEBA, 19°20'S, 44°24'W), in the municipality of Paraopeba, in southeastern Brazil. The climate is type AW according to the Köppen classification, with a rainy summer and a dry season from April to September, corresponding to the fall and winter. The average annual temperature is 20ºC and the annual accumulated rainfall is about 1300 mm (INMET 2015INMET - Instituto Nacional de Meteorologia. 2015. http://www.inmet.gov.br/portal/. 12 Feb. 2015.
http://www.inmet.gov.br/portal/...
). Annual climatic variation is shown in Fig. 1.

Figure 1 .
Average monthly precipitation and temperature in Paraopeba-MG.

Data collection

In August 2013, 10 reproductive individuals of Copaifera langsdorffii Desf. were selected at the study area. The trees were five to seven meters high, had well-formed crowns and were in a good phytosanitary state (e.g. without lianas or parasitic plants). Fruits were haphazardly collected from throughout the canopy of each selected tree (Costa et al. 2010Costa FV, Fagundes M, Neves FS. 2010. Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Ecología Austral 20: 9-17.). All collected fruits were manually treated and using similarly sized seeds, with malformed seeds and those with visual signals of attack by predators or pathogens being eliminated. After processing, the seeds of all individuals were mixed and divided randomly among four treatments, with 100 seeds per treatment. The probability of germination was calculated assuming each seed to be a statistically independent experimental unit (see Warton & Hui 2011Warton D, Hui F. 2011. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92: 3-10.).

The treatments used here simulate situations observed in the field that are suspected to influence the germination process. To evaluate the affect of aril removal by different seed dispersers and of fire on seed germination of C. langsdorffii, the seeds were submitted to the following treatments: control treatment, seeds placed to germinate with aril intact; acid treatment, simulation of the passage through the digestive tract of birds by exposing seeds to sulfuric acid (H2SO4) for 5 minutes; aril removed, simulation of aril removal by ants; fire treatment, seeds lacking arils into were partially buried in a layer of 5 cm of Cerrado soil in a 20 x 40 cm tray and covered by a litterfall layer from the study area, which was subsequently burned for about 30 minutes. After all treatments the seeds were rinsed with distilled water and tested for germination.

The seeds were placed in a gerbox, properly identified with their treatment, and covered with filter paper. The germination experiment was conducted in a germination chamber with controlled photoperiod and temperature (12 h/light at 30°C e 12 h/dark at 25°C). The seeds were monitored daily for 30 days to determine the percentage of germination and time to germination. A seed was considered germinated when primary root protrusion occurred (Ferreira & Borghetti 2004Ferreira AG, Borghetti F. 2004. Germinação: do básico ao aplicado. Porto Alegre, Artmed.).

A soaking test was conducted under the same germination conditions using 30 different seeds. Seed mass was determined and then all seeds were immersed in distilled water and reweighed after 6, 18, 30, 48, 72, 96, 120, 144, 168, 192, 216 and 240 hours of water absorption. Relative increase in fresh weight (Wr) of seeds was calculated as Wr = [(Wf −Wi)/ Wi] ×100 where Wi is the initial seed weight and Wf the weight after each time interval of water absorption (Baskin & Baskin 2004). Thus, imbibition curves were based on the increase in seed mass at different time intervals of seed immersion in distilled water.

Data Analysis

Data were analyzed using R software (R Core Team 2014R Development Core Team 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org.
http://www.rproject.org...
). Germinability was evaluated by constructing a generalized linear model (GLM) using an appropriate error distribution for each response variable. The model was assessed via residual analysis (Crawley 2007Crawley MJ. 2007. The R Book. New York, John Wiley and Sons. ). The germinability of a seed, based on a binary response (germinated or non germinated), is commonly expressed as a percentage (Ranal & Santana 2006Ranal MA, Santana DG. 2006. How and why to measure the germination process? Revista Brasileira de Botânica 29: 1-11.). We used the binomial distribution error, indicated for binary data as the germination. Recently, Warton & Hui (2011) showed that this statistical approach provides a significant gain in power. The effect of treatments on germination was tested using the germination percentage of each treatment as response variables and treatments as explanatory variables.

To evaluate the probability of germination over a period of time, survival analysis was performed in order to test the effect of treatments on time of seed germination (Souza & Fagundes 2014). Thus, germination percentage within each treatment was used as response variables, while germination time was the explanatory variable. Survival analysis evaluates the likelihood of germination at a certain point in time, thus avoiding the temporal pseudo-replication inherent to the data.

Seed water absorption was tested by constructing Generalized Linear Mixed Models (GLMM), since these data also showed temporal pseudo-replication (Souza & Fagundes 2014). Thus, increased seed mass (Wr) was used as the response variable and time of water absorption (6, 18, 30, 48, 72, 96, 120, 144, 168, 192, 216 and 240 hours) as the explanatory variable.

Results

Germinability varied among treatments (X² = 89.735, P< 0.001). Our results demonstrated that aril removal positively influenced germination (Fig. 2). No significant differences were observed in the proportion of germinated seeds between acid treatment and without aril. No seed with aril intact (control treatment) germinated (Fig. 2). Fire also positively affected seed germination (Fig. 2), having the highest germination percentage among treatments with about 80% of the seeds germinating. At the end of the germination test, all non-germinated seeds were examined and found to be damaged and marked by the presence of fungi.

Figure 2.
Percentage of seeds of Copaifera langsdorffii succesfully germinatiing in different treatments. Control: seeds placed to germinate with aril intact. Acid: simulation of the seed passage through the digestive tract of birds through exposing seeds to sulfuric acid for 5 minutes. Aril removal: simulation of aril removal by ants. Fire: aril removal followed by partial burial.

Overall, seeds germinated from the 4th to 25th day. The time to seed germination varied among treatments (X² = 16.225, P< 0.001). In this case, the removal of the aril affected germination time. Seeds submitted to acid treatment germinated more quickly than those without aril and those exposed to fire, which did not differ significantly (Fig. 3). The soaking test showed that water absorption varied with time (F = 243.609, P <0.001), and that the seeds of C. langsdorffii exhibited great variation in water imbibition (Fig. 4).

Figure 3.
Time to seed germination for Copaifera langsdorffii in different treatments. Vertical lines indicate the time required for germination of 50% of the seeds. Acid: simulation of the seed passage through the digestive tract of birds by exposing seeds to sulfuric acid for 5 minutes. Aril removal: simulation of aril removal by ants. Fire: aril removal followed by partial burial.

Figure 4.
Imbibition curve for seeds of Copaifera langsdorffii.

Discussion

In this study we examined some of the factors that affect seed germination of Copaifera langsdorffii. Our results demonstrate that removing the aril is essential for seed germination in this species, since the maintenance of the aril completely inhibited seed germination. Studies show that zoochorous seeds have secondary compounds that inhibit germination (Cipollini & Levey. 1997; Yagihashi & Miyamoto 1998; Robertson et al. 2006). The presence of secondary compounds (e.g. coumarins) in arils may inhibit seed germination by one of two ways: by direct chemical inhibition or by influencing micro-environmental factors such as light and oxygen (Cipollini & Levey 1997). The characteristics of the seeds of C. langsdorffii indicate that germination inhibition is chemical, since the seeds are not photoblastic and the aril only partially covers the seed. Furthermore, the presence of the aril favors the growth of fungi, which may prevent seed germination (Ohkawara & Akino 2005Ohkawara K, Akino T. 2005. Seed cleaning behavior by tropical ants and its anti-fungal effect. Journal of Ethology 23: 93-98.). Our results also show that the seeds of C. langsdorffii do not exhibit physical dormancy, despite their slow water uptake (Baskin & Baskin 2004).

Aril removal positively affected germination. The treatments that simulated the effects of a disperser increased germination by about 50%. These results are in accordance with other studies (Leal & Oliveira 1998; Robertson et al. 2006; Christianini et al. 2007; Lessa et al. 2013; Lima et al. 2013), and demonstrate the potential benefits of the seed dispersal process on seed germination (Lima et al. 2013). These results suggest that dispersers, in addition to transporting seeds away from the mother plant and thus avoiding intraspecific competition and decreasing the likelihood of an attack by predators (Janzen 1970Janzen DH. 1970. Herbivores and number of tree species in tropical forests. The American Naturalist 104: 501-528. ; Swamy et al. 2011Swamy V, Terborgh J, Dexter KG, Best BD, Alvarez P, Cornejo F. 2011. Are all seeds equal? Spatially explicit comparisons of seed fall and sapling recruitment in a tropical forest. Ecology Letters 14: 195-201.), are essential in the germination success of C. langsdorffii. Furthermore, during passage through the digestive tract of a frugivore, the seeds become scarified such that structures that can reduce or even prevent germination may be removed. Such scarification can accelerate the speed of germination and increase the proportion of successful germinating seeds (Robertson et al. 2006).

In many cases, zoochorous seeds, being produced in large numbers, are not all consumed by a primary disperser and usually fall to the soil near the mother plant, becoming available to other groups of animals, among which are other important dispersers (Christianini & Oliveira 2010; Lima et al. 2013). Specifically, C. langsdorffii has supra annual mass reproduction with high fruit production (Fagundes et al. 2013; Souza et al. 2015) and many seeds may go uneaten in this manner. Studies have shown that in such cases, ants are important secondary seed dispersers, carrying the seeds far from the mother plant (see Christianini & Oliveira 2010). Also, by removing the arils, ants reduce the chances of fungal attack on the seeds fallen on the fungi-prone tropical forest floor (Lima et al. 2013).

Our results indicate that fire was not detrimental to the survival of seeds of C. langsdorffii. Historically, fires appeared concomitantly with the origin of land plants and have played an important role throughout the history of life (Pausas & Keeley 2009Pausas JG, Keeley J. 2009. A burning btory: The role of fire in the history of life. BioScience 59: 593-601.). Traits adaptive to fire, such as tolerance to high temperatures, increased plant fitness in these environments (Keeley et al. 2011). Studies in savannas have shown that some species adapted to these environments are able to tolerate high temperatures from the passage of fire (Delgado et al. 2008Delgado JA, Serrano JM, Lopez F, Acosta FJ. 2008. Seed size and seed germination in the Mediterranean fire-prone shrub Cistus ladanifer. Plant Ecology 197: 269-276.; Fichino et al. 2012Fichino B, Fidelis A, Schmidt I, Pivello V. 2012. Efeitos de altas temperaturas na germinação de sementes de capim-dourado (Syngonanthus nitens (Bong.) Ruhland, Eriocaulaceae): implicações para o manejo. Acta Botanica Brasilica 26: 508-511.; Ribeiro et al. 2013; Ribeiro & Borghetti 2014). Copaifera langsdorffii is a common tree species in tropical forest environments (Carvalho 2003), and fire tolerance may be an attribute important for the occurrence of this species in the Cerrado (Rizzini 1976Rizzini CT. 1976. Influência da temperatura sobre a germinação de diásporos do cerrado. Rodriguésia 28: 341-381.). Seeds of C. langsdorffii tolerate high temperatures, and the germination percentage increases after the passage of fire, which can be attributed to the control of microorganisms, such as fungi (Alencar et al. 2009Alencar KMC, Laura VA, Rodrigues APAC, Resende RMS. 2009. Tratamento térmico para superação da dormência em sementes de Stylosanthes SW. (Fabaceae Papilionoideae) . Revista Brasileira de Sementes 31: 164-170.). In fact, in our study, the seeds treated with fire had a low level of infestation by fungi.

Finally, our results show that biotic and abiotic factors can interact synergistically, affecting time to germination and the percentage of successful germinations of a zoochorous Neotropical tree. Evaluating the effects of dispersal on germination is important for understanding the qualitative effectiveness of seed dispersal, as well as elucidating the role that dispersers play in the population dynamics of plants (Schupp et al 2010Schupp E, Jordano P, Gomez JM. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188: 333-353.). The lack of germination among seeds with their arils intact demonstrates the importance of dispersal to the germination of C. langdorffii. Thus, conservation of viable habitat for the maintenance of dispersers is essential for the reproductive success of C. langsdoffii. Considering the approaches, results and analyses of the present study, additional investigations into germination in field conditions are needed to elucidate the factors that determine the spatial distribution and abundance of species in natural plant communities.

Acknowledgments

We thank all the collaborators of the Plant Physiology Laboratory - UFMG, for logistical support in the fieldwork. The authors are indebted to Thais Ferreira Costa for her valuable revision of the English version. We also thank the directors of FLORESTA NACIONAL DE PARAOPEBA for logistical support. This study was carried out with financial support from CNPq and FAPEMIG. The authors also acknowledge CAPES, CNPq and FAPEMIG for research grants.

References

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Publication Dates

  • Publication in this collection
    Oct-Dec 2015

History

  • Received
    11 Apr 2015
  • Accepted
    11 June 2015
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