acta oecologica 32 (2007) 328–336

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Original article

Spatial variation in post-dispersal seed removal in an Atlantic forest: Effects of habitat, location and guilds of seed predators Alexander V. Christianinia,*, Mauro Galettib a

Departamento de Botaˆnica, Plant Phenology and Seed Dispersal Research Group, Instituto de Biocieˆncias, Universidade Estadual Paulista (UNESP), CP 199, 13506-900 Rio Claro, SP, Brazil b Laborato´rio de Biologia da Conservac¸a˜o, Departamento de Ecologia, Plant Phenology and Seed Dispersal Research Group, Instituto de Biocieˆncias, Universidade Estadual Paulista (UNESP), CP 199, 13506-900 Rio Claro, SP, Brazil

article info

abstract

Article history:

Studies of post-dispersal seed removal in the Neotropics have rarely examined the magni-

Received 19 November 2005

tude of seed removal by different types of granivores. The relative impact of invertebrates,

Accepted 20 June 2007

small rodents, and birds on seed removal was investigated in a 2,178 ha Atlantic forest frag-

Published online 17 August 2007

ment in southeastern Brazil. We used popcorn kernels (Zea maysdPoaceae) to investigate seed removal in a series of selective exclosure treatments in a replicated, paired design

Keywords:

experiment that included forest understory, gaps, and forest edge sites. We recorded the

Birds

vegetation around the experimental seed stations in detail in order to evaluate the influence

Edge effect

of microhabitat traits on seed removal. Vertebrate granivores (rodents and birds) were sur-

Granivory

veyed to determine whether granivore abundance was correlated with seed removal levels.

Habitat fragmentation

Seed removal varied spatially and in unpredictable ways at the study site. Seed encounter

Rodents

and seed use varied with treatments, but not with habitat type. However, seed removal

Seed predation

by invertebrates was negatively correlated with gap-related traits, which suggested an avoidance of large gaps by granivorous ants. The abundance of small mammals was remarkably low, but granivorous birds (tinamous and doves) were abundant at the study site. Birds were the main seed consumers in open treatments, but there was no correlation between local granivorous bird abundance and seed removal. These results emphasize the stochastic spatial pattern of seed removal, and, contrary to previous studies, highlight the importance of birds as seed predators in forest habitats. ª 2007 Elsevier Masson SAS. All rights reserved.

1.

Introduction

In tropical forests, many plant species are absent from sites apparently suitable for recruitment (Nathan and Muller-Landau, 2000, and references therein). Since seeds are subject to heavy

mortality after dispersal from the mother tree (Janzen, 1971; Wenny, 2000), it is possible that seed predators have a great influence on spatial patterns of plant recruitment (but see Andersen, 1989), although there is also great natural variation in seed rain (Nathan and Muller-Landau, 2000). Indeed, seed

* Corresponding author. Present address: Programa de Po´s-graduac¸a˜o em Ecologia, Instituto de Biologia, Departamento de Zoologia, Universidade Estadual de Campinas (UNICAMP), CP 6109, 13083-970 Campinas, SP, Brazil.: Fax: þ55 19 3289 3124. E-mail address: [email protected] (A.V. Christianini). 1146-609X/$ – see front matter ª 2007 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2007.06.004

acta oecologica 32 (2007) 328–336

predation can influence recruitment, plant species diversity and community structure at various levels (Janzen, 1971; Crawley, 1992; Hulme, 1998). Animals do not prey on seeds at random inside the forest. The foraging behavior of seed predators is influenced by vegetation structure and the associated risk of mortality. For example, rodents usually concentrate their foraging in areas with the densest vegetation cover and avoid open patches where they are more susceptible to aerial and/or visually oriented predators (e.g. Manson and Stiles, 1998). Consequently, seed predators can potentially change the original plant seed shadow and modify seed density and distribution by producing sites with a high probability of seed mortality, as well as sites where seeds are reasonably safe from predators (Hay and Fuller, 1981; Schupp, 1988; Bowers and Dooley, 1993; Manson and Stiles, 1998). Generalizations about post-dispersal removal and predation in Neotropical forests are based primarily on studies of large-seeded plants (e.g. seeds >5 mm; Janzen, 1971; Sork, 1987; Forget and Milleron, 1991; Fleury and Galetti, 2004) which are most likely consumed by rodents, other mammals, and insect larvae. Such generalizations may be misleading, since just a few studies investigated the impact of the whole guild of seed predators on seeds in the Neotropics (Hulme, 1998). Moreover, small-seeded plants (e.g. seeds <5 mm), although produced by the majority of the local plant species (Foster and Janson, 1985), are much less studied. Small seeds are most likely to be consumed by birds and adult insects such as ants (Janzen, 1971; Levey and Byrne, 1993; Kaspari, 1996; Pe´rez and Bulla, 2000). Granivorous birds have a great contribution to the biomass of bird assemblages in Neotropical forests (Terborgh et al., 1990), which is suggestive of their possible role in post-dispersal seed removal of small seeds (Pizo and Vieira, 2004). In this study, we used a selective exclosure cafeteria method to quantify the relative impact of invertebrates, small rodents, and birds to seed removal in an Atlantic forest fragment. The main objectives of this study were: (1) to evaluate the relative proportion of seeds removed by different granivores on the forest floor, (2) to quantify the spatial variation in seed removal within and among microhabitats, (3) to evaluate whether seed removal was influenced by vegetation structure, and (4) to evaluate whether seed removal rates were influenced by the local abundance of vertebrate granivores.

2.

Material and methods

2.1.

Study site

This study was done in a 2178 ha, semideciduous Atlantic forest fragment at the Caetetus Ecological Station (CES), close to Ga´lia (22 240 S, 49 420 W), in the State of Sa˜o Paulo, southeastern Brazil. CES is surrounded mostly by coffee plantations and pasturelands, and harbors predominantly old-growth forest that is rich in tree species belonging to the Rutaceae, Euphorbiaceae, Lauraceae, Apocynaceae, and Meliaceae. Vines are especially abundant in gaps and along forest edges (Durigan et al., 2000). The mean annual temperature is 20  C, with a total

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annual rainfall of around 1500 mm that is concentrated during the hot, rainy season that extends from October to February (SMA, 1998).

2.2.

Seed predators

Granivorous (e.g. Pheidole and Solenopsis) and fungus-growing ants (e.g. Atta and Acromyrmex) are ubiquitous at CES and collect a large number of seeds from the forest floor (Levey and Byrne, 1993; Leal and Oliveira, 1998). Several species of granivorous birds occur at CES, including nine pigeon and dove species (Columbidae), three tinamous (Tinamidae), and one quail (Phasianidae) (Willis and Oniki, 1981). These birds feed on a wide variety of fruits and seeds (Bokermann, 1991; Pe´rez and Bulla, 2000). Most information about small mammals at CES is restricted to anecdotal information. Rodents of the genera Akodon Meyen, Oligoryzomys Bangs, Holochilus Brandt, Nectomys Peters and Sciurus Linnaeus are expected to occur at the study site (Emmons and Feer, 1990). Peccaries Tayassu tajacu Linnaeus and T. pecari Link, which are recognized seed predators, are common at the study site (Cullen et al., 2000).

2.3.

Experimental design

Throughout this study, the term ‘‘seed’’ is used as a unit of dispersal. Popcorn kernels (Zea mays L.dPoaceae) (diameter 5.89  0.46 mm; weight 0.14  0.02 g; mean  SD; n ¼ 10) were used in the seed removal experiments to compare the relative contribution of ants, birds, and mammals to seed removal at this site. Non-native seeds were used in many seed predation studies worldwide (e.g. Thompson et al., 1991). We already know that popcorn kernels were attractive to most species in the forest floor and thus we could investigate the seed predation pressure in an unbiased way across different taxa and microhabitats. The seeds could be eaten in situ or carried away by animals for later consumption. Seed predation is the most likely fate for seeds removed from the experiments (Schupp, 1988; Hulme, 1998; Pizo and Vieira, 2004). However, some small and large seeds can be secondarily dispersed by ants (Levey and Byrne, 1993) and rodents (Forget and Milleron, 1991), respectively. Since we did not follow seed fate after removal we chose to apply the term ‘‘seed removal’’ to all seeds that were found eaten or not recovered from the experiments. A series of selective exclosure treatments was used to identify and quantify the sources of seed removal. The experimental unit (‘‘seed station’’) consisted of three plastic Petri dishes (9 cm in diameter) placed 30 cm from each other. Each Petri dish was glued to the top of a 10-cm nail, filled with ten popcorn seeds (30 seeds per seed station), and assigned to one treatment as follows: (1) Open treatment (control): the nail that anchored the dish was pushed into the ground until the lip of the dish wall was flush with the soil surface so that the seeds were available to birds, mammals and invertebrates. (2) Rodent treatment: the nail of the dish was pushed into the ground until the dish was ca. 3 cm above ground level. An insect trap glue (Tanglefootª) was spread around the nail to prevent the access of ground invertebrates, such as ants, to the seeds. A cage (20 cm  20 cm  9 cm) covered

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acta oecologica 32 (2007) 328–336

with a mesh of 2.7 cm  3.5 cm was placed above this apparatus. The seeds were accessible to any vertebrate that could pass the wire mesh and remove them (e.g. small rodents). (3) Invertebrate treatment: A Petri dish was assembled as in treatment 1, but within a small cage (16 cm  16 cm  9 cm) covered with a mesh of 1.5 cm  2.0 cm such that the seeds were available to only invertebrates (see Roberts and Heithaus, 1986). The seeds and the experimental apparatus were handled with rubber gloves and rubber boots to avoid leaving olfactory cues to the predators (Duncan et al., 2002). A plastic sheet (1 m2) with cords attached to the corners was strung to nearby trees and hung flat 1.5 m above each seed station to prevent the seeds from being washed away by rainfall. The plastic sheet seems not to have affected the behavior of local predators, since we recorded several vertebrates removing seeds from the experiments (see results). The number of seeds removed was checked 5 days after the experiments had been set up. This length of time was apparently enough to assess the impact and spatial patterns of seed consumption since most seed removal occurs during the first few days after seed fall (Sa´nchez-Cordero and Martı´nez-Gallardo, 1998; Wenny, 2000; Guimara˜es and Cogni, 2002). A camera-trap with a passive infrared trigger mechanism and an automatic, weather proof, 35 mm Yashica camera with an auto flash (Wildlife Pro Camera System, Forest Suppliers Inc.) was installed at each of five seed stations to help identify potential seed predators. Tracks, feces and seed remains were recorded whenever possible to identify the animals that visited the experimental sites. Seed stations were set up along several 1 m wide transects that crossed the study site, 5 to 30 m outside transects, and at least 50 m from the nearest replicate in order to guarantee the independence of the experimental units. Most Atlantic forest rodents do not move more than 50 m between consecutive days (Gentile and Cerqueira, 1995). This distance is also enough to provide independent discoveries by different ant colonies since most ants forage at shorter distances to their nests (Levey and Byrne, 1993; Leal and Oliveira, 1998). The area of forest covered by the experimental set ups was nearly 500 ha.

2.4.

Spatial variability of seed removal

To assess the spatial variation in seed removal within and among microhabitats, each seed station was replicated 30 times in each of three microhabitats: (1) at understory forest sites >300 m from the nearest edge of the fragment, and at least 50 m in a random direction from the closest edge of any other gap, (2) within recently formed (<2 years) gaps with a canopy opening of at least 100 m2, and (3) within a 10 m strip of the forest fragment starting from the forest edge, along the borders that separated the forest from coffee plantations. Sample sizes were sometimes less than 30 because some of the exclosure treatments were disturbed by peccaries or other animals, thereby allowing the access of all predators. Experiments were conducted during November and December 2000, including the same number of replicates per microhabitat at a time.

To assess the possible relationship between seed removal and local traits, we measured 14 microhabitat variables at each seed station (Table 1). The variables consisted of attributes related to vegetation structure (e.g. cover, height, etc.) and distance to objects (fallen logs, trees) that could influence the activity of granivores and seed removal (Bowers and Dooley, 1993; Manson and Stiles, 1998; Wenny, 2000).

2.5. Distribution and abundance of vertebrate seed predators In January 2001, after the end of the experiments, two Sherman live-traps (15  15  30 cm) were placed at ground level around each experimental unit during five consecutive days and nights to capture rodents that may have eaten the seeds during the experiments. The trap effort was 900 trap-nights (300 trap-nights per microhabitat). We used a mixture of banana, peanut butter, and popcorn kernels as bait. All of the animals captured were identified, marked and subsequently released. Granivorous birds were sampled concurrently with the seed removal experiments. A point count method was used to estimate the relative abundance of granivorous birds (Bibby et al., 1993) within habitats (forest interior or edge) and per transect. Forty-three point counts were established along the same transects close to the seed stations, with a minimum distance of 200 m between consecutive points. Each point count was sampled once for 20 min, from 06:00 to 09:00 h,

Table 1 – Microhabitat features recorded at each seed station #

Name

1.

Tree distance

2.

Tree DBH

3. 4.

Tree heighta Canopy heighta

5. 6.

Canopy coverb Liana distance

7.

Log distance

8. 9. 10. 11.

Small logsc Medium logsc Large logsc Herbaceous covera,c

12. Woody covera,c 13. Understory coverc,d 14. Understory heightc,e a

Description Distance (m) to the nearest tree (>10 cm DBH) Diameter at breast height (cm) of the tree sampled at 1 Height (m) of the tree sampled at 1 Height (m) of the canopy around the experimental unit Canopy cover (%) Distance (m) to the nearest liana at ground level Distance (m) to the nearest log (>20 cm in diameter) within 5 m Number of logs 5–10 cm in diameter Number of logs 10–20 cm in diameter Number of logs >20 cm in diameter Percentage of ground cover by herbaceous vegetation Percentage of ground cover by woody stems Understory cover Mean height (m) of the understory

Estimated visually. Measured with a densiometer (Lemmon, 1957). c Within a 2 m radius around the experimental unit. d Number of touches from 0 to 2 m on a pin lowered vertically eight times through the vegetation around the experimental unit. e Assigned as the 0.5 m interval of the pin with the highest number of touches. b

acta oecologica 32 (2007) 328–336

the period of highest activity for the local granivorous bird community (Sick, 1997). All of the points were sampled by the same person (A.V.C.), in a random order and in the absence of rain or strong wind. Special effort was taken to avoid double counting of the same bird since this would lead to an overestimate in the survey. The relative abundances of birds were determined based on the number of visual plus auditory contacts with granivorous birds, regardless of the distance, divided by the number of point counts in a given habitat or transect.

2.6.

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exploitation followed similar trends: seed removal varied across treatments (H ¼ 67.93; df ¼ 2; P < 0.001), but not across microhabitats (H ¼ 0.24; df ¼ 2; 0.75 < P < 0.90) (Fig. 1b). Open treatments had three times more seeds removed than either rodent or invertebrate access treatments (Fig. 1b). Rodents removed as many seeds as invertebrates (U ¼ 2.92; P ¼ 0.10). Once discovered, a seed station usually had all seeds removed, and there was therefore considerable variation around the

Statistical analysis

Seed removal was assessed based on the seed encounter (the probability of at least one seed being removed from a dish) and seed exploitation (the proportion of seeds removed from a dish). Seed encounter is a binary variable (encountered or not encountered), and was analyzed using Chi-square goodness of fit tests, assuming an equal probability of seed encounter among treatments or microhabitats. Since the proportion of seeds removed per treatment and microhabitat was not normally distributed, even after transformations, non-parametric analyses were used. Treatment and habitat differences in seed removal were evaluated with a two-way Kruskall–Wallis, the Sheirer–Ray–Hare extension of the Kruskall–Wallis test (Scheirer et al., 1976; Sokal and Rohlf, 1995). This test works in a similar way to the two-way ANOVA, but with the use of ranks. Exclusion treatment and microhabitat were considered fixed effects. Multiple comparisons among treatments were done with Mann–Whitney U-tests, according to the recommendations of Shirley (1987). Principal component analysis (PCA) of the correlation matrices with microhabitat features was used to summarize environmental variation among seed stations (Manly, 1997). To assess the possible relationship between seed removal and local traits, we regressed the first two principal components on seed encounter and seed exploitation with logistic regression and Spearman’s rank correlation, respectively (Wenny, 2000). Bird abundance was related to seed removal in open treatments by combining all seed stations in a given transect (n ¼ 13) or with the nearest (<200 m) seed stations (n ¼ 41), and using a critical value of alpha (a) ¼ 0.025 to control for multiple comparisons (a ¼ 0.05/2, Bonferroni correction) (Sokal and Rohlf, 1995). Separate analyses were done for each species, individually and with all species together. Stations visited by large mammals (e.g. peccaries) were excluded from the analysis. Since few small mammals were trapped (see Section 3), the abundance of rodents was related to seed removal only qualitatively.

3.

Results

3.1.

Seed encounter and seed use

Seed encounter varied among treatments (c2 ¼ 43.57; df ¼ 2; P < 0.001), but not with microhabitat type (c2 ¼ 0.055; df ¼ 2; P ¼ 0.97) (Fig. 1a). Most open controls had at least one seed removed, while rodent access treatments were more rarely discovered, as were invertebrate treatments (Fig. 1a). Seed

Fig. 1 – (a) Encounter rates for seed stations in a given microhabitat per exclusion treatment. A seed station was assumed to be encountered if at least one seed was removed from a given treatment during the experiments: white bars, open treatment; shaded bars, rodent access; hatched bars, invertebrate access. (b) Seed exploitation (the proportion of seeds removed from a dish) in a given microhabitat per exclusion treatment. Sample sizes (n) appear below the bars. See right-hand side for an explanation of the box-and-whisker plot and the text for detailed results of the statistical comparisons.

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median values of seed exploitation (Fig. 1b). The interaction treatment x microhabitat was not significant (H ¼ 4.07; df ¼ 4; 0.25 < P < 0.50). Seed removal in invertebrate treatments was not correlated with those in rodent access treatments (rs ¼ 0.14; P ¼ 0.24; n ¼ 77) or with open treatments (rs ¼ 0.16; P ¼ 0.17; n ¼ 78). Seed removal in open treatments was weakly but significantly correlated with seed removal in rodent access treatments (rs ¼ 0.47; P < 0.001; n ¼ 85). Most seeds were removed from open treatments, leaving no seed remains, which suggested that they were taken whole and swallowed, or carried away. Photos obtained by cameras-trap revealed three visits of Brown tinamou Crypturellus obsoletus and two of Plush-crested jay Cyanocorax chrysops to the experiments. White-lipped peccaries visited at least six seed stations, based on three photos taken by the camera-traps and by the signs they left. Brown capuchin monkey Cebus apella and Paca Agouti paca had one photo record each. Pheidole ants (Formicidae: Myrmicinae) consumed the seeds on the spot, while large Attini ants (Atta spp. and Acromyrmex spp.) carried the seeds away to their nests.

3.2.

Influence of vegetation structure on seed removal

The microhabitats differed in virtually all of the traits sampled (Table 2). The first axis of the PCA explained nearly 23% of the variation in microhabitat traits and was related to a gradient of increasing forest succession; this axis was positively correlated with canopy cover, understory height and distance to the nearest liana, and negatively correlated with herb and understory cover (Table 3). The second axis of the PCA explained 20.6% of the variation and was related to gaps in the vegetation; this axis was positively correlated with the density of logs and woody cover, and negatively correlated with the distance to the nearest log. Two other principal components were selected from the analysis, but they accounted for a comparatively lower variance of habitat traits (Table 3).

The influence of the second axis of the PCA on seed encounter in the invertebrate access treatments was marginally significant (c2 ¼ 3.66; P ¼ 0.056; y ¼ exp (0.285  0.456x)/ 1 þ exp (0.285  0.456x)). None of the other logistic regressions of seed encounter versus any axis of the PCA, taken together or one at a time, was significant (results not shown). Indeed, seed removal in open or rodent access treatments was not explained by microhabitat variation among seed stations. However, seed removal by invertebrates was weak, but significantly influenced by gap-related traits (Table 3). The microhabitat characteristics of the seed stations that had at least one seed removed from open treatments were not different from those at seed stations with no seed removal (PCA Axis 1: U ¼ 655, P ¼ 0.88; PCA Axis 2: U ¼ 552, P ¼ 0.24; PCA Axis 3: U ¼ 648, P ¼ 0.83; PCA Axis 4: U ¼ 569, P ¼ 0.83).

3.3. Distribution and abundance of vertebrate seed predators Only three species of small mammals were captured during the trap survey: the marsupials Didelphis albiventris and Micoureus demerarae (Didelphidae) (two captures each), and the rodent Akodon sp. (Muridae) (two captures of a single individual). All of the marsupials were caught within forest microhabitats, while the rodent was captured in a gap. No small mammals were captured at edges. In contrast to small mammals, granivorous birds were quite common at the study site. The abundance of granivorous birds was 5.7  3.8 contacts per point, while the density estimates reached 4.6  3.4 birds/ha (A.V. Christianini, unpublished data). Granivorous birds were significantly more common at edges than within the forest fragment (t ¼ 4.03; df ¼ 41; P < 0.001), even after excluding the visual detection of birds at all points sampled, since the probability of visual detection is higher at edges. Seed removal was not correlated with the abundance (r ¼ 0.01; P ¼ 0.95; n ¼ 41) of granivorous birds sampled at points close to the seed stations, as well as for bird abundance combined for transects (r ¼ 0.15;

Table 2 – Traits of the microhabitats sampled at the seed stations. Values are the mean ± 1 SD. Means followed by the same superscript letter in a given row do not differ among microhabitats (P > 0.05, Tukey HSD test).See Table 1 for details of the variables Variable

Forest understory

Tree distance Tree DBH Tree height Canopy height Canopy cover Liana distance Log distance Small logs Medium logs Large logs Herbaceous cover Woody cover Understory cover Understory height *P < 0.05, **P < 0.01 and ***P < 0.001.

a

1.98  0.89 31  23a 11.77  3.80a 14.30  3.66a 90  2a 0.45  0.40a 4.22  1.26a 1.23  1.43a 0.77  0.82a 0.17  0.46a 14  7a 5  4a 6.53  3.76a 0.88  0.54a

Gaps

Edges b

3.17  1.27 23  12a 8.97  3.56b 13.17  3.67a 75  10b 0.20  0.20b 2.00  1.23b 2.73  2.30b 1.53  1.53b 1.00  0.87b 23  14b 9  6b 13.63  8.31b 0.82  0.52a

Comparison b

3.67  3.54 28  25a 8.17  2.39b 8.89  2.65b 79  16b 0.11  0.13b 4.58  1.00a 1.21  1.37a 0.21  0.49a 0.07  0.26a 24  23b 2  3a 12.72  11.08b 1.33  0.66b

F2,86 ¼ 7.95*** F2,89 ¼ 1.31 F2,86 ¼ 9.62*** F2,86 ¼ 21.02*** F2,90 ¼ 14.61*** F2,89 ¼ 12.68*** F2,89 ¼ 42.43*** F2,89 ¼ 7.36** F2,89 ¼ 12.04*** F2,89 ¼ 22.32*** F2,89 ¼ 3.96* F2,86 ¼ 19.95*** F2,89 ¼ 10.75*** F2,89 ¼ 6.90**

acta oecologica 32 (2007) 328–336

Table 3 – Principal component analysis for microhabitat traits at the experimental seed stations. The columns show the coefficients of correlation between a given variable and a principal component. Significant values (P < 0.05) in bold. The correlation between principal components and seed removal at the seed stations according to treatment type is also shown Variable

Axis 1

Axis 2

Axis 3

Axis 4

Tree distance Tree DBH Tree height Canopy height Canopy cover Liana distance Log distance Small logs Medium logs Large logs Herbaceous cover Woody cover Understory cover Understory height Eigenvalues Variation explained (%)

0.751 0.067 0.009 0.034 0.835 0.354 0.303 0.0004 0.105 0.242 0.813 0.123 0.597 0.345 3.21 22.89

0.005 0.032 0.018 0.202 0.207 0.162 0.807 0.481 0.312 0.794 0.011 0.714 0.044 0.047 2.89 20.63

0.140 0.636 0.881 0.641 0.205 0.234 0.081 0.225 0.009 0.117 0.045 0.103 0.105 0.041 1.88 13.43

0.119 0.156 0.064 0.389 0.009 0.430 0.166 0.346 0.732 0.020 0.182 0.332 0.416 0.670 1.26 9.00

Correlation between seed removal and the principal components Control 0.056 0.039 0.110 Small mammals 0.017 0.106 0.013 Invertebrates 0.124 0.240 0.093

0.054 0.016 0.0344

P ¼ 0.60; n ¼ 13). The abundance of each granivorous bird species did not influence seed removal levels (results not shown).

4.

Discussion

Studies of post-dispersal seed removal in the Neotropics have rarely examined the magnitude of seed removal by different types of granivores. The available information suggests that rodents are among the main seed predators on the forest floor (Crawley, 1992; Hulme, 1998). However, the low abundance of rodents at our study site and the lower levels of seed removal in the rodent treatments indicated that other animals were the main seed predators. Our findings seem not to be biased due to differential seed consumption by rodents of seeds within selective exclosures, since previous investigation indicated that small mammals move freely into the wire cage (Christianini and Galetti, 2007). Seed removal in the open treatments was not correlated with seed removal in the invertebrate treatments but was correlated with that in rodent treatments. However, in this case, the variance explained was low, indicating that other animals removed most of the seeds. Large mammals, such as peccaries, left signs of their visit at just six (7%) seed stations. Most seed stations had no seed remains, indicating that the animals consumed the seeds whole, what is compatible with seed removal by granivorous birds that swallow the seeds. Birds represent a high-demand sink for seeds: a granivore bird weighing only 27 g should eat 4.7 g of seeds (dry mass) to meet its daily requirements (Karasov, 1990). In our study site, the biomass of the terrestrial granivore bird community

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is ca. 0.8 kg/ha within the forest and twice as high at the forest edge (A.V. Christianini, unpublished data). Similar values for the biomass of granivorous birds (including parrots, parakeets and macaws) were obtained for an undisturbed Amazonian forest bird community (Terborgh et al., 1990). Hence, birds probably exert high seed predation pressure in Neotropical forests. There are several reasons why birds have been overlooked for so long as post-dispersal seed predators in Neotropical forests. First, there is still no efficient means for quantifying birds separately from other sources of seed removal. Several granivorous birds overlap in body size, diet, habitat and activity schedule with many species of small to medium-sized mammals, including squirrels and agoutis. Second, granivorous birds such as tinamous and pigeons usually swallow the seeds whole and crack them in their gizzard (Schubbart et al., 1965; Bokermann, 1991), thereby removing evidence of their foraging on these seeds. Third, the size of the seeds used in most seed removal experiments in the Neotropics is usually too large to be eaten by the local granivorous bird guild so that birds tend to be excluded from these studies by a gape-width limitation. Although most plants from tropical forests produce small seeds (e.g. <5 mm; Foster and Janson, 1985), many seed removal studies have focused on plants from the Burseraceae, Lecythidaceae, Arecaceae and Sapotaceae, most of which produce large seeds (e.g. >15 mm in diameter) that may be consumed only by peccaries, rodents or by specialized invertebrate seed predators, such as bruchid beetles (Janzen, 1971; Hulme, 1998). In contrast, studies using smaller seeds have usually indicated that granivorous birds may also be an important source of seed removal (Zipparro, 1999; Pizo and Vieira, 2004; this study). Several studies have shown that granivorous birds in the Neotropics can eat a large variety of small seeds (E´rard and Sabatier, 1986; Pe´rez and Bulla, 2000). Seeds from the Euphorbiaceae, Rutaceae, and Poaceae are commonly found in the stomach contents of columbids and tinamids (Schubbart et al., 1965; Bokermann, 1991). Most of these seeds are anemo- or authocoric and provide no resource for a bird other than the seed itself, which suggests that birds would not be secondarily dispersing them. The paucity of studies in other forest fragments and their experimental design limit possible comparisons with the results obtained at CES. To date, the study of Pizo and Vieira (2004) with Croton priscus is the only one designed to compare seed removal by birds versus rodents in Neotropical forests, although these authors did not concomitantly investigate seed removal by ants, which disperse the seeds of C. priscus (Passos and Ferreira, 1996). Pizo and Vieira (2004) found a tendency towards higher levels of seed removal during the day (assumed to be done by birds) than at night in a 250-ha Atlantic forest fragment. These authors suspected that the seed removal by terrestrial birds reflected the effects of forest fragmentation which reduced the density of mammalian seed predators and increased the density of terrestrial granivorous birds. However, in large tracts of forests, isolated and protected from illegal hunting, large tinamids, such as Tinamus solitarius and Crypturellus noctivagus, are frequently flushed, while in small, disturbed forest patches, these large tinamids usually disappear and smaller tinamids and doves increase in abundance and dominate the guild (Willis, 1979;

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Aleixo and Vielliard, 1995; Sick, 1997). CES is nearly nine times larger than the fragment studied by Pizo and Vieira (2004), and can be considered a medium-sized forest fragment. Although the great impact of birds in seed removal seen in our study could be the result of forest fragmentation, we believe that birds are important seed predators even in larger tracts of undisturbed forests (see Zipparro, 1999), but this remains to be confirmed by large scale, replicated studies of post-dispersal seed removal using selective exclosures. Our low success in trapping rodents cannot be attributed to seasonality since the sampling was done during the wet season, when small mammal populations reached their peak (Bergallo and Magnusson, 1999). Moreover, an additional trapping effort of 800 trap-nights during the dry season gave similar results (A.V. Christianini, unpublished data). Small mammal communities of the Atlantic forest fragments are dominated by marsupials (Fonseca and Robinson, 1990), which are not seed eaters and are apparently able to exclude other species from these communities through either direct competition or predation on nestlings (Fonseca and Robinson, 1990). Hence, low rates of seed removal by rodents observed in small Atlantic forest fragments could increase the role of birds as seed predators as fragment size decreases (Pizo and Vieira, 2004). In this study, seed removal by invertebrates was low, ranging from 19% to 25% of the seeds in the invertebrate treatments in any microhabitat. In the tropics, ants are considered seed predators of less importance than rodents (Estrada and Coates-Estrada, 1991; Horvitz and Schemske, 1994; Gryj and Dominguez, 1996), and some ant species are being increasingly recognized as important secondary dispersers of seeds (Pizo et al., 2005). However, ants focus on small seeds (Levey and Byrne, 1993; Pizo and Oliveira, 1999) and our study may have underestimated seed removal by ants because the seeds were too large for some species to carry (Kaspari, 1996). This issue of seed size probably affects other studies of seed predation in Neotropical forests (Hulme, 1998). Abiotic conditions may also influence invertebrate foraging behavior. Like other invertebrates, ants are sensitive to spatial variation in light, temperature and moisture (Kaspari, 1993). Gaps in semideciduous forests, where temperature and light are higher and moisture levels much more variable than in the forest understory (Restrepo and Vargas, 1999), are probably poor quality foraging patches for many groundforaging ants. The results from this study indicated that ants avoided taking seeds from large open patches, where the probability of mortality by desiccation is higher (Kaspari, 1993). This behavior would be especially important in semideciduous forests which have lower relative humidity and are subject to greater seasonal variations than ombrophilous forests (Hueck, 1972). Indeed, very low levels of post-dispersal seed predation by ground invertebrates were also found in a dry forest in Mexico (Gryj and Dominguez, 1996), while in ombrophilous forests gaps did not reduce the exploitation of seeds by ants (Pizo and Oliveira, 1999). The density of Atta and Acromyrmex (Attini) ant nests is usually higher at edges than inside the forest (Vasconcelos and Cherrett, 1995), but this did not translate into higher levels of seed removal by invertebrates at edges. Edges can be harsh environments for some ant species (Majer et al., 1997). The fate of seeds may differ if the ant species composition varies between

edges and the forest interior (Guimara˜es and Cogni, 2002). If an increase in Attini ants at edges compensates for habitat-mediated changes in the ant species responsible for seed removal within forest microhabitats, then such changes may not be readily detected by counting the number of seeds removed, and may have masked the results of this study. Compensatory effects among microhabitats for other ant species were also reported by Pizo and Oliveira (1999). Since our experiments were not designed to indicate which ant species removed the seeds at seed stations, this point deserves further attention. Overall, seed removal did not vary with microhabitat type, and the microhabitat characteristics of seed stations where seeds were preyed upon did not differ from those seed stations with no seed predation. Most spatial variation in seed predation occurred within rather than between microhabitats. The lack of any strong effect of microhabitat may simply reflect the generalist behavior of seed predators (Manson and Stiles, 1998), or compensatory effects resulting from shifts in species composition among microhabitats. The lack of influence of microhabitat traits on seed removal (with the exception of invertebrates) should reflect the low abundance of rodents at CES, since rodents are the main seed predators to show strong preferences for certain microhabitat traits (e.g. Manson and Stiles, 1998). Consequently, in relation to microhabitat variation, local seed removal was a stochastic event. Indeed, post-dispersal seed removal in gaps could be higher, equal to, or lower than beneath the canopy in the tropics (Fleury and Galetti, 2004, and references therein). Edges have also inconclusive effects on seed removal (e.g. Holl and Lulow, 1997; Guimara˜es and Cogni, 2002; Fleury and Galetti, 2004, 2006). Large scale, replicated experiments are needed to disentangle the possible multiple effects of seed species, predator assemblages, historical and matrix effects under these results (Fleury and Galetti, 2006). The lack of correlation between the abundance of granivorous birds and seed removal may be due to the fact that most Neotropical forest plant species produce seeds that promptly germinate (Vasquez-Yanes and Orozco-Segovia, 1993). Consequently, seeds would be an ephemeral resource for many nonspecialized granivores. Indeed, avian granivores forage over relatively large areas and congregate in high-density patches of seeds (Thompson et al., 1991). With the exception of tinamous, none of the granivorous birds sampled at CES are territorial and they forage over a wide variety of habitats (Sick, 1997; A.V. Christianini, personal observations). Although birds contributed significantly to seed removal in this study, the small scale of our experimental patches relative to the scale of the foraging area used by avian granivores probably precluded any influence of bird abundance on seed removal. An adequate assessment of the effect of granivore bird abundance on post-dispersal seed removal could be obtained by replicating selective exclosure experiments on a larger spatial scale, preferably including several forest fragments.

5.

Conclusion

Birds are an important source of seed removal in the floor of a medium-size semideciduous forest, and their generalist behavior, coupled with the relative scarcity of rodents, may have

acta oecologica 32 (2007) 328–336

reflected the absence of microhabitat effects on seed removal. Seed removal by ants was an exception, being negatively influenced by gaps. Granivorous birds are probably an overlooked source of post-dispersal seed predation in the floor of Neotropical forests. We recommend that birds should be considered seed predators of potential importance in future studies of seed predation conducted in other Neotropical forests, which could enhance our knowledge about the evolutionary and ecological implications of seed predation in these areas.

Acknowledgments We thank the Instituto Florestal de Sa˜o Paulo for permission to work at Caetetus. We are grateful to Paulo S. Oliveira, Milene M. Martins and two anonymous reviewers for their suggestions that improved the manuscript. This study was supported by fellowships from the Brazilian National Council for Scientific and Technological Development (CNPq) (AVC) and by grants from FAPESP and PROAP-CAPES (MG). The facilities provided by the PPG Ecologia at Unicamp made possible the preparation of this paper. A.V.C. and M.G. are currently supported by FAPESP and CNPq fellowships, respectively.

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Spatial variation in post-dispersal seed removal in an ...

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