Download Relative Importance of Seed-Bank and Post

BIOTROPICA ]](]]): 1–5 2009
10.1111/j.1744-7429.2009.00605.x
Relative Importance of Seed-Bank and Post-Disturbance Seed Dispersal on Early Gap
Regeneration in a Colombian Amazon Forest
Luis S. Castillo1 and Pablo R. Stevenson
Universidad de Los Andes, Laboratorio de Ecologı́a de Bosques Tropicales y Primatologı́a, Centro de Investigaciones Ecológicas La Macarena,
Carrera 1a No. 18a- 12, Bogotá, Colombia
ABSTRACT
Early forest gap regeneration may be generated by postdisturbance seed rain and by seed, seedling or bud banks (i.e., resprouting). The relative importance of each
process may depend on several factors (e.g., fruit/seed production, abundance and behavior of seed dispersers, gap characteristics, etc.). We experimentally compared
the importance of seed-bank and seed-rain affecting early recruitment of seedlings in an Amazonian forest (Zafire Biological Station, Colombia), using soil transplants
from forests to gaps and seed rain enclosures. We found that, during the 8-mo study, the seed-bank contributed with a larger number of individuals and species than
seed-rain. The low seedling recruitment rates may be associated with reduced populations of animal seed-dispersers due to hunting and/or low levels of forest fruit
production.
Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp
Key words: pioneer plants; secondary succession; seed dormancy; seed rain; Zafire Biological Station.
NATURAL GAPS MAY PLAY IMPORTANT ROLES in forest regeneration,
floristic composition, and diversity in tropical forests. Canopy gaps
contribute to environmental heterogeneity and, consequently, provide more niches to be exploited by organisms (Grubb 1977, Connell 1978, Denslow 1987, Wright 2002). The intermediate
disturbance hypothesis describes how frequency, magnitude and
time since disturbance may affect plant diversity, and predicts that
the highest number of coexisting species should be found at intermediate magnitudes of these processes (Connell 1978). Gap regeneration is a complex process since dynamics are affected by a variety
of factors associated with gap size and age, the surrounding plant
and animal communities, weather, and human intervention,
among others (Schupp et al. 1989).
Gap regeneration arises from four different sources: (1) the
seed bank which refers to the seeds dormant or transient in the soil
(Swaine & Hall 1983, Lawton & Putz 1988, Dalling & Hubbell
2002, Martins & Engel 2007); (2) the seedling bank, including recently germinated plants that were present in the site before gap
formation (Teketay 1997, Frey et al. 2007); (3) the bud bank, representing damaged plants able to sprout after gap formation (Bond
& Midgley 2001, Klimešová & Klimeš 2007); and (4) the postdisturbance seed rain that corresponds to the seeds arriving to the
gap after disturbance (Schupp et al. 1989, Gorchov et al. 1993,
Estrada-Villegas et al. 2007). Few studies have made experimental
approaches to quantify regeneration dynamics in gaps (Dalling &
Hubbell 2002), and to our knowledge only Lawton and Putz
(1988) have compared the importance of seed bank and postdisturbance seed rain in this process in a Costa Rican cloud forest. The
aim of this study was to experimentally evaluate the relative importance of seed banks and seed rain in early seedling recruitment in
Received 13 April 2009; revision accepted 5 September 2009.
1
Corresponding author; e-mail: [email protected]
natural Amazonian forest gaps, using a novel approach, with some
elements from Lawton and Putz (1988).
METHODS
STUDY SITE.—Field work was conducted in a continuous, unlogged
terra firme Amazonian forest in Zafire Biological Station
(4100 0 0000 S, 69153 0 5700 W, 130 m asl) between September 2007
and April 2008. The station is 27 km north of Leticia city (Colombia). Temperature is on average 261C, with low variation over the
year, and mean monthly precipitation is 280 mm, without consistent dry seasons (minimum monthly precipitation ca 160 mm), although the months with less rainfall tend to occur between June and
August (IDEAM Institute 2001). We conducted the experiments in
ten recently formed natural gaps (range: 2–24 mo old) distributed in
25 ha of forest, each one with an area of 101–309 m2 (174.4 67.2
SE) and average canopy openness of 21.7 percent (8.2–39.5%).
SOIL SAMPLES AND TREATMENTS.—We used four different treatments
in each gap: seed-bank (SB), seed-bank plus seed-rain (SB1SR),
seed-rain (SR), and a control (C). The SB treatment consisted of
the transport of soil from primary forest to the gap and the obstruction of seed-rain with nylon nets (0.5 0.5 mm pores). Soil
samples were collected from 0–10 cm deep, a depth at which many
seeds are deposited by secondary seed dispersers (Andresen & Levey
2004) and are able to form the seed bank. The litter present in the
soils was not excluded from the samples. In this treatment, all recruits came only from the seeds that were present in the primary
forest soil bank. The SB1SR treatment differed from the SB treatment because it did not have the exclusion net. In this treatment,
recruitment included seedlings emerging from the seed bank and
the seed rain. The SR treatment consisted of sterilized primary
forest soil, which then was carried to the gaps. The sterilization
r 2009 The Author(s)
Journal compilation r 2009 by The Association for Tropical Biology and Conservation
1
2
Castillo and Stevenson
consisted in placing the soil sample during 2 h in a closed pot that
was inside another pot with boiling water (Bell & Williams 1998).
In the SR treatment, all seeds were killed so that recruits came only
from the seed rain. The C treatment differed from the SR treatment
because it had a net that prevented the arrival of seeds, thus we also
excluded recruitment from the seed rain. The estimated volume of
soil for each treatment was about 45 L (100 50 cm wide, 8–10 cm
deep). All soil samples were taken from primary forest at least 30 m
away from the corresponding gap and were situated randomly inside holes with the same dimensions and at least 2 m away from gap
edge. The nets were box-shaped and situated upside down at 5 cm
above the ground to allow the movement of small seed and seedling
predators. This nylon net had larger dimensions than the area with
translocated soil samples (110 60 cm wide, 60 cm high), to reduce seed rain contamination through the space between the net
and the ground. For the SB, SR, and SB1SR treatments we performed two repetitions in each gap and the average was used in
subsequent analyses as replicates. Our methodology resembles the
protocol used by Lawton and Putz (1988), since both studies included translocation of primary forest sample soils to gaps, exclosures to isolate the effect of the seed rain, and soil sterilization. This
study differs in two main aspects: (1) they spread the mature forest
samples (1000 cm2) in a larger area (3600 cm2) inside gaps; and (2)
in their study, the soil was sterilized with carcinogenic methyl-bromide application. As a result, chemical residuals might be affecting
soil microorganism colonization and germination of seeds that
come from postdisturbance dispersion.
MEASURED VARIABLES AND STATISTICS.—Recruited vascular and nonvascular seedlings 4 1 cm were identified to morphospecies and
marked to assess their fate over the next 8 mo. For each treatment in
each gap we recorded the number of individuals, the cumulative
number of individuals, species richness and calculated Simpson’s
reciprocal index of diversity [index = 1/Sp2, where p represents the
proportion of individuals of morphospecies i in the population
(Krebs 1999)]. Measurements were taken weekly for the first 2 mo,
fortnightly for the next 2 mo, and a final reading 4 mo later. To
evaluate the statistical differences among treatments over time, and
since the assumption of sphericity of the variances (i.e., that differences of variances between any time period are the same) could not
be met (Mauchly’s test for all variables; W = 0, P o 0.001), we used
two alternatives to a repeated measures (RM) test: (1) we adjusted
the RM F-ratio using a Greenhouse–Geisser (G–G) analysis; and (2)
we summarized the responses for each treatment/time as a single
value: the slope obtained in a regression analysis using log-transformed data (Quinn & Keough 2002, Gotelli & Ellison 2004). The
calculated treatment slopes were measured in each gap as replicates
and their means and variances were compared with a Kruskal–Wallis
(K–W) test and, subsequently, with a Tukey multiple comparisons
test. The significance level used was 0.05.
RESULTS
New seedlings first emerged during the second week after the treatments were set up in all gaps. During the following 6 weeks, the
seedling emergence rate was relatively high and similar in the SB
and the SB1SR treatments, but it gradually declined there after. In
contrast, seedling emergence was very low in the SR and C treatments throughout the study (Fig. 1). Significant differences were
observed between two groups of treatments (SB = SB1SR 4 SR
= C) for all parameters (G–G RM test: number of individuals:
Ftreat = 19.4, Ftreatweek = 11.0; cumulative number of individuals:
Ftreat = 20.1, Ftreatweek = 15.0; number of morphospecies: Ftreat
= 19.6, Ftreatweek = 10.7; and Simpson’s reciprocal index of diversity: Ftreat = 14.1, Ftreatweek = 5.68, P values o 0.001; and K–W
test of slopes: w2 = 29.0; w2 = 29.9; w2 = 28.7; w2 = 22.6, respectively,
P values o 0.001; Table S1). The most abundant taxa recruiting
were mainly pioneer species: Cecropia spp. (Urticaceae), some
members of Melastomataceae, Apeiba sp. (Malvaceae), and members of Dilleniaceae, Solanaceae, Annonaceae and Poaceae. The
representation of shade tolerant species (e.g., Iryanthera sp.) was
small in all treatments (6.6% of individuals in week 32).
DISCUSSION
In our study, the seed-bank played an important role in early gap
regeneration compared with that from the seed rain. This pattern
has been found in other studies (e.g., upland evergreen forest in
Ghana: Swaine & Hall 1983; cloud forest in Costa Rica: Lawton &
Putz 1988; moist tropical forest in Panamá: Dalling & Hubbell
2002; and seasonal semideciduous tropical forest in Brazil: Martins
& Engel 2007), where the recruiting seedling community tightly
reflected the seed bank composition. In our two seed bank treatments (SB and SB1SR), seed germination of pioneer species began
in the first 2 weeks as a consequence of favorable conditions to
which the seeds were exposed (Bazzaz & Pickett 1980, Garwood
1983, Kozlowski 2002). At the end of the experiment, these two
seed bank treatments had more than six times the number of individuals and accumulated number of individuals, and three times the
morphospecies richness and diversity, than those in the seed rain
treatment and control. Seed rain after gap formation played a minor role in the early natural regeneration process in our site during
the study period.
The data showed a nonsignificant trend for higher seedling
emergence in the SB treatment compared with the SB1SR treatment (Figs. 1A and B). Possibly, independent of the species, the
nylon net could reduce seedling predation, reduce seed removal (by
predators and rainfall), and increase seedling survival (i.e., reducing
the variability in humidity, temperature, and radiation). The sterilization method used in the SR and C treatments could reduce
microorganism populations in the soil potentially affecting seedling
emergence, growth, and survival. Nevertheless, since there were no
physical or chemical barriers, we assumed that microorganisms
could colonize in these soils again. We also assumed that the soil
sterilization method did not considerably change the soil physical
and chemical characteristics. The control treatment showed a reduced number of germinated seedlings, similar to the SR treatments. All those seedlings are of pioneer plants. We assume that the
great proportion of those seedlings came from horizontal dispersion
(e.g., earthworms: Willems & Huijsmans 1994; ants: MacMahon
Seed-Bank vs. Seed-Rain in Early Gap-Dynamics
3
FIGURE 1. Effects of experimental treatments (seed-bank plus seed rain [SB1SR], seed bank [SB], seed rain [SR] and control [C]) through time on four parameters
of early gap regeneration dynamics: (A) mean number of individuals; (B) mean cumulative number of individuals; (C) mean number of morphospecies; and (D) mean
reciprocal Simpson’s index. Sampling was performed in 10 different gaps. Each gap contained one 0.5 m2 sample of each treatment in the Zafire Biological Station,
Colombian Amazon. The ‘a’ group differs statistically from the ‘b’ group of treatments (Kruskal–Wallis test of Slopes and Greenhouse-Geisser RM analysis,
P o 0.001). Error bars correspond to 95% CI.
et al. 2000; dung beetles: Andresen 2001; and abiotic factors such as
wind and runoff), rather than ineffective sterilization or nylon net
seed permeability.
At the end of the study seedling mortality was close to 30
percent in all treatments. It is possible that during the gap regeneration process, at some point, the recruitment rates from seed
rain will become higher than those from the seed bank, due to a
continuous seed input from the seed rain. Then, in the long run,
the relative importance of these sources of recruitment will
depend on the size of gaps and seed dispersal processes (Hubbell
et al. 1999).
The differences between seed rain and seed bank recruitment
in early regeneration have many explanations that are not exclusive.
(1) The seed bank has more time to build up than the seed rain
(Swaine 2001), and a great proportion of these seeds (i.e., pioneer
species), can be dormant for a long period of time. (2) In contrast to
the seed bank, seed rain could depend more closely on plants fruiting during the study period and on biotic and abiotic dispersal
agents. Thus, dispersal limitation may affect the recruitment of
plants from the seed rain (Hurtt & Pacala 1995, Hubbell et al.
1999, Nathan & Muller-Landau 2000), and not so strongly from
the seed bank. (3) Young gaps may not be attractive to biotic dispersers like birds and bats, since in gaps these organisms may face
high predation risks and low levels of resources (Schupp et al.
1989). Nevertheless, bats continue to be the most important agents
of dispersion in open areas because they use these sites and they can
defecate in flight (Gorchov et al. 1993, Medellı́n & Gaona 1999).
Finally, (4) the Amazonian forest, like the one at Zafire Station,
grows on old, nutrient-poor soils associated with sedimentation of
black-water rivers (Irion 1978). Soil conditions limit forest productivity and, as a consequence, the community of seed dispersers
shows low densities (Palacios & Peres 2005). The relationship between forest productivity and the abundance of dispersers has been
documented in primates (Stevenson 2001, 2007b), birds (Loiselle
& Blake 1991) and bats (Medellı́n et al. 2000).
The low representation of recruits from shade-tolerant plants
may also be linked to the role and abundance of large seed dispersers (Peres & van Roosmalen 2002). We witnessed some degree of
local hunting (L. S. Castillo pers. obs.), which is known to affect the
densities of some important seed dispersers like primates and large
birds (Peres & Palacios 2007). In addition, large seeds are transient
in the seed bank because they do not have long dormancy periods
4
Castillo and Stevenson
(Swaine 2001, Martins & Engel 2007) and, as a result, their number in the soil seed community is reduced (Dalling & Hubbell
2002). Another potential factor affecting the low representation of
large seeds is the higher predation risk that these face in gaps compared with mature forest (Schupp et al. 1989). This may result since
they are easier to find, more nutritious than small seeds, and may be
prone to predation in an impoverished seed environment (Stevenson 2007a). We predict that in sites where forest productivity is
higher and animal dispersers are abundant, regeneration rates will
be faster since the seed bank and seed rain will be enriched, and
shade tolerant seeds will be less limited by dispersal. Nevertheless, it
is necessary to undertake other studies in different sites to evaluate
our predictions.
ACKNOWLEDGMENTS
We are grateful to M. C. Peñuela and the indigenous communities
to allow the study in Zafire Biological Station. We thank the members of LEBTYP (Laboratorio de Ecologı́a de Bosques Tropicales
y Primatologı́a), C. Escallón and D. Cadena for their comments.
We also thank the referees for their useful comments on an earlier
version of this manuscript.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
TABLE S1. Slopes from the relationship between log time and four
variables of early seedling regeneration.
Please note: Wiley-Blackwell Publishing are not responsible for
the content or functionality of any supporting materials supplied by
the authors. Any queries (other than missing material) should be
directed to the corresponding author for the article.
LITERATURE CITED
ANDRESEN, E. 2001. Effects of dung presence, dung amount and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae)
seeds in Central Amazonia. J. Trop. Ecol. 17: 61–78.
ANDRESEN, E., AND D. J. LEVEY. 2004. Effects of dung and seed size on secondary
dispersal, seed predation, and seedling establishment of rain forest trees.
Oecologia 139: 45–54.
BAZZAZ, F. A., AND S. T. A. PICKETT. 1980. Physiological ecology of tropical
succession: A comparative review. Annu. Rev. Ecol. Syst. 11: 287–310.
BELL, D. T., AND D. S. WILLIAMS. 1998. Tolerance of thermal shock in seeds.
Aust. J. Bot. 46: 221–233.
BOND, W. J., AND J. J. MIDGLEY. 2001. Ecology of sprouting in woody plants:
The persistence niche. Trends Ecol. Evol. 16: 45–51.
CONNELL, J. H. 1978. Diversity in tropical rain forest and coral reefs. Science
199: 1302–1310.
DALLING, J. W., AND S. P. HUBBELL. 2002. Seed size, growth rate and gap microsite conditions as determinants of recruitment success for pioneer
species. J. Ecol. 90: 557–568.
DENSLOW, J. S. 1987. Tropical rain forest gaps and tree species diversity. Annu.
Rev. Ecol. Syst. 18: 431–451.
ESTRADA-VILLEGAS, S., J. PÉREZ-TORRES, AND P. STEVENSON. 2007. Dispersión de
semillas por murciélagos en un borde de bosque montano. Ecotropicos
20: 1–14.
FREY, B. R., M. S. ASHTON, J. J. MCKENNA, D. ELLUM, AND A. FINKRAL. 2007.
Topographic and temporal patterns in tree seedling establishment,
growth, and survival among masting species of southern New England
mixed-deciduous forest. For. Ecol. Manage. 245: 54–63.
GARWOOD, N. C. 1983. Seed germination in a seasonal tropical forest in
Panamá: A community study. Ecol. Monogr. 53: 159–181.
GORCHOV, D. L., F. CORNEJO, C. ASCORRA, AND M. JARAMILLO. 1993. The role
of seed dispersal in the natural regeneration of rain forest after stripcutting in the Peruvian Amazon. Vegetatio 107/108: 339–349.
GOTELLI, N. J., AND A. M. ELLISON. 2004. A primer of ecological statistics. Sinauer Associates Inc, Sunderland, Massachusetts.
GRUBB, P. J. 1977. The maintenance of species-richness in plant communities:
The importance of the regeneration niche. Biol. Rev. 52: 107–145.
HUBBELL, S. P., R. B. FOSTER, S. T. O’BRIEN, K. E. HARMS, R. CONDIT, B.
WECHSLER, S. J. WRIGHT, AND S. LOO DE LAO. 1999. Light-gap disturbances, recruitment limitation, and tree diversity in a Neotropical forest.
Science 283: 554–557.
HURTT, G. C., AND S. W. PACALA. 1995. The consequences of recruitment limitation: Reconciling chance, history and competitive differences between
plants. J. Theor. Biol. 176: 1–12.
IDEAM INSTITUTE. 2001. Reporte de los principales parámetros meteorológicos
(promedios históricos 1961–1990) de la Estación Meteorológica del
aeropuerto Internacional Vásquez Cobo de la ciudad de Leticia (Amazonas). Ministerio de Ambiente, Vivienda y Desarrollo Territorial. Sistema Nacional Ambiental. Colombia. Available at www.ideam.gov.co/
sectores/aero/climat/index4.htm (accessed April 10, 2008).
IRION, G. 1978. Soil infertility in the Amazonian rain forest. Naturwissenschaften 65: 515–519.
KLIMEŠOVÁ, J., AND L. KLIMEŠ. 2007. Bud banks and their role in vegetative
regeneration–A literature review and proposal for simple classification
and assessment. Perspect. Plant Ecol. Evol. Syst. 8: 115–129.
KOZLOWSKI, T. T. 2002. Physiological ecology of natural regeneration of harvested and disturbed forest stands: Implications for forest management.
For. Ecol. Manage. 158: 195–221.
KREBS, C. J. 1999. Ecological methodology. Addison-Wesley Educational Publishers, Inc, Glenview, Illinois.
LAWTON, R. O., AND F. E. PUTZ. 1988. Natural disturbance and gap-phase
regeneration in a wind-exposed tropical cloud forest. Ecology 69:
764–777.
LOISELLE, B. A., AND J. G. BLAKE. 1991. Temporal variation in birds and fruits
along an elevational gradient in Costa Rica. Ecology 72: 180–193.
MACMAHON, J. A., J. F. MULL, AND T. O. CRIST. 2000. Harvester ants (Pogonomyrmex spp.): Their community and ecosystem influences. Annu.
Rev. Ecol. Syst. 31: 265–291.
MARTINS, A. M., AND V. L. ENGEL. 2007. Soil seed banks in tropical forest fragments with different disturbance histories in southeastern Brazil. Ecol.
Eng. 31: 165–174.
MEDELLÍN, R. A., M. EQUIHUA, AND M. A. AMIN. 2000. Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conserv.
Biol. 14: 1666–1675.
MEDELLÍN, R. A., AND O. GAONA. 1999. Seed dispersal by bats and birds
in forest and disturbed habitats of Chiapas, México. Biotropica 31:
478–485.
NATHAN, R., AND H. C. MULLER-LANDAU. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends
Ecol. Evol. 15: 278–285.
PALACIOS, E., AND C. A. PERES. 2005. Primate population densities in three nutrient-poor Amazonian terra firme forests of South-Eastern Colombia.
Folia Primatol. 76: 135–145.
PERES, C. A., AND E. PALACIOS. 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forest: Implications for animal-mediated seed dispersal. Biotropica 39: 304–315.
Seed-Bank vs. Seed-Rain in Early Gap-Dynamics
PERES, C. A., AND M. VAN ROOSMALEN. 2002. Primate frugivory in two speciesrich Neotropical forests: Implications for the demography of largeseeded plants in overhunted areas. In D. J. Levey, W. R. Silva, and M.
Galetti (Eds.). Seed dispersal and frugivory: ecology, evolution and conservation, pp. 407–421. CABI Publishing, Wallingford, UK.
QUINN, G. P., AND M. J. KEOUGH. 2002. Experimental design and data analysis
for biologists. Cambridge University Press, Cambridge, UK.
SCHUPP, E. W., H. F. HOWE, C. K. AUGSPURGER, AND D. J. LEVEY. 1989. Arrival
and survival in tropical treefall gaps. Ecology 70: 562–564.
STEVENSON, P. R. 2001. The relationship between fruit production and primate
abundance in Neotropical communities. Biol. J. Linn. Soc. 72: 161–178.
STEVENSON, P. R. 2007a. A test of the escape and colonization hypotheses for
zoochorous tree species in a Western Amazonian forest. Plant Ecol. 190:
245–258.
STEVENSON, P. R. 2007b. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In A. J.
5
Dennis, E. W. Schupp, R. J. Green, and D. W. Westcott (Eds.). Seed
dispersal: Theory and its application in a changing world, pp. 340–362.
CABI Publishing, Wallingford, UK.
SWAINE, M. 2001. Protocol for assay of soil seed banks. In: Proceedings of the
Euroworkshop on Functional Groups in Tropical Forest Trees. Available at http://www.nbu.ac.uk/tropical/SSBprotocol_Swaine.doc (accessed April 10, 2008).
SWAINE, M. D., AND J. B. HALL. 1983. Early succession on cleared forest land in
Ghana. J. Ecol. 71: 601–627.
TEKETAY, D. 1997. Seedling populations and regeneration of woody species
in dry Afromontane forest of Ethiopia. For. Ecol. Manage. 98:
149–165.
WILLEMS, J. H., AND K. G. A. HUIJSMANS. 1994. Vertical seed dispersal by earthworms: A quantitative approach. Ecography 17: 124–130.
WRIGHT, S. J. 2002. Plant diversity in tropical forest: A review of mechanisms of
species coexistence. Oecologia 130: 1–14.