Wind-Generated Seed Shadow in Southern Brazil: The Influence of the Mother Plant and Wind Direction

Leone Genz Camila Kissmann About the authors

Abstract

Diaspore dispersal is an essential function of plant species, with effects on plant populations and natural forest dynamics. This study examines how traits of the mother plant (height, crown spread and distance from the diaspores) and the wind (wind speed) affect the spatial distribution of anemochorous diaspores of Apuleia leiocarpa, Peltophorum dubium, and Jacaranda micrantha in Southern Brazil. The number of diaspores from A. leiocarpa, P. dubium, and J. micrantha decrease with the increase in distance from the mother plant and there was no influence of wind direction on the spatial distribution of diaspores. Diaspore sizes of these plants were not related to their dispersal distances. Diaspore dispersal for A. leiocarpa was negatively correlated to the plant height and the crown spread. The dispersal of Peltophorum dubium and Jacaranda micrantha were not influenced by the diaspores and plants traits considered in this study.

Keywords:
Brazilian Atlantic Forest; biodiversity conservation; dispersal syndrome; spatial distribution of diaspores

1. INTRODUCTION AND OBJECTIVES

Dispersal is a critical ecological process with consequences for plant reproduction, population and community dynamics, and gene flow among populations (Croteau, 2010Croteau EK. Causes and consequences of dispersal in plants and animals. Nature Education Knowledge 2010; 3(10): 12.; Robledo-Arnuncio et al., 2014Robledo-Arnuncio JJ, Klein EK, Muller-Landau HC, Santamaría L. Space, time and complexity in plant dispersal ecology. Movement Ecology 2014; 2: 16. 10.1186/s40462-014-0016-3
https://doi.org/10.1186/s40462-014-0016-...
). Knowledge of dispersal strategies has long been recognized as important for understanding plant evolution processes, as well as for explaining current distribution of plants across landscapes (Kuhlmann & Ribeiro, 2016Kuhlmann M, Ribeiro JF. Evolution of seed dispersal in the Cerrado biome: ecological and phylogenetic considerations. Acta Botanica Brasilica 2016; 30(2): 271-182. 10.1590/0102-33062015abb0331
https://doi.org/10.1590/0102-33062015abb...
; Sadló et al., 2018Sádlo J, Chytrý M, Pergl J, Pyšek P. Plant dispersal strategies: a new classification based on the multiple dispersal modes of individual species. Preslia 2018; 90: 1-22. 10.23855/preslia.2018.001
https://doi.org/10.23855/preslia.2018.00...
). Nowadays, such knowledge has become essential to understand, predict and manage the responses of individuals, populations and species to ecosystem perturbation and climate changes (Robledo-Arnuncio et al., 2014Robledo-Arnuncio JJ, Klein EK, Muller-Landau HC, Santamaría L. Space, time and complexity in plant dispersal ecology. Movement Ecology 2014; 2: 16. 10.1186/s40462-014-0016-3
https://doi.org/10.1186/s40462-014-0016-...
).

The dispersal units of plants, called diaspores, comprise fruits, seeds or other plant particles (Van der Pijl, 1982Van Der Pijl L. Principles of dispersal in higher plants. 3rd ed. New York: Springer-Verlag; 1982.) moved away from the individual in which they were born to another location where they will settle and reproduce (Croteau, 2010Croteau EK. Causes and consequences of dispersal in plants and animals. Nature Education Knowledge 2010; 3(10): 12.). Diaspores can be dispersed by several agents, including biotic (animal or self-dispersal) and abiotic ones (such as wind or water) (Martins et al., 2014Martins VF, Cazotto LPD, Santos FAM. Dispersal spectrum of four forest types along an altitudinal range of the Brazilian Atlantic Rainforest. Biota Neotropica 2014; 14(1): 1-22. 10.1590/S1676-06020140003
https://doi.org/10.1590/S1676-0602014000...
). Anemochorous species exhibit diaspores of small size and mass that are light enough for dispersal by wind (Van der Pijl, 1982Van Der Pijl L. Principles of dispersal in higher plants. 3rd ed. New York: Springer-Verlag; 1982.). Such diaspores are classified as flyers (balloon, winged, plumed and dust diaspores), rollers or throwers (Van der Pijl, 1982Van Der Pijl L. Principles of dispersal in higher plants. 3rd ed. New York: Springer-Verlag; 1982.). They can alternatively be classified according to their morphological and aerodynamic traits in still air as floater, autogyro, rolling autogyro, undulator or helicopter (Augspurger, 1986Augspurger CK. Morphology and dispersal potential of wind-dispersed diaspores of Neotropical trees. American Journal of Botany 1986; 73(3): 353-363. 10.2307/2444078
https://doi.org/10.2307/2444078...
).

In addition to diaspores morphological and aerodynamic traits, factors such as wind conditions, height of the mother plant and characteristics of the surrounding vegetation influence the mean potential dispersal distance of anemochorous diaspores, which may be carried over long distances or be concentrated under the canopy of the mother plant (Horn et al., 2001Horn HS, Nathan RAN, Kaplan SR. Long-distance dispersal of tree seeds by wind. Ecological Research 2001; 16(5): 877-885. 10.1046/j.1440-1703.2001.00456.x
https://doi.org/10.1046/j.1440-1703.2001...
; Thomson et al., 2011Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 2011; 99(6): 1299-1307. 10.1111/j.1365-2745.2011.01867.x
https://doi.org/10.1111/j.1365-2745.2011...
). The spatial distribution resulting from the diaspore dispersal around the mother plant (source) is known as “seed shadow” (Nathan & Muller-Landau, 2000Nathan R, Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Tree 2000; 15(7): 278-285. 10.1016/S0169-5347(00)01874-7
https://doi.org/10.1016/S0169-5347(00)01...
). Studies about seed shadows on local and larger spatial scales enable the identification of differences in the seed dispersal of species, and consequently provide insights into the processes, which structure plant communities (Clark et al., 2005Clark CJ, Poulsen JR, Bolker BM, Connor EF, Parker VT. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 2005; 86(10): 2684-2694. 10.1890/04-1325
https://doi.org/10.1890/04-1325...
).

Many studies have shown that dispersal distances are strongly related to the seed dispersal mode (Arjona et al., 2018Arjona Y, Nogales M, Heleno R, Vargas P. Long-distance dispersal syndromes matter: diaspore-trait effect on shaping plant distribution across the Canary Islands. Ecography 2018; 41(5): 805-814. 10.1111/ecog.02624
https://doi.org/10.1111/ecog.02624...
; Seidler & Plotkin, 2006Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol 2006; 4(11): e344. 10.1371/journal.pbio.0040344
https://doi.org/10.1371/journal.pbio.004...
). Other studies have demonstrated that there is wide variation in dispersal distances among species that share the same seed dispersal mode (Clark et al., 2005Clark CJ, Poulsen JR, Bolker BM, Connor EF, Parker VT. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 2005; 86(10): 2684-2694. 10.1890/04-1325
https://doi.org/10.1890/04-1325...
; Muller-Landau et al., 2008Muller-Landau HC, Wright SJ, Calderón O, Condit R, Hubbell SP. Interspecific variation in primary seed dispersal in a tropical forest. Journal of Ecology 2008; 96: 653-667. 10.1111/j.1365-2745.2008.01399.x
https://doi.org/10.1111/j.1365-2745.2008...
). Researchers have recently been studying the influence of plant traits (such as growth form, height and others) on dispersal distances and seed shadow (Augspurguer et al., 2017; Tamme et al., 2014Tamme R, Götzenberger L, Zobel M, Bullock JM, Hooftman DAP, Kaasik A, Pärtel M. Predicting species’ maximum dispersal distances from simple plant traits. Ecology 2014; 95(2): 505-513. 10.1890/13-1000.1
https://doi.org/10.1890/13-1000.1...
; Thomson et al., 2011Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 2011; 99(6): 1299-1307. 10.1111/j.1365-2745.2011.01867.x
https://doi.org/10.1111/j.1365-2745.2011...
). For Neotropical species, Augspurguer et al. (2017) showed that wind dispersal is predicted more accurately by the plant height rather than by diaspore traits. These studies are scarce for tropical species from the Atlantic Forest, especially when anemochorous species and seasonal forests are considered.

While the effects of forest fragmentation (Herrera & García, 2010Herrera JM, García D. Effects of forest fragmentation on seed dispersal and seedling establishment in Ornithochorous Trees. Conservation Biology 2010; 24(4): 1089-1098. 10.1111/j.1523-1739.2010.01459.x
https://doi.org/10.1111/j.1523-1739.2010...
) and animal extinctions (Pires et al., 2018Pires MM, Guimarães PR, Galetti M, Jordano P. Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services. Ecography 2018; 41(1): 153-163. 10.1111/ecog.03163
https://doi.org/10.1111/ecog.03163...
) on animal-dispersed plants are well studied, the effects of such factors on wind-dispersed species remain unknown. Because wind-dispersed species seem to benefit from open environments (Silva et al., 2017Silva BG, Castello ACD, Koch I, Silva WR. Pathways affect vegetation structure and composition in the Atlantic Forest in southeastern Brazil. Acta Botanica Brasilica 2017; 31(1): 108-119. 10.1590/0102-33062016abb0402
https://doi.org/10.1590/0102-33062016abb...
), they are especially important for colonizing areas after natural or anthropogenic disturbances (Martini & Santos, 2007Martini AMZ, Santos FAM. Effects of distinct types of disturbance on seed rain in the Atlantic Forest of NE Brazil. Plant Ecology 2007; 190(1): 81-95. 10.1007/s11258-006-9192-6
https://doi.org/10.1007/s11258-006-9192-...
). In Europe, Montoya et al. (2008Montoya D, Zavala MA, Rodríguez MA, Purves DW. Animal versus wind dispersal and the robustness of tree species to deforestation. Science 2008; 320(5882): 1502-1504. 10.1126/science.1158404
https://doi.org/10.1126/science.1158404...
) observed that wind-dispersed species are more vulnerable to forest fragmentation than animal-dispersed species. In Brazil, studies about seed shadow of anemochorous species are scarce and the ones about the effects of Atlantic Forest fragmentation on the seed shadow of anemochorous species are nonexistent. Thus, improved understanding regarding the seed shadow of these species, as well as how the diaspores and plant traits influence them, is important for devising management strategies for these species and predicting the potential for recovery of such areas following natural (such as forest gaps) or anthropogenic disturbances.

Therefore, this study conducted a field experiment to evaluate the spatial distribution of anemochorous diaspores of Apuleia leiocarpa (Vogel) J.F. Macbr., Peltophorum dubium (Spreng.) Taub. and Jacaranda micrantha Cham. and their relationship with the distance from the mother plant, height and crown spread of trees and wind speed. Three emergent species were chosen to avoid the influence of plant growth form on the spatial distribution of the seeds. All studied species commonly occur in the emergent layer of the Seasonal Deciduous Forest and produce rolling autogyro diaspores. However, A. leiocarpa and P. dubium diaspores are fruits, while J. micrantha diaspores are seeds. In addition to being larger, P. dubium and A. leiocarpa diaspores are heavier than those of J. micrantha, as reported in literature (Lorenzi, 1992Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Nova Odessa: Instituto Plantarum; 1992.). Therefore, a larger percentage of J. micrantha diaspores should be expected compared with A. leiocarpa and P. dubium in areas distant from the mother plant. Specifically, the following questions are addressed: 1) Does the diaspore density of A. leiocarpa, P. dubium, and J. micrantha decrease with an increase in distance from the mother plant? 2) Does the dispersal distance of A. leiocarpa, P. dubium, and J. micrantha diaspores increase with an increase in tree height and crown spread? 3) Are the spatial distributions of A. leiocarpa, P. dubium, and J. micrantha diaspores influenced by wind direction?

2. MATERIALS AND METHODS

2.1. Study area

This study was conducted in the National Forest of Chapecó (Figure 1), in the western region of the state of Santa Catarina, southern Brazil (27° 5’ 19.9” S latitude and 52° 46’ 47.3” W longitude) (ICMBio, 2013Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio. Plano de manejo da Floresta Nacional de Chapecó: resumo executivo [Internet]. 2013 [cited 2014 June 30]. Available from: Available from: https://bit.ly/2SiBVXH
https://bit.ly/2SiBVXH...
). The National Forest of Chapecó covers 1,590.60 ha and is divided into three zones (called “glebas”): Gleba I (1,287.54 ha), Gleba II (302.62 ha) and Gleba III (0.433 ha) (ICMBio, 2013Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio. Plano de manejo da Floresta Nacional de Chapecó: resumo executivo [Internet]. 2013 [cited 2014 June 30]. Available from: Available from: https://bit.ly/2SiBVXH
https://bit.ly/2SiBVXH...
). This study was carried out in Gleba I. The natural vegetation in the National Forest of Chapecó comprises Mixed Ombrophilous Forest and Seasonal Deciduous Forest (ICMBio, 2013Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio. Plano de manejo da Floresta Nacional de Chapecó: resumo executivo [Internet]. 2013 [cited 2014 June 30]. Available from: Available from: https://bit.ly/2SiBVXH
https://bit.ly/2SiBVXH...
), with the latter characterized by the loss of the emergent tree foliage during autumn and winter (IBGE, 2012Instituto Brasileiro de Geografia e Estatística - IBGE. Manual técnico da vegetação brasileira. Rio de Janeiro; 2012.).

Figure 1
Localization of the National Forest of Chapecó, Santa Catarina State, Southern Brazil.

The climate in the region is Cfa according to the Köppen classification, i.e., a mesothermal humid subtropical climate with hot summers, rains distributed throughout the year, and severe frost (Köppen, 1948Köppen W. Climatologia: con un estudio de los climas de la terra. Pánuco: Fondo de Cultura Económica; 1948.). Data on monthly rainfall (mm), maximum wind speed (km/h) and wind direction during the study period (December 2014 to August 2015) were monitored by a weather station belonging to the Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina (Epagri; Ciram, [2015?]Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina - Epagri; Centro de Informações de Recursos Ambientais e de Hidrometeorologia de Santa Catarina - Ciram. Solicitação de informações [Internet]. [2015?] [cited 2015 Oct. 15]. Available from: Available from: https://bit.ly/39xCB1f
https://bit.ly/39xCB1f...
), located in Chapecó, 13 km from the study area.

2.2. Study species

Three deciduous native pioneer species with anemochorous dispersal that naturally occur in the seasonal deciduous forest were studied: Apuleia leiocarpa (Vogel) J. F. Macbr., Peltophorum dubium (Spreng.) Taub., and Jacaranda micrantha Cham. Apuleia leiocarpa and P. dubium, known by the common names of grapia and canafistula, respectively. They have ornamental and economic importance due to their wood qualities (Carvalho, 2003Carvalho PER. Espécies arbóreas brasileiras. Brasília: Embrapa; 2003.; Sobral et al., 2013Sobral M, Jarenkow JA, Brack P, Irgang B, Larocca J, Rodrigues RS. Flora arbórea e arborescente do Rio Grande do Sul, Brasil. São Carlos: Novo Ambiente; 2013.). Both species belong to the Fabaceae family (Carvalho, 2003; Felippi et al., 2012Felippi M, Maffra CRB, Cantarelli EB, Araújo MM, Longhi SJ. Fenologia, morfologia e análise de sementes de Apuleia leiocarpa (Vogel) J. F. Macbr. Ciência Florestal 2012; 22(3): 477-491. 10.5902/198050986616
https://doi.org/10.5902/198050986616...
) and their dispersal units are fruits, which are flattened and winged, and classified as samaroid legumes (Filardi et al., 2009Filardi FLR, Garcia FCP, Okano RMC. Caesalpinioideae (Leguminosae) lenhosas na Estação Ambiental de Volta Grande, Minas Gerais, Brasil. Revista Árvore 2009; 33(6): 1071-1084. 10.1590/S0100-67622009000600010
https://doi.org/10.1590/S0100-6762200900...
). The fructification period of A. leiocarpa in the state of Santa Catarina occurs from November to April (Simioni & Belotti, 2009Simioni K, Belotti A. Calendário para coleta e sementes florestais nativas: bioma Mata Atlântica região Sul. Chapecó: Argos; 2009.), while that of P. dubium from June to August (Carvalho, 2003; Simioni & Belotti, 2009). Jacaranda micrantha (Bignoniaceae), known by the common name of caroba, is important for its ornamental, medicinal and economic value (Carvalho, 2003; Sobral et al., 2013). J. micrantha diaspores are seeds, which are light, winged and flattened (Carvalho, 2003), and the fructification period of this species in Santa Catarina occurs between June and September (Carvalho, 2003; Simioni & Belotti, 2009). The three species are found in the emergent layer of the seasonal deciduous forest of the National Forest of Chapecó. The criteria for plant selection were: 1) adult trees, characterized by their reproductive activity; and 2) the isolation of the plant in the area, to avoid collecting seeds from other neighboring plants.

2.3.Experimental design

The diaspore dispersal was evaluated separately for each species, according to their reproductive phenology. Five adult plants of each species (A. leiocarpa, P. dubium and J. micrantha) were examined in the reproductive stage; which was identified by the presence of flowers and fruits. Three collectors were positioned in line for each plant at 1, 10 and 20 m from the stem in each of the four cardinal directions so that a total of 12 collectors were installed around each plant. Diaspore collectors of 1 m² were made of wood and nylon mesh (1 mm) and installed at 90 cm above the soil. The collectors were checked weekly during the entire dispersal period and all material deposited on it was collected and taken to the laboratory, where the number of diaspores was recorded. This number was consequently used to calculate the diaspore density at different distances and cardinal directions. The experimental period extended from December 2014 to August 2015.

Tree height was estimated by visually comparing the distance between the tree base and the tree top to an object of known height (10 m) (Durigan, 2003Durigan G. Métodos para análise de vegetação arbórea. In: Cullen L Jr, Rudran R Jr, Valladares-Pádua C, editors. Métodos de estudos em biologia da conservação e manejo da vida silvestre. Curitiba: Editora da UFPR; 2003. p. 455-479.), while the average crown spread was obtained by measuring the longest and shortest extent of the crown (Blozan, 2006Blozan W. Tree measuring guidelines of the Eastern native tree society. Bulletin of the Eastern Native Tree Society 2006; 1(1): 3-10.). Finally, we measured the length and width of one hundred diaspores found in the collectors to characterize their mean size. Length was measured from the base to the apex of the diaspore, and width was measured at their middle region.

2.4. Data analysis

A two-way analysis of variance (Anova) was performed for each species to test the effects of the distance (1, 10 and 20 m) and direction (North, South, East and West) on diaspore density. Twenty replicates (collectors) were used to evaluate the influence of distance from the mother plant and five replicates were used to evaluate the effect of direction. The Tukey test (p < 0.05) was used to compare the mean results. The correlation between plant height or crown spread and seed density in each distance and direction was also performed for each species using the Pearson correlation test (p < 0.05). Considering that the wind direction differed between the months, we separately performed One-way Anova for each species to test the differences between the directions in each month (p < 0.05). Statistical analyses were developed in the SigmaPlot version 12 software program.

3. RESULTS

The greatest accumulated precipitation during the study period was in July 2015, followed by January and June; the highest average wind speed (47 km/h) in this period was recorded in January (Figure 2). The wind prevailed in the East-Southeast (ESE) direction from December to February, and in the East direction from March to June; wind in in east-northeast (ENE) was recorded only in August (Figure 2).

Figure 2
Total monthly rainfall (mm), maximum wind speed (km/h) and wind traits (cardinal direction and degrees) in the municipality of Chapecó during the study period. The columns represent accumulated monthly precipitation (mm) and the points indicate the average values of the maximum wind speed. The bars indicate standard deviation. E: east, ESE: east-southeast, ENE: wind in east-northeast.

A. leiocarpa diaspore dispersal began in December 2014 with a peak in January (64% of the diaspores), followed by a large decrease in February (Figure 3a). Dispersal ended in April, when no diaspores were found in the collectors (Figure 3a). A total of 2.553 diaspores were recorded over the 134 days of the dispersal period. A density of 73 diaspores/m² were recorded at 1 m from the mother plant, 41 diaspores/m² at 10 m, and 13 diaspores/m² at 20 m.

Figure 3
Diaspore density of Apuleia leiocarpa, Peltophorum dubium and Jacaranda micrantha collected monthly in the National Forest of Chapecó between December 2014 and August 2015.

The dispersal period of P. dubium lasted from January to August 2015, with a peak in March (21% of the dispersal), followed by a small decline the next month, and then remaining constant until June. A second dispersal peak was observed in July, before ending completely in August (Figure 3b). A total of 3.364 diaspores were collected for 204 days. The densities were 128 diaspores/m² at 1 m from the mother plant, 31 diaspores/m² at 10 m, and 9 diaspores/m² at 20 m from the mother plant.

The dispersal period for J. micrantha extended from April to August 2015, and the dispersal peak was observed in May 2015 (63%). A sharp reduction in dispersal was observed in June and it ended completely in August (Figure 3c). The dispersal period lasted for approximately 127 days in which 4,748 diaspores were collected, with densities of 126 diaspores/m² at 1 m, 75 diaspores/m² at 10 m, and 36 diaspores/m² at 20 m from the mother plant.

The dispersal peak of A. leiocarpa was observed in January, coinciding with the month of high wind speed and precipitation, which may have contributed to greater synchronization in the abscission of its diaspores (Figures 2 and 3). On the other hand, the dispersal period of P. dubium coincided with a reduction in the wind speed, which may explain its longer diaspore dispersal period (Figures 2 and 3).

There was no interaction between the distance from the mother plant and cardinal directions regarding diaspore density in any of the studied species (p > 0.05). When the factors were evaluated separately, we observed higher diaspore density of the three species near the mother plant, which decreased with increasing distance from the mother plant (Figures 4a, 4c, 4e). Apuleia leiocarpa and J. micrantha exhibited more diaspores at 1 m than at 10 m, which in turn was higher than the amount collected at 20 m (p < 0.05) (Figures 4a, 4e). The amount of P. dubium diaspores dispersed at 10 m and 20 m was similar, but lower than those collected at 1 m from the mother plant (Figure 4c). The diaspore dispersal was not influenced by the cardinal directions (p > 0.05) (Figures 4b, 4d, 4f). The means varied between 40 ± 30.7 and 47.1 ± 28.6 for A. leiocarpa, 51.1 ± 92.5 and 62.6 ± 94.6 for P. dubium, and 74.2 ± 43.1 and 86.5 ± 42.3 for J. micrantha. No differences were observed between the cardinal directions for any species, even when the dispersal was evaluated in each month separately (p > 0.05) (Figure 5).

Figure 4
Density of diaspores (number of diaspores/m2 ± standard deviation) of Apuleia leiocarpa (a and b), Peltophorum dubium (c and d), and Jacaranda micrantha (e and f) as a function of distance from the mother plant (a, c, and e) and the cardinal directions (b, d, and f) in the National Forest of Chapecó. The absence of letters indicates the lack of significant difference, and distinct letters show significant differences between means by the Tukey test (p > 0.05).

Figure 5
Density (number of diaspores/m2) and standard deviation of Apuleia leiocarpa (a), Peltophorum dubium (b), and Jacaranda micrantha (c) diaspores in the cardinal direction in each month along the dispersal period in the National Forest of Chapecó. The absence of letters indicates the lack of significant difference, and distinct letters show significant differences between means by the Tukey test (p > 0.05).

Negative correlations were observed for dispersal of A. leiocarpa diaspores in relation to both the height of the mother plant and the crown spread, so that the higher the plant height and the crown spread, the lower the number of diaspores dispersed at 1 and 10 m. The number of diaspores at 20 m from the mother plant was only influenced by the height of the mother plant. P. dubium and J. micrantha dispersal were not influenced either by the height of the mother plant nor by the crown spread (Table 1).

Table 1
Pearson correlation coefficients and p-values (in parenthesis) of the relationship between plant height, crown spread, total diaspore density, distance from the mother plant and cardinal directions for Apuleia leiocarpa, Peltophorum dubium and Jacaranda micrantha dispersal in the National Forest of Chapecó.

The length and width of diaspores differed among the species. Peltophorum dubium diaspores (fruits) exhibited the highest lengths, followed by A. leiocarpa and J. micrantha. On the other hand, A. leiocarpa diaspores (fruits) exhibited the highest width (Table 2).

Table 2
Mean length and width and standard deviation of Apuleia leiocarpa, Peltophorum dubium, and Jacaranda micrantha diaspores collected in the National Forest of Chapecó during the 2014/2015 dispersal period. Total diaspores by species = 100.

4. DISCUSSION

Although the diaspores of the three studied species share the characteristics of being winged and flattened, there was variation in diaspore size. The length of P. dubium diaspores was almost twice as high than the length of A. leiocarpa diaspores, which in turn were also almost twice as high than the length of J. micrantha diaspores. However, these diaspore traits do not seem to influence the diaspore dispersal of these species, as all of them showed a higher number of diaspores near the mother plant.

Adaptations of anemochorous diaspores increase the probability of dispersal to areas which are distant from the mother plant (Augspurger, 1986Augspurger CK. Morphology and dispersal potential of wind-dispersed diaspores of Neotropical trees. American Journal of Botany 1986; 73(3): 353-363. 10.2307/2444078
https://doi.org/10.2307/2444078...
). However, in our study we observed that most diaspores were deposited under or near the canopy of the mother plant. Such accumulation of diaspores near the mother plant, as observed for the three species studied herein, is commonly reported for a great number of plant species, regardless of their dispersal mechanism (Almeida-Cortez, 2004Almeida-Cortez JS. Dispersão e banco de sementes. In: Ferreira AG, Borghetti F, editors. Germinação: do básico ao aplicado. Porto Alegre: Artmed; 2004. p. 225-236.; Clark et al., 2005Clark CJ, Poulsen JR, Bolker BM, Connor EF, Parker VT. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 2005; 86(10): 2684-2694. 10.1890/04-1325
https://doi.org/10.1890/04-1325...
). Regarding anemochorous species, Lopes et al. (2010Lopes SF, Oliveira AP, Neves SB, Schiavini I. Dispersão de sementes de uruvalheira (Platypodium elegans VOG.) (Fabaceae) em um cerradão, Uberlândia-MG. Revista Árvore 2010; 34(5): 807-813. 10.1590/S0100-67622010000500006bbb
https://doi.org/10.1590/S0100-6762201000...
) also observed a decline in the density of diaspores with distance from the mother plant, regardless of their morphological adaptations.

The dispersal units of A. leiocarpa and P. dubium are fruits classified as samaroid legumes (Filardi et al., 2009Filardi FLR, Garcia FCP, Okano RMC. Caesalpinioideae (Leguminosae) lenhosas na Estação Ambiental de Volta Grande, Minas Gerais, Brasil. Revista Árvore 2009; 33(6): 1071-1084. 10.1590/S0100-67622009000600010
https://doi.org/10.1590/S0100-6762200900...
), which have pericarp projections to aid in anemochorous dispersal, whereas the dispersal units of J. micrantha are the seeds themselves, which have tegument expansions (called wings) to aid in dispersal. Moreover, Apuleia leiocarpa and P. dubium fruits may also be dispersed both by barochory and by anemochory (Carvalho, 2003Carvalho PER. Espécies arbóreas brasileiras. Brasília: Embrapa; 2003.). Thus, we expected that J. micrantha seeds would present more seeds at 10 and 20 m than at 1 m from the mother plant, whereas A. leiocarpa and P. dubium would present a higher number of fruits at 1 m from the mother plant. Contrary to our expectations, J. micrantha presented higher diaspore density at 1 m than at 10 and 20 m from the mother plant, similar to those observed for the other two species.

The seed dispersal distance for some species may be more strongly correlated with the plant than with diaspore traits (Augspurger et al., 2017Augspurger CK, Franson SE, Cushman KC. Wind dispersal is predicted by tree, not diaspore, traits in comparisons of Neotropical species. Functional Ecology 2017; 31(4): 808-820. 10.1111/1365-2435.12791
https://doi.org/10.1111/1365-2435.12791...
; Thomson et al., 2011Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 2011; 99(6): 1299-1307. 10.1111/j.1365-2745.2011.01867.x
https://doi.org/10.1111/j.1365-2745.2011...
). Indeed, the dispersal of A. leiocarpa diaspores in our study was more influenced by plant traits (height and crown spread) than by diaspore size. The height and the crown spread of the mother plant negatively affected the diaspore dispersal of this species. However, we did not observe such influence for the other two species.

In addition to the diaspores and plant traits, dispersal is also influenced by environmental factors such as wind traits and the surrounding vegetation. In order to facilitate the dispersal of diaspores far from the mother plant, anemochorous species must reach a great height and emerge from the forest canopy to gain exposure to the winds that are practically non-existent in a continuous canopy (Horn et al., 2001Horn HS, Nathan RAN, Kaplan SR. Long-distance dispersal of tree seeds by wind. Ecological Research 2001; 16(5): 877-885. 10.1046/j.1440-1703.2001.00456.x
https://doi.org/10.1046/j.1440-1703.2001...
). Although Apuleia leiocarpa, P. dubium, and J. micrantha are emerging species of seasonal forests (Lindenmaier & Budke, 2006Lindenmaier DS, Budke JC. Florística, diversidade e distribuição espacial das espécies arbóreas em uma floresta estacional na Bacia do Rio Jacuí, Sul do Brasil. Pesquisas 2006; 57: 193-216.), their heights may not have been sufficient to place these species in the emergent layer of the forest. The Apuleia leiocarpa, P. dubium, and J. micrantha plants sampled in this study presented mean heights of 20.6 ± 1.5, 23.6 ± 2.4 and 18.6 ± 1.9 m (means ± standard deviation), respectively; however, according to Lorenzi (1992Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Nova Odessa: Instituto Plantarum; 1992.) and Sobral et al. (2013Sobral M, Jarenkow JA, Brack P, Irgang B, Larocca J, Rodrigues RS. Flora arbórea e arborescente do Rio Grande do Sul, Brasil. São Carlos: Novo Ambiente; 2013.), such species can reach heights of between 35 and 40 m. Thus, the higher diaspore density observed near the mother plant for the studied species in the National Forest of Chapecó is possibly related to both the low tree height of plants and to the proximity of arboreal individuals of non-deciduous species which form physical barriers that decrease the effectiveness of the dispersal vector (wind) (Fenner, 1985Fenner M. Seed ecology. London: Chapman and Hall; 1985.).

Although variations were observed in the predominant direction of the wind during the study period, we recorded no preferential distribution of the diaspores of any species in any cardinal direction. This observation may also be related to the density of plants (i.e. a greater number of physical barriers against the wind action) in the National Forest of Chapecó, as many plant species from the Seasonal Forests of Southern Brazil tend to exhibit aggregated distribution (Loregian et al., 2012Loregian AC, Silva BB, Zanin EM, Decian VS, Oliveira CH, Budke JC. Padrões espaciais e ecológicos de espécies arbóreas refletem a estrutura em mosaicos de uma floresta subtropical. Acta Botanica Brasilica 2012; 26(3): 593-606. 10.1590/S0102-33062012000300009
https://doi.org/10.1590/S0102-3306201200...
; Sühs & Budke, 2012Sühs RB, Budke JC. Spatial distribution, association patterns and richness of tree species in a seasonal forest from the Serra Geral formation, southern Brazil. Acta Botanica Brasilica 2011; 25(3): 605-617. 10.1590/S0102-33062011000300014
https://doi.org/10.1590/S0102-3306201100...
).

The diaspore dispersal of P. dubium and J. micrantha occurred simultaneously among the individuals of each species as diaspores were found in all collectors during the dispersal period of each species. The dispersal of P. dubium extended for a longer period than expected based on previous studies (Carvalho, 2003Carvalho PER. Espécies arbóreas brasileiras. Brasília: Embrapa; 2003.; Simioni & Belotti, 2009Simioni K, Belotti A. Calendário para coleta e sementes florestais nativas: bioma Mata Atlântica região Sul. Chapecó: Argos; 2009.). The dispersion timing as well as month of occurrence are associated with dispersion vector availability. In the case of anemochorous species such as those studied herein, wind is the primary vector. It is responsible for both the separation of diaspores from the mother plant and the subsequent dispersal to distant locations (Greene, 2005Greene DF. The role of abscission in long-distance seed dispersal by the wind. Ecology 2005; 86(11): 3105-3110. 10.1890/04-1430
https://doi.org/10.1890/04-1430...
). Thus, the abscission of certain anemochorous diaspores may be conditioned by the occurrence of winds which are strong enough to cause such separation (Augspurger & Franson, 1987Augspurger CK, Franson SE. Wind dispersal of artificial fruits varying in mass, area and morphology. Ecology 1987; 68(1): 27-42. 10.2307/1938802
https://doi.org/10.2307/1938802...
; Deminicis et al., 2009Deminicis BB, Vieira HD, Araújo SAC, Jardim JG, Pádua FT, Chambela Neto A. Dispersão natural de sementes: importância, classificação e sua dinâmica nas pastagens tropicais. Archivos de Zootecnia 2009; 58: 35-58.). The dispersal of P. dubium diaspores occurred in the period of reduced wind speed in the region, and as such this may have contributed to the longer diaspore dispersal time observed in this study. According to Durigan et al. (1997Durigan G, Figliolia MB, Kawabata, M, Garrido MAO, Baitello JB. Sementes e mudas de árvores tropicais. São Paulo: Páginas e Letras; 1997.), P. dubium fruits are dispersed slowly by the wind and the ripe fruits remain in the trees for an extended time, as observed in this study. On the other hand, A. leiocarpa showed maximum dispersion in January, when higher wind speeds and precipitation probably contributed to the greater synchronization in diaspore abscission.

5. CONCLUSION

Our results showed that the diaspore density of A. leiocarpa, P. dubium, and J. micrantha decrease with the increase in distance from the mother plant. Diaspore sizes of these plants were not related to their dispersal distances. Diaspore dispersal of A. leiocarpa was negatively correlated to the plant height and the crown spread. The spatial distribution of diaspores was not influenced by wind direction.

ACKNOWLEDGEMENTS

L. Genz thanks the Fundo de Apoio à Manutenção e ao Desenvolvimento da Educação Superior (Fumdes) for the master scholarship. The authors thank the Universidade Comunitária da Região de Chapecó (Unochapecó) for the support.

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Publication Dates

  • Publication in this collection
    22 June 2020
  • Date of issue
    2020

History

  • Received
    21 Dec 2017
  • Accepted
    03 Jan 2019
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