Seed dispersal phenology and dispersal syndromes in a subtropical ...

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Author's personal copy Forest Ecology and Management 258 (2009) 1147–1152

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Seed dispersal phenology and dispersal syndromes in a subtropical broad-leaved forest of China Yanjun Du a,b, Xiangcheng Mi a, Xiaojuan Liu a, Lei Chen a, Keping Ma a,* a b

State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, No. 20 Nanxincun, Xiangshan, Beijing 100093, China Graduate University of Chinese Academy of Sciences, Beijing 100049, China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 3 March 2009 Received in revised form 31 May 2009 Accepted 2 June 2009

This study describes the dispersal phenology and syndromes in Gutianshan 24 ha plot in a subtropical broad-leaved forest of China. The 130 0.5 m2 seed traps collected 69,115 mature seeds, representing 27 species (belonging to 24 genera, and 15 families) in 12 months. One marked peak in the number of seeds and species during the year was found in dry season (November). Zoochory was the most common dispersal syndrome (70.4%), followed by anemochory (18.5%), ballistic dispersal (11.1%). Among fruit types, berry (33%), capsule (22%), nut (18%), and drupe (11%) were common in the subtropical evergreen forest. In fruit color, brown was the commonest (40%), followed by dark brown (30%), black (15%), red (11%), and yellow (4%). Overall, the community level seed rain study revealed that one marked peak in seed number occurred in the middle of dry season; zoochory was the principal dispersal mode of woody plants in subtropical forest, and dry seasons favor seed dispersal by animal and wind. ß 2009 Elsevier B.V. All rights reserved.

Keywords: Seed rain Dispersal mode Fruiting phenology Fruit color Seasonality Evergreen forest

1. Introduction Seed dispersal is a critical event in plant life history for the survival of populations, and the survival must link to various biotic and abiotic factors (Vanschaik et al., 1993). The diasporas of many plant species have characteristic morphological structures and traits that enhance their probability of being dispersed away from the mother plant (Tiffney, 1984; Hughes et al., 1994; Griz and Machado, 2001). Among these traits are fruit color, seed size and shape, and time of fruit ripening (Willson and Whelan, 1990). The most commonly used classification system of dispersal syndromes is based on the agent or vector of dispersal, typically inferred from seed morphology (Levin et al., 2003). The principal agents of dispersal are either abiotic or biotic, and the dispersal syndromes are termed, respectively, anemochory, ballistic, and zoochory. The proportion of dispersal modes in a particular vegetation type is defined as the dispersal spectrum, which is influenced by community attributes, environmental circumstances and floristic composition (Van der Pijl, 1982; Hughes et al., 1994). Although dispersal syndromes have many exceptions and are moderately predictive about dispersal mechanisms (Fleming et al., 1993), knowledge on dispersal spectra of plant communities is helpful for interpreting local ecology and for understanding factors that

* Corresponding author. Tel.: +86 10 62836223; fax: +86 10 62590835. E-mail address: [email protected] (K. Ma). 0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.06.004

control composition and structure of communities (Howe and Westley, 1988; Arbelaez and Parrado-Rosselli, 2005). Seed dispersal by animals predominates tropical forest plant species (Willson et al., 1989), and involves a tremendous diversity of animal species and behaviors. Animals may consume fruit and drop, spit or defecate the seeds, carry seeds in their coats or scatterhoard seeds for later consumption. Abiotic strategies such as wind, water and ballistic dispersal form the main mode of seed movement for the remaining 10–30% of tropical tree species (Willson et al., 1989). However, little research studies the seed dispersal syndromes in subtropical tree species. Seasonality exposes plants to periodic changes in the quality and abundance of resources (Fretwell, 1972). And almost all subtropical environments vary seasonally in temperature, rainfall, wind speed and daylength. All of these factors would play a role in triggering phenological changes in subtropical plants. A seasonal climate also brings about fluctuations in pollinators, seed dispersal agents, predators, and competitors (Griz and Machado, 2001). The activity of pollinators and seed dispersers, and breeding periods of animals depend on the seasonal production of flowers and fruits in the community. Phenological patterns are of great importance in determining the temporal changes, which constrain the physiological and morphological adaptations in plant community for utilization of resources (Herrera, 1986; Vanschaik et al., 1993; Selwyn and Parthasarathy, 2006) by fauna. However, phenological patterns of seed dispersal in subtropical broad-leaved forests are little known.

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In this paper, we address the following questions: (1) What is the pattern of seed dispersal phenology in the subtropical forest understory? (2) What is the dispersal mode for major woody plant species in subtropical forest? (3) Do climate or seasons favor one dispersal mode over another?

2. Materials and methods 2.1. Study site The study was conducted in a 24-ha permanent forest plot (29815.1010 –29815.3440 N, 118807.0100 –118807.4000 E) in Gutianshan National Nature Reserve (GNNR), Kaihua County, Zhejiang Province in eastern China. GNNR covers a total area of approximately 8107 ha. The topography is characterized by mountains with steep slopes. The substrate consists mainly of granite. The dominant soils can be classified into four types: red soil, red-yellow soil, yellow-red soil and marsh soil. The mean annual temperature is 15.3 8C. The hottest month is July with a mean temperature of 27.6 8C, and the coldest is January with a mean temperature of 4.7 8C. The mean annual precipitation is 1787 mm with seasonal distribution over the year (Yu et al., 2001). Wet season occurs from March to July, whereas dry season runs from August to February next year. The mean annual number of frost-free days is 250. A total of 1991 vascular plant species, belonging to 244 families and 897 genera, were recorded within the entire GNNR. The dominant vegetation type in GNNR is subtropical evergreen broad-leaved forest dominated by Castanopsis spp., Cyclobalanopsis spp. and Schima superba (Chen and Feng, 2002; Hu et al., 2003). 2.2. Methods 2.2.1. Plot set In 2005, a permanent plot covering 24-ha (400 m 600 m, horizontal distance) was established within the evergreen broadleaved forest in GNNR. The plot was established and data were collected following the plot standards of the CTFS (Center for Tropical Forest Science) network (Condit, 1998). The elevation range between the highest and lowest point in the plot was 269 m (from 446 to 715 m). The first tree census was conducted in 2005. All woody stems 1 cm in DBH were mapped, measured, identified, and tagged (Legendre et al., 2009). 2.2.2. Seed collection Seed rain has been censused weekly since June 2006, using 130 seed traps set along 2.3 km of trails within the plot (Wright and Calderoń, 1995; Wright et al., 1999). Each seed trap consists of a square, 0.5 m2 PVC frame supporting a shallow, open-topped, 1mm nylon mesh bag, and suspended 0.8 m above the ground on four PVC posts. All seeds, fruits, seed-bearing fruit fragments, flowers, capsules, and other reproductive parts of plants that fall into the traps were identified to species and recorded. Fruits were categorized as aborted, immature, damaged, fragments and mature. Because the seed traps were located above the ground, they captured fruits and seeds falling directly from trees, as well as those spat or defecated by birds, bats and arboreal mammals; they did not, however, record secondary dispersal by rodents and other terrestrial animals (Muller-Landau et al., 2008). All data presented refer to seed number, based upon either a count of actual seeds per fruit, or calculated based upon the mean number of seeds per fruit. Dispersal syndrome was assigned to each species based on fruit morphology and unpublished observations of fruit consumption. Each plant species was assigned to one main dispersal mode. Fruit

Fig. 1. The mean monthly temperature and rainfall during the period of study and in the 50-year mean.

morphology was the basis for classifying species as dispersed by wind, animals, or explosion. We also assigned the dispersal mode to each species by ‘‘Exclusion hypotheses’’ (Hughes et al., 1994). 3. Results Seed rain. The 130 understory seed traps collected 69,115 mature seeds, representing 27 species (belonging to 24 genera, and 15 families) in 52 weekly censuses between June 2006 and May 2007. Seed rain understory totaled 1064 seeds/m2 during the 12month period (total trap area = 65 m2). The Pearson correlation coefficient value between adult tree basal area and seed production is 0.456 (p = 0.000 < 0.01, n = 147). Dispersal Phenology. There were negative correlations between rainfall and seed number (R = 0.494, p = 0.103), between rainfall and seed species number (R = 0.812, p = 0.001 < 0.05) (Figs. 1 and 2). We found one marked peak in the number of seeds and species during the year (Fig. 2). The highest peak occurred in the middle of dry season (November), which accounts for 47.6% of seeds all the year (Figs. 1 and 2). The lowest number of fruiting species was found in June (55 seeds/month), July (188 seeds/month) and August (403 seeds/month) also showed few fruiting species. The number of seeds in wet season is 6582, which accounts for 10% of the total seeds of the year, and the number in dry season is 62,533 accounting for 90%. Seeds of ten species were collected during the dry season, while 23 species were collected during the wet season. Dispersal modes. Dispersal modes for all species are listed in Table 1. Three dispersal syndromes were considered: zoochory (animal dispersal), anemochory (wind dispersal), and ballistic dispersal. Zoochory was the most common dispersal mode, represented by 70.4% of all studied species, followed by anemochory (18.5%), and ballistic dispersal (11.1%) (Fig. 3). The most frequent families were Fagaceae (19%), Ericaceae (15%) and

Fig. 2. The number of seeds and number of species falling into the traps per month during the period of study.

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Table 1 Fruit type, dispersal units, diaspore color and dispersal syndromes of woody species from subtropical forest in East China (T, tree; S, shrub; Z, zoochory; A, anemochory; B, ballistic; F, fruit; S, seed). Species

Family

Life-forms

Fruit type

Diaspore color

Dispersal syndrome

Unit

Styrax dasyanthus Quercus serrata Murray Vaccinium carlesii Eurya muricata Machilus thunbergii Ternstroemia gymnanthera Daphniphyllum oldhami Corylopsis glandulifera Loropetalum chinense Vaccinium mandarinorum Itea chinensis Fraxinus insularis Pinus massoniana Rhododendron ovatum Schima superba Nyssa sinensis Cyclobalanopsis glauca Cyclobalanopsis myrsinaefolia Albizia kalkora Idesia polycarpa Lithocarpus glabra Castanopsis eyrei Vaccinium bracteatum Ilex micrococca Distylium myricoides Toxicodendron succedaneum Eurya rubiginosa

Styracaceae Fagaceae Ericaceae Theaceae Lauraceae Theaceae Daphniphyllaceae Hamamelidaceae Hamamelidaceae Ericaceae Saxifragaceae Oleaceae Pinaceae Ericaceae Theaceae Nyssaceae Fagaceae Fagaceae Leguminosae Flacourtiaceae Fagaceae Fagaceae Ericaceae Aquifoliaceae Hamamelidaceae Anacardiaceae Theaceae

S T S S T S S S S S S T T S T T T T T T T T S T S S S

Achene Nut Berry Berry Berry Berry Drupe Capsule Capsule Berry Capsule Samara Cone Capsule Capsule Drupe Nut Nut Legume Berry Nut Nut Berry Berry Capsule Drupe Berry

Brown Green Dark brown Dark brown Dark brown Red Dark brown Black Black Black Brown Black Brown Brown Brown Dark brown Brown Brown Brown Red Brown Dark brown Dark brown Red Brown Yellow Dark brown

Z Z Z Z Z Z Z B B Z A A A A A Z Z Z Z Z Z Z Z Z B Z Z

S S F F F S F S S F S S S S S F S S S F S S F F S F F

or T

or T or T or T or T

or T or T or T

Theaceae (15%) (Fig. 4). During one year’s collection, 11 families were only represented by one species each, 1 family by three species, 2 families by four species each, and 1 family by five species (Fig. 5). Among fruit types, berry (33%), capsule (22%), nut (18%), and drupe (11%) were common in the subtropical evergreen forest (Fig. 6). In fruit color, brown was the commonest (40%), followed by dark brown (30%), black (15%), red (11%), and yellow (4%) (Fig. 7). All berry (9 species) and nut fruits (5 species) were animal dispersal. Dark brown diaspore could be berry, nut, drupe, but all of them were dispersed by animals. All red fruits were berry, and only dispersed by animals. Nearly all zoochory species have deep fruit/seed color, like dark brown and red (Table 1). All five Fagaceae species were animal dispersed. Three-fourth Ericaceae species were also animal dispersed. All three Hamamelidaceae species were ballistic dispersed. Three of four Theaceae species were animal dispersed. All anemochory species have brown or black fruits (Table 1).

4. Discussion 4.1. Seed rain The seed rain of the Gutianshan was highly variable, but continuous throughout the year. During a one-year period, we collected seeds belonging to 27 species, out of a total of 159 species in the whole plot. The regression between adult basal area and seed rain suggests that

Fig. 4. Percentage of family during the study period.

Fig. 3. Dispersal modes in sub-tropical forest in East China. Percentage of species per dispersal mode relative to the total number of plant species collected.

Fig. 5. The number of species in each family.


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November must wait until March or April before reliable rains permit germination. If most seeds dispersed in wet season in subtropical forest, the seed would germinate immediately, and seedlings will suffer a long winter season which is unfavorable for seedling establishment. Here is a study on the reproductive phenology of Hong Kong shrubland in South China which exhibited similar patterns (Corlett, 1993). Seed rain has a December peak and a May–June low. The simplest adaptive explanations are either a phenological match with the migratory movements of millions of partly frugivorous birds (thrushes etc.) through subtropical Asia in October–November and/or diet switching by resident insectivorefrugivores as insect availability declines in the cool-dry season (Corlett, 1993). Liu (2000) studied the soil seed bank dynamics in a subtropical evergreen broad-leaved forest in China and found that most seeds germinated in April, which shows that most seeds postpone germination until more favorable conditions take place in the spring.

Fig. 6. Percentage of fruit types during the study period.

4.2. Dispersal syndromes

Fig. 7. Percentage of diaspore color during the study period.

interspecific variations in primary seed dispersal could be explained by average basal area of adults. The fundamental limitation on recruitment could be absence of parent trees. Unless seed production and dispersal are high, recruitment limitation is likely for many taxa simply on the basis of parent tree abundance. The seed rain averaged 1064 seeds m2 yr1, but the seed density we got maybe underestimated because some seeds might have been removed from seed traps by seed predator prior to our sampling. The time of reproduction is one of the traits that are directly affected by the availability of limiting resource, such as water (Volis, 2007). We found one marked peak both in the number of seeds and in the number of species in November. Even fleshy fruits matured during the dry season (e.g., Vaccinium carlesii, Eurya muricata, Vaccinium mandarinorum, Idesia polycarpa, Vaccinium bracteatum). This is not in agreement with previous reports at other sites (Frankie et al., 1974; Lieberman, 1982; Murali and Sukumar, 1994; Griz and Machado, 2001), where fruiting peaked during the wet season. This does not facilitate the germination of seeds, which depend largely on sufficient water availability. Although researchers held the view that fruiting peak may be related to environmental conditions both for dispersal (e.g., stronger winds during the dry season) and for germination, we thought that fruiting peak in dry season in our study is not related to germination, but for seedling establishment. This suggests that there are other advantages in winter fruiting. Seed dispersed in

We found that zoochory was the principal dispersal mode of plants in subtropical forest understory. Our results are similar to studies conducted in tropical forests around the world (Table 2, see also Selwyn and Parthasarathy, 2006). Study found that dispersal syndrome could explain significant variation in clumping of seed deposition (Muller-Landau et al., 2008). Dispersal by animals (particularly birds) could help seeds escape high mortality conditions near their parents, where predation, abundance of pathogens and intraspecific competition are at their highest (Janzen, 1970). Birds vary in their movement and fruit handling patterns, and therefore exert differing influences on seed viability and the spatial patterns of seed deposition (Howe, 1989, 1993; Clark et al., 2005). Anemochorous species only represent 18.5% of all species at this site, which is lower than other studies (Table 2). We think this may be because these forests have more open canopy vegetation, allowing greater wind circulation at all forest levels when compared to dense evergreen forests, particular during the dry season. In our study, anemochorous fruits were produced exclusively in the dry season. Dispersal by wind is more efficient during the dry season, because dry conditions favor the liberation of the seeds and allow their wings and plumes to fully expand (Sharpe and Fields, 1982). Ballistic dispersal represented 11.1% of all species at this site. All ballistic dispersal occurred in dry season. This is different from the previous studies which showed positive correlation with the occurrence of rain, suggesting the influence of rain in fruit dehiscence (Murray, 1986; Griz and Machado, 2001). This difference may be explained by the fact that precipitation in subtropical region is greater than that of arid environments, where it favors dispersal of seeds when conditions for germination, seedling establishment and growth are optimal (Gutterman, 1994). Many temperate-zone plants produce fruits that are adapted for seed dispersal by birds, and many of these fruits are conspicuously

Table 2 Comparison of frequency distribution and seasonal dominance of dispersal syndromes with other forests (blanks represent data not observed or not comparable from reference; A, anemochory; Z, zoochory). Sites

Zoochroy

Anemochory

%

(n)

%

(n)

Costa rica Cerrado, Brazil Ghana Caatinga, Brazil Colombia

50 52 75 36 47

(53) (142) (59) (15) (137)

30 30 25 32 23

(32) (81) (20) (13) (68)

Gutianshan, China

70

(19)

(18)

(5)

Duration of rainy Season (month)

Annual rainfall (mm)

Seasonal dominance Dry season

Rainy season

Reference

4 6 5 7 No marked rainy season 5

1533 1300 1100 549 3060

A A A A –

Z Z Z Z –

Frankie et al. (1974) Gottsberger and Silberbauer-Gottsberger (1983) Lieberman (1982) Griz and Machado (2001) Arbelaez and Parrado-Rosselli, 2005

1787

Z

–

This study


colored (Willson and Thompson, 1982). In our study, brown was the commonest, followed by dark brown, black, red, and yellow. This result is similar to other studies around the world (Turcek, 1963; Willson and Thompson, 1982; Van der Pijl, 1982). Turcek (1963) showed that black and red were common colors for European fruits whose seeds were dispersed by birds (see also Van der Pijl, 1982). Corlett (1996) studied 255 native plant species in Hong Kong and also showed that the commonest color of fruit is black, followed by red. It is similar in our sub-tropical forest where we differentiate deep brown and black, but actually they are close. Colorful displays of ripe fruit likely evolved in order to attract avian dispersal agents. Frugivorous birds thus serve as selective agents of plants by favoring those species whose seeds could disperse to potential ‘safe sites’. The subsequent seed dispersal pattern not only determines the potential area of plant recruitment, but also serves as a template for subsequent processes, such as predation, competition and mating (Nathan and Muller-Landau, 2000). Other colors such as yellow, green, and orange, frequently the colors of unripe fruits, were less popular (Willson and Thompson, 1982). The fruits of red, brown, deep brown color with pulp as a reward exhibit animal dispersal mode. The anemochory and ballistic species were almost brown fruits without any reward. 4.3. Seasonality Natural selection might favor plants with a pattern of reproductive phenophases dispersed throughout the growing season (Vanschaik et al., 1993). Our study showed that most seeds dispersed during the dry season, and it was also possible to find 10 species dispersed seeds during the wet season. This may be because the efficiency of dispersal depends on the number of seeds eaten, and if at one time of the year there are a greater number of seeds available than can be eaten, then the energy that went into the production of the surplus will be wasted. Conversely, if there are not enough seeds at one time of the year, then the potential dispersal agents will either starve or will eat something else (Smythe, 1970). And any species that fruits during this time will increase its chances of dispersal, which will ultimately promote recruitment. Our study showed that zoochory dominated the dry season, and this is different from previous studies. Griz and Machado (2001) found that zoochorous (i.e. fleshy) diasporas were most common during the rainy season at Caatinga, Brazil seasonally, which is in accordance with a previous case (Barbosa et al., 1989). The fact that zoochorous species showed a fruiting peak during the wet season follows a general pattern among tropical dry forests (Table 2, see also Bullock, 1995), where periods of greater precipitation seem to favors animal dispersal (Jackson, 1981; Gottsberger and Silberbauer-Gottsberger, 1983; Machado et al., 1997). There is evidence that the period of fleshy fruit production is associated with changes in behavioral patterns of dispersers (Smythe, 1970; Stiles, 1980; Wheelwright, 1985). However, studies on animal behaviors in Gutianshan subtropical forests are still scarce, and further work on possible relationships between the foraging behaviors of animals and fruiting patterns of zoochorous species in this community would be of great value. Although only one year of data was considered, the dispersal phenology pattern could be representative of subtropical evergreen broad-leaved forests based on findings by other studies at similar latitudes. One such study on the reproductive phenology of Hong Kong shrublands in South China (228170 N, 1148090 E) over a three years period showed similar patterns to what we found (Corlett, 1993). Community patterns of reproductive phenology are highly seasonal and vary little between years. Most species flowered and fruited every year but Machilus cf. thunbergii did not flower in 1988 and Rapanea neriifolia flowered but did not fruit in

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1989. A similar pattern, with a November–December fruiting peak, was seen in mostly woody species at Dinghushan Biosphere Reserve in South China (238100 N, 1128310 E) (Li and Wang, 1984). Au et al. (2006) studied seed rain in woody plant communities in Hong Kong (228250 N, 1148070 E), China, and also found similar patterns to those seen in our study in Gutianshan. They found that most seed rain occurred between September and January, with peaks in December and January. 5. Conclusion Overall, the community level seed rain study revealed that one marked peak in seed number occurred in the middle of dry season (November). The lowest seed number of fruiting species was found in wet season (June). Zoochory was the principal dispersal mode of plants in subtropical forest understory. Dry seasons favor seed dispersal by animal and wind. Our study will provide the needed knowledge which would contribute to study on seedling establishment and recruitment in subtropical forests. Further works should focus on possible relationships between the foraging behaviors of animals and fruiting patterns of zoochorous species in this community. We should also conduct a more detailed evaluation of the spatial patterns of adults and seed rain. Since only one year of data was considered in the study, we should continue to study the year to year variability in seed production and the phenology of dispersal. Acknowledgements We would like to thank Dr. Joe Wright and Dr. Helene MullerLandau for many discussion sessions which contributed to the formulation of the ideas presented here. We will also thank Mr. Fang Teng and Mr. Chen Bin for identifying dispersal modes for some species and two anonymous reviewers who help us improve this paper. We gratefully acknowledge the support from the Administration Bureau of the Gutianshan National Nature Reserve. This study was financed by Key Innovation Project of CAS (KZCX2YW-430). References Arbelaez, M.V., Parrado-Rosselli, A., 2005. Seed dispersal modes of the sandstone plateau vegetation of the middle Caqueta river region, Colombian Amazonia. Biotropica 37, 64–72. Au, A.Y.Y., Corlett, R.T., Hau, B.C.H., 2006. Seed rain into upland plant communities in Hong Kong, China. Plant. Ecol. 186, 13–22. Barbosa, D.C., Alves, J.L., Prazeres, S.M., Paiva, A.M.A., 1989. Dados fenolo´gicos de 10 espećies arbo´reas de uma a´rea de caatingga (Alagoinha PE). Acta Bot. Bras. 3, 109–117. Bullock, S.H., 1995. Plant reproduction in neotropical dry forests. In: Bullock, S.H., Mooney, H.A., Medina, E. (Eds.), Seasonally Dry Tropical Forests. Cambridge University Press, Cambridge, UK, pp. 277–297. Chen, J., Feng, Z., 2002. Study on geographical compositions of seed plant flora in Gutianshan Mountain of Zhejiang Province. J. East China Norm. Univ. (Nat. Sci.) 48, 104–111. Clark, C.J., Poulsen, J.R., Bolker, B.M., Connor, E.F., Parker, V.T., 2005. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 86, 2684– 2694. Condit, R., 1998. Tropical Forest Census Plots. Springer-Verlag, Berlin, Germany. Corlett, R.T., 1993. The reproductive phenology of Hong Kong shrubland. J. Trop. Ecol. 9, 501–510. Corlett, R.T., 1996. Characteristics of vertebrate-dispersed fruits in Hong Kong. J. Trop. Ecol. 12, 819–833. Fleming, T.H., Venable, D.L., Herrera-M, L.G., 1993. Opportunism vs. specialization: the evolution of dispersal strategies in fleshy-fruited plants. Vegetatio 107–108, 107–120. Frankie, G.W., Baker, H.G., Opler, P.A., 1974. Comparative phenological studies of trees in tropical wet and dry forests in lowlands of Costa-Rica. J. Ecol. 62, 881– 919. Fretwell, S.D., 1972. Populations in a seasonal environment. Monogr. Popul. Biol. 5, 1–217. Gottsberger, G., Silberbauer-Gottsberger, I., 1983. Dispersal and distribution in the Cerado vegetation of Brazil. Sonderbaende des Naturwissenschaftlichen Vereins in Hamburg 7, 315–352.

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