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Seed dispersal, plant recruitment and spatial distribution of Bactris acanthocarpa Martius (Arecaceae) in a remnant of Atlantic forest in northeast Brazil
Acta Oecologica 22 (2001) 259−268 © 2001 Éditions scientifiques et médicales Elsevier SAS. All rights reserved S1146609X01011171/FLA
Seed dispersal, plant recruitment and spatial distribution of Bactris acanthocarpa Martius (Arecaceae) in a remnant of Atlantic forest in northeast Brazil Maria G. Silva, Marcelo Tabarelli* Departamento de Botânica, Universidade Federal de Pernambuco, CEP: 50670–901 Recife, PE, Brazil
Received 6 October 2000; revised 4 August 2001; accepted 21 August 2001
Abstract – Seed dispersal ecology of Bactris acanthocarpa Mart. (Arecaceae), an Atlantic forest understory palm, was investigated during two years as an attempt to test the following predictions: (i) seeds of Bactris are dispersed by mammals and large-gaped birds; (ii) Bactris benefits from seed dispersal in terms of seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults is related to patterns of seed dispersal. The study was conducted at Dois Irmãos Reserve, a 387.4-ha reserve of Atlantic forest in northeastern Brazil (8º S–35º W). Black–rumped agoutis (Dasyprocta prymnolopha) and Guianan squirrels (Sciurus aestuans) were identified as the seed dispersers/predators, moving seeds short distances (< 4 m from parents) and at low rates (0.04-0.05 diaspore/palm/day). Pyrene burial prevented seed predation by vertebrates and reduced by half seed infestation by Scolytidae beetles. Only buried pyrenes germinated. Pyrene predation was not correlated with distance from conspecific adults. In contrast, early seedling mortality was higher near conspecific adults. Most adults (64%) had their nearest conspecific adult neighbour > 4 m away in contrast to 96% of seedlings that occurred concentrated within 4 m from adults (77% under the palm crowns). Here, we present evidence that spatial distribution of B. acanthocarpa is partly due to low rates of seed removal, short-distance seed dispersal by agoutis and squirrels, and early seedling mortality associated with presence of seedlings under palm crowns. © 2001 Éditions scientifiques et médicales Elsevier SAS Atlantic forest / Bactris / plant demography / rodents / seed dispersal
1. INTRODUCTION Seed dispersal has been recognised as one of the most important factors affecting plant recruitment, spatial distribution and long term viability of populations [2, 23, 26]. Benefits of seed dispersal usually include reduction in levels of seed predation, improvement of seed germination and colonisation of new habitats [9, 39]. Studies on palm dispersal ecology have identified rodents [17, 22, 32, 43], primates [8], birds [38] and ungulates [5, 18] as seed dispersers. Although some rodents and ungulates can function as both seed predators and dispersers, there are important benefits in terms of seed predation avoidance, seed germination and seedling survival associated with seed dispersal by
*Correspondance and reprints: Fax: +055 2181 2718350. E-mail address: [email protected] (M. Tabarelli).
vertebrates for palm species. For example, spiny rats (Proechimys semispinosus) may function as effective seed dispersers of Astrocaryum standleyanum if seeds are removed to favourable germination sites unavailable to other seed predators [22]. A similar situation is observed in seeds of A. mexicanum, which are protected from predation by other animals if they are scatterhoarded by Heteromys desmarestianus and agoutis (Dasyprocta punctata) [6]. In addition to these benefits, seed dispersal can affect the spatial distribution of palms. The small seeds (< 2 cm length) of Euterpe edulis, an Atlantic forest understory palm, are dispersed by toucanets, cracids and agoutis, at short and long distances [35]. Euterpe edulis can show both clumped or random distribution if rodents or birds act as dispersers [37]. In contrast, Astrocaryum paramaca is dispersed at short distances (< 50 m) only by spiny rats (Proechymis spp.) and acouchis (Myoprocta exilis) [14]. Evidence from other
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tree species also suggests that seed dispersal by rodents may result in clumped distribution of adult plants [33]. Bactris acanthocarpa Martius is an understory palm species that occurs in both the Amazonian and Atlantic rain forest of Brazil. It has small (< 15 mm diameter), orange to red fruits attached to exposed infructescences near the ground level [30]. Several species of Bactris have been described in the literature as gutdispersed species, specially large-gaped birds [38]. In addition other palm species with fruit morphology similar to Bactris (i.e., orange to red/purple-black fruits < 15 mm diameter) have mammals and largegaped birds as effective seed dispersers [37, 38]. Therefore the following predictions can be made about B. acanthocarpa: (i) seed dispersal is carried out by mammals and large-gaped birds; (ii) benefits of seed dispersal will include seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults will be related to patterns of seed dispersal. Seed dispersal ecology of B. acanthocarpa was investigated during two years in a remnant of the Brazilian Atlantic forest to test these predictions. In particular, we identify the seed dispersers/predators, rates of fruit/pyrene removal, and also analyse the benefits of seed burial relative to predation and germination. Furthermore, we test the correlation between seed predation, seedling mortality and distance from conspecific adults. Finally, we discuss possible effects of dispersal by rodents upon spatial distribution of B. acanthocarpa. 2. METHODS 2.1. Study site This study was conducted at Dois Irmãos Reserve (8ºS–35ºW), a 387.4-ha reserve of Atlantic forest, in the State of Pernambuco, northeastern Brazil (figure 1). At present Dois Irmãos is isolated from other forest remnants by sugar cane an by urban areas [31]. The study site is located on low altitude plateaus (10-100 m a.s.l.) of Formação Barreiras, where prevailing soils are latosols [25]. The climate matches Koeppen’s tropical (As’), with a 3-month dry season [10]. The annual rainfall is around 2460 mm, with the wettest period between March and August [10]. The vegetation can be classified as tropical lowland rain forest (terra firme forest), one of the Brazilian Atlantic forest types that occurs at 50-100 m altitude [47]. The study site presents a plant community similar to other Atlantic lowland forests described in the literature, with Leguminosae, Lauraceae, Euphorbi-
aceae, Melastomataceae and Sapotaceae as the richest families [20]. Detailed information on plant species, birds and mammals in the study site is available in the literature [31]. 2.2. Bactris acanthocarpa Martius Bactris acanthocarpa is an understory palm species that occurs in the Amazonian and lowland Atlantic forest [21]. Stems are medium-sized (< 2 m tall), spiny, solitary or clustered. Leaves (5-15) are pinnate and densely covered with black spines [30]. Fruits are one-seeded obovoid drupes. In the study site they are 12.3 ± 1.5 mm (mean ± SD, n = 50) diameter, orange to red and covered with short spinules (figure 2). Pericarp is thin (< 1 mm) and the mesocarp is pulpy (1-2 mm). Pyrenes are globular with a coconut-like endosperm [21]. Infructescences are usually exposed near ground level (< 1 m height) and contain over 100 fruits (54-196, n = 10). Ripening fruits are not dropped beneath the parents, therefore not producing “seed shadows”. 2.3. Diaspore dispersers In order to identify diurnal fruit removers 14 focal adults bearing ripening fruits were selected in six different areas in the study site. Observations were carried out using 10 × 40 binoculars during 3 h intervals of daylight early in the morning (06400-09400 h) and at dusk (16400-19400), periods which usually overlap the foraging peak of agoutis and squirrels [32, 33]. Observations were conducted 25-30 m distant from focal adults, which were observed during a one-year period (January-December 1998), totalling 400 h of palm observation. Agoutis and squirrels were censused in the study site by line transect sampling [7]. A straight trail of 1000 m length and 1 m wide was cut in the best preserved tract of forest. Distance of sighting was limited to 20 m outward transect. Diurnal censuses started before sunrise or early morning and terminated before1 h of survey. Effort was made to keep the walking speed as constant as possible at ca. 1 km h–1. Thirty five censuses were carried out, totalling 35 km walked, over 35 h of sampling during five months (February-August 2000). We estimated agouti density by dividing the number of individuals recorded by the total area sampled (transect length × number of censuses × 40 m). Nocturnal surveys were not carried out since there was no evidence for nocturnal activity of medium to large-bodied nocturnal rodents that act as seed dispersers in the study site [11, 12]. To identify small-bodied nocturnal fruit removers 30 traps (similar to Tomahawk 16” × 5” × 5”) were placed in 1-ha grid in a Bactris palm stand. Ripening fruits of Bactris, peanut butter and fresh cassava roots
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20 adults were selected. Beneath these adults artificial
Figure 1. Location of the study site- Dois Irmãos Reserve, Brazil.
were used as baits. Trapping was conducted during a three-month period (July-September 1999). 2.4. Rate of diaspore removal and seed fate
2.4.1. Fruit primary dispersal In order to estimate rates of fruit removal from parents, 25 adults bearing ripening fruits were selected inside a 2-ha plot. Fruit removal was censused three times a week during a 10-month period including dry and wet season (December 1998-September 1999). Fruits removed were classified in the following categories: (i) predated by vertebrates (crushed pyrenes); (ii) infested by bruchid and Scolytidae beetles (pyrenes with small one-to-three 2-3 mm opercules and endosperm absent); (iii) left under the crowns; and (iv) removed away from parents.
2.4.2. Pyrene secondary dispersal To estimate the rates of secondary dispersal and fate of secondarily dispersed pyrenes (seed plus endocarp),
Figure 2. Infructescence (a) and fruits (b) of Bactris acanthocarpa Mart. (Arecaceae).
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piles of 10 pyrenes (one pile per adult) were placed. Removed pyrenes were classified according to the same categories described above. This method was used because we previously observed that ripening fruits not removed from adults usually dried and dropped under the palm crowns. Removal of pyrenes was investigated from February to September 1999. Dispersal trials with tagged pyrenes were conducted during 16 months. These were based on a set of a 96 pyrenes which had been cleaned to allow adherence of an inconspicuous piece of epoxy used to cement the end of a 30 cm long copper filament (0.2 mm diameter). A small piece (5 cm) of bright-orange Vinyl flag numbered with permanent ink was then tied to the opposite end of the filament. Marked pyrenes were placed at 16 seed stations (piles of 6 pyrenes) near Bactris adults. This marking technique has been successfully used elsewhere [33, 40]. 2.5. Effects of burial on seed germination In order to evaluate the effects of pyrene burial on seed germination, post-dispersal infestation by beetles, and predation by vertebrates, we conducted experiments in a green-house and in the field. In the green-house, three treatments with 17 replicates were used: (i) buried pyrenes; (ii) pyrenes on the soil surface; and (iii) pyrenes on the soil surface covered by litter. For each treatment we used 50 pyrenes distributed in groups of 2-3, placed on 17 plastic pots (8 cm × 5 cm). Pots were protected against direct sunlight. Soil, litter and ripening fruits were collected in the study site. The experiment was followed during 16 months (September 1998-January 2000) and pyrenes were classified as intact or germinated. In the forest understorey, three treatments with 14 replicates were established: (i) pyrenes on the ground and protected from vertebrates by an exclosure (20 cm tall, 10 cm diamenter) built from galvanized wire cloth (mesh squares 5 mm each side); (ii) free-of-exclosure pyrenes on the ground; and (iii) buried pyrenes (23 cm deep). Piles of 6 pyrenes, obtained from ripening fruits in the study site, were placed at each station. This experiment was conducted by over 16 months (September 1998-January 2000), and pyrenes were classified as: (i) predated by vertebrates; (ii) infested by beetles; (iii) intact; (iv) removed; and (v) germinated. Beetle specimens were collected and identified by specialists at Universidade Federal do Paraná, Brazil. Specimens are available in the collection of the Invertebrate Laboratory, Universidade Federal de Pernambuco, Brazil. In order to confirm the effects of burial on seed germination we measured the depth of pyrene burial of 100 one-leaf seedlings sampled haphazardly in the
study site. Buried pyrenes were classified in three depth classes: (i) 0-2 cm; (ii) 2-4 cm; and (iii) > 4 cm deep. 2.6. Effects of distance from conspecific adults on post-dispersal seed predation We evaluated the effects of distance from conspecific adults on post-dispersal seed predation by using 10 focal adults of Bactris bearing fruits. For each adult, we set out three 10 m lines (in three cardinal directions). Each line received 10 pyrenes 1 m apart from each other, totalling 30 pyrenes per adult and 300 pyrenes offered. Seed fate was monitored for 6 months (March-September 1999). We limited the evaluation of seed predation to 10 m from conspecific adults due to the high local aggregation of Bactris. 2.7. Effects of distance from conspecific adults on seedling mortality In order to evaluate the effects of distance from conspecific adults on seedling mortality we selected one hundred one-leaf seedlings (5-10 cm tall) and measured their distances to the nearest conspecific adult. Mortality was followed weekly during 9 months (February-October 1999). Dead seedlings were classified in two broad classes of causes of mortality: herbivory (i.e., complete or partial removal of leaves and stems), and unknown causes. Based on 50 adults, we estimated the average crown diameter of adults by the following procedure: the largest plus the smallest crown diameter/2. This information was used to estimate the rate of seedling mortality under the adult crowns. 2.8. Spatial distribution of adults and seedlings of Bactris In order to assess the spatial distribution of Bactris in the study site, line-transect censuses were conducted along two trails 500 m long (each transect segment of 20 m). All individuals > 1 m tall detectable to 20 m from the transect were counted. We also recorded all adults in a 1 ha grid (25 plots, each 20 m × 20 m). We used the data from transects to produce two estimations of Bactris density in the study site. Morisita’s index of dispersion [29] was used to measure the extent to which Bactris adults were spatially clumped within the study plots, given a specified quadrat size. Thus, we considered two levels of analysis for spatial distribution: local (selected grove: 1 ha plot) and landscape (study area: 2 transects). The average nearest neighbour distance [29] was also estimated measuring the distance of the four nearest adults to 50 adults randomly selected. Seedling distribution around parents was investigated by measuring the distance
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between 100 one-leaf seedlings and the adult nearest to each of them. 2.9. Statistical analysis G-tests for independence [44] were used to compare differences in the proportion of: (i) fruits and pyrenes within categories of seed fate; (ii) pyrenes within categories of germination; (iii) seedlings within categories for depth of buried pyrenes; (iv) predated pyrenes within classes of distance from conspecific adults; (v) dead seedlings within classes of distance from conspecific adults; (vi) dead seedlings within causes of mortality; (vii) seedlings within classes of distance from conspecific adults; and (viii) adults within classes of distance from the nearest neighbour. All analyses were carried out using the SYSTAT 7.0 software package [49].
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predated by vertebrates, 8 (5.6%) disappeared and 4 (2.8%) were left intact. Fruits removed directly from infructescences and taken away from palms prevailed (G = 132.7, df = 3, P < 0.001). Among those left under the crowns, predation and infestation prevailed (G = 226.7, df = 1, P < 0.001). Thus, from 423 removed fruits, at least 129 (30.4%) were predated near the parents. In the study of secondary dispersal, among the 200 pyrenes piled near the palms, 121 (60.5%) were removed away from piles, 51 (25.5%) were predated by vertebrates, and 28 (14%) were infested by beetles. Removed pyrenes prevailed (G = 34.1, df = 2, P < 0.001). This represented a removal rate of 0.04 pyrene/palm/day. Unfortunately 90 marked pyrenes had the copper filament cut off, which prevented us from evaluating their fate. We retrieved 6 pyrenes, all of which were buried 2-3 cm deep and 0.12-5.3 m distant from the seed stations.
3. RESULTS 3.3. Effects of burial on seed germination 3.1. Diaspore dispersers/predators During the 400 h of palm observation black–rumped agoutis (Dasyprocta prymnolopha Wagler, 1831) were observed once scatterhoarding seeds. More specifically, an agouti manipulated ripening (completely red) fruits during ca. 30 min, picking and dropping ca. 30 fruits direct from one infructescence (40 cm above ground level), some of which were eaten (gnawed) immediately, whereas others were buried (2-3 cm deep) < 2.5 m from the palm. Fruits which were either eaten or buried had first their skin separated from the pulp. Guianan squirrels (Sciurus aestuans Linnaeus, 1766) were observed (n = 3) picking up ripening fruits directly from infructescences and subsequently eating them perched in small trees near the parents (< 4 m distant). During the 35 km of censuses seven sightings of agoutis were recorded, totalling 12 individuals (seven adults and five young). Density of agoutis was 8.5 individuals km–2. No rodents of any kind were trapped during nocturnal surveys. 3.2. Diaspore removal and seed fate In the study of primary dispersal, from 874 monitored ripening fruits, 423 (48.4%) were removed from adults and 451 (51.6%) remained attached to the infructescences (few dropped during fruit counts) in the 10 month period. This represented a fruit removal rate of 0.05 fruit/palm/day, which was similar among the twenty five palms recorded. Among the 423 fruits removed, fate of 321 was followed: 180 (56.1%) were removed away from palms and 141 (43.9%) were recorded under the crowns. Among the latter, 69 (48.9%) were infested by beetles, 60 (42.5%) were
Pyrenes left on the ground without exclosure were intensively predated (42%) by vertebrates (G = 59.8, df = 1, P < 0.001, seed fate comparison) (figure 3). Those protected by the vertebrate-exclosures were mostly attacked by beetles (54%) (G = 24.7, df = 2, P < 0.0001, seed fate comparison). Only seeds of buried pyrenes germinated (n = 4) after a 10-month period. In the green house, 11 seeds (7.3%) germinated (seven from buried and four from unburied pyrenes) after a 16-month period. Considering all pyrenes (forest and green-house) seed germination occurred preferentially in buried pyrenes (G = 4.56, df = 1, P = 0.03). Infestation by beetles was 28% in buried pyrenes and 54% in unburied pyrenes, a significant difference (G = 8.9, df = 1, P < 0.003). Pachymerus cardo Fahraeus, 1839 (Bruchidae) and Coccotrypes palmarum Eggers, 1933 (Scolytidae) were recorded infesting seeds, pre- and post- dispersal, respectively. Among the 100 seedlings sampled, 10 had pyrenes buried < 2.0 cm deep; 67 in the 2-4 cm deph class, and 23 had pyrenes buried > 4 cm deep. Thus, pyrenes buried > 2 cm deep prevailed (G = 11.3, df = 1, P = 0.001). 3.4. Effects of distance from conspecific adults on post-disperal seed predation and seedling mortality Among the 300 pyrenes piled around palms, only 11 were predated by vertebrates, whereas 138 were removed away from piles (46%). No significant relationship was found between predation or removal of pyrenes and distance from conspecific adults. In contrast, 30% of the one-leaf seedlings died during the
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Figure 3. Fate of Bactris pyrenes (n = 252) at Dois Irmãos Reserve, Brazil.
9-month period and seedling mortality was higher near the adults (< 4 m) than far (> 4 m) from them (G = 3.13, df = 1, P = 0.07) (figure 4a). Palm crown diameter varied between 1.3 m and 3.3 m, averaging 2.1 ± 0.49 (n = 30, mean ± SD), and most adults (96%) had crown diameter < 3 m (figure 4b). Thus, 80% of seedling mortality occurred under the adult crowns. Herbivory killed 5% of the one-leaf seedlings, less than mortality due to unknown causes (25%) (G = 29.1, df = 1, P < 0.001). 3.5. Spatial distribution of adults and seedlings of Bactris Adults of Bactris presented a clumped distribution in the study site and inside the grove (IP = 0,5: P < 0,001). Density of individuals > 1 m tall ranged from 8.7 ± 7.3 individuals 400 m–2 (mean ± SD, transect 1) to 15.8 ± 10.1 (transect 2), i.e., between 218 and 397 individuals ha–1. The spatial distribution of Bactris is thus best described as clumped at a local and landscape level. Most of the seedlings (96%) were within 4 m of adults (G = 186.1, df = 1, P < 0.001). The average nearest neighbour distance was 5.08 ± 2.3 m (n = 50, mean ± SD), and 64% of adults had the nearest neighbour > 4 m away (G = 10.4, df = 3, P < 0.01) (figure 5). These two patterns of spatial distribution (seedlings vs. nearest neighbours among adults) were significantly different (G = 99.1, df = 3, P < 0.001). 4. DISCUSSION 4.1. Seed dispersers/predators, seed-removal rate and seed fate Our results suggest that, among vertebrates, seeds of Bactris acanthocarpa are dispersed/predated exclu-
Figure 4. Percentage of early seedling mortality within classes of distance from conspecific adults (n = 100) (a), and of palms within classes of crown diameter (n = 50) (b) at Dois Irmãos Reserve, Brazil.
sively by agoutis (D. prymnolopha) and squirrels (S. aestuans). It is also suggested that seed removal is low (0.04-0.05 diaspore/palm/day), most seeds are predated and few are buried, always near the parents. Based on fruit morphology (red fruits < 15 mm length), we also expected Bactris seeds to be dispersed by large frugivorous birds (gape > 15 mm) and other partly-frugivorous vertebrates such as ungulates and primates. Bactris and other palms with fruits < 1.5 cm length (e.g., Euterpe, Geonoma) are referred to in the literature as endozoochorous, especially birds [37, 38]. The hypothesis of dispersal by birds in B. acanthocarpa is also reinforced by our observations in the study site which suggest that if ripening fruits are not directly removed from infructescences they remain attached to them more than 12 months before falling under the crowns. During this time, the pulp dries
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Figure 5. Percentage of Bactris seedlings within classes of distance from conspecific adults (n = 100), and of adults within classes of distance from the nearest neighbour (n = 50) at Dois Irmãos Reserve, Brazil.
(6 months after fruit ripening) and pyrenes are infested by beetles (Coccotrypes palmarum). Some seeds germinate and after that seedlings die trapped in the palm foliage above the ground. Effective palm seed dispersal by scatterhoarding rodents is usually associated with the presence of “seed shadows” in the ground [14, 43]. There are 19 large-gaped birds (e.g., cotingas, curassaws, guans, trogons) in the Atlantic forest of northeastern Brazil [41]. Many of them were recorded in the study site or in adjacent forest remnants in the first half of last century [4, 35]. However, recent studies in our study site [3, 11] have not recorded such birds, as well as ungulates (deer, tapir, peccaries) and red-handed howler monkeys- typical animals from this tract of the Atlantic forest [12]. Other rodents recognised as seed dispersers of palms, e.g. Proechimys, Myoprocta and Heteromys [8, 14, 22, 43], were not recorded in this tract of the Atlantic forest (i.e. north of São Francisco River) [12]. Therefore, only agoutis and squirrels remain in the study site, but they appear not to be abundant. In some tracts of Amazonian forest, for instance, agouti density can reach 44 individuals km–2 [34]. The pattern of seed dispersal we found at Dois Irmãos may be typical of Bactris even in pristine forest. However, we hypothesise that dispersal of Bactris in the vertebrate-impoverished remnants of Atlantic forest is restricted to agoutis and squirrels. In those remnants with a pristine frugivorous-vertebrate fauna, in contrast, seed dispersal is carried out by a myriad of other rodents and large-gaped birds promot-
ing higher rates of seed removal and to greater distances that those reported here. 4.2. Benefits of seed dispersal We found evidence that seed burial enhances seed germination as germination was much more frequent among the buried seeds and most of the one-leaf seedlings had pyrenes that had been buried > 2 cm deep. Advantages of seed burial by agoutis for germination have been widely documented in the literature [6, 13, 15, 42, 43, 45, 48], and burial is usually associated with seed protection against predation (by vertebrates and invertebrates) and better microclimatic conditions for germination. For instance, seed burial of Vouacapoua americana by agoutis and acouchis (Dasyprocta leporina and Myoprocta exilis) accelerates germination because microclimatic features prevent germination of unburied seeds during the short dry season [13]. In Astrocaryum standleyanum fruit peeling by agoutis (Dasyprocta punctata) removes invertebrate larvae before they have time to penetrate the endocarp of seeds [43]. In this study we recognised infestation of Bactris seeds by two beetle species. The first one is Pachymerus cardo, a 10 mm bruchid that infests fruits before they ripen. The second is Coccotrypes palmarum, a 1 mm beetle that infests fruits after seed dispersal. In buried pyrenes infestation by beetles was reduced by half and predation by vertebrates was not recorded. Thus, scatterhoarding of Bactris seeds by agoutis probably reduces seed infestation by beetles and seed predation by other vertebrates. High rates of pre- and
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post-dispersal seed predation by beetles (mainly bruchids) have also been recorded for other palms, such as Astrocaryum paramaca [14], A. macrocalyx [28], Scheelea zonensis [50] and S. rostrata [27]. Differences in seed removal or predation associated with distance from conspecific adults were not found in this study. In contrast, early seedling mortality was associated with the area covered by the palm crowns. Other results also reinforce the hypothesis that seedlings suffer higher mortality near parents (under the crowns vs. outside crowns): seedlings occurred preferentially < 2 m from adults, whereas adults were on average 5 m apart, and no saplings were observed under palm crowns. The source of this pattern of mortality (e.g., herbivores, competition) is not yet clear. There is, though, direct and indirect evidence that seed dispersal by agoutis and squirrels is advantageous to Bactris in relation to both seed and seedling survival. 4.3. Spatial distribution of B. acanthocarpa Our results confirmed previous accounts that Bactris has a clumped distribution, forming groves in the study site. Such groves of Bactris, in which adult nearest-neighbour distance averages 5 m and palm density can reach 397 individuals (> 1 m tall) in a single hectare, may be accounted for by three processes: low rates of seed removal, short-distance seed dispersal by agoutis and squirrels, and early seedling mortality beneath palm crowns. For several species of palms and other trees and shrubs, seed dispersal by agoutis has been identified as an important process affecting plant recruitment and spatial distribution [2, 13, 17, 45, 46]. There is also evidence that scatterhoarding by neotropical squirrels can affect plant distribution and recruitment [16, 19]. Agouti and other caviomorph rodents are usually short-distance seed dispersers (1-50 m), although some seeds may be removed > 50 m apart from parents [14, 17]. Dasyprocta leporina scatterhoards Bertholletia seeds to an average distance of 5 m, and rarely beyond 20 m [33]. Bertholletia tree groves in Amazonian forest can be largely accounted for by the quantitatively dominant effect of short distance dispersal by caviomorph rodents [33]. Although we have evidence that clumped distribution of Bactris is in part due to low rates of shortdistance seed dispersal by rodents, we are not able to conclude that this pattern would be typical of Bactris in pristine forest. Higher densities of agoutis and squirrels, and long distance seed dispersal by other mammals and by large-gaped frugivorous birds probably would modify plant recruitment and spatial distribution of Bactris in the study site. Unfortunately, local extinction of large frugivorous vertebrates is a
widespread situation in the remnants of the Atlantic forest of northeastern Brazil [1, 41]. It includes the large-gaped cracids, recognised as one of the most important groups of seed dispersers in neotropical forests [36], and caviomorph rodents (pers. obs.). Therefore, clumped distribution or within-grove high density of Bactris may just reflect the scarcity or ultimately the absence of long-distance dispersal events. Recent studies have predicted local extinction of plants by disruption of seed dispersal processes due to extirpation of frugivorous vertebrates [24, 36, 41]. However, we predict that some plant species might become spatially aggregated before they face local extinction if seed dispersal is diminished. 5. CONCLUSIONS Three general predictions were addressed at the beginning of this paper. It was expected that in B. acanthocarpa: (i) seed dispersal is carried out by mammals and large-gaped birds; (ii) benefits of seed dispersal include seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults would be influenced by seed dispersal patterns. In general these three predictions were confirmed, although seed dispersal in Bactris in the site we studied was restricted to two species of rodents. Extremely important is the fact that both seed dispersal ecology and demography of Bactris acanthocarpa may be at present affected by the local extirpation of large-gaped birds and other frugivorous vertebrates. Our conclusions and stated hypotheses require verification in the near future as they have important implications for species conservation in the Brazilian Atlantic forest. Acknowledgments. We thank the Brazilian Science and Research Council (Conselho Nacional Científico e Tecnológico, CNPq) for funding this study. We are also grateful to two anonymous reviewers that offered constructive criticisms on the manuscript.
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[40] Schupp E.W., Seed and early seedling predation in the forest understorey and in treefall gaps, Oikos 51 (1998) 71–78. [41] Silva J.M.C., Tabarelli M., Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil, Nature 404 (2000) 72–74. [42] Smythe N., Relationships between fruiting seasons and seed dispersal methods in a neotropical forest, Am. Nat. 104 (1970) 25–35. [43] Smythe N., Seed survival in the palm Astrocaryum standleyanum: evidence for dependence upon its seed dispersers, Biotropica 21 (1989) 50–56. [44] Sokal R.R., Rohlf F.J., Biometry, W.H. Freeman and Company, New York, 1995. [45] Spironello W.R., The Sapotaceae community ecology in a Central Amazonian forest: effects of seed dispersal and seed predation. PhD Thesis, University of Cambridge, 1999.
[46] Vandermeer J.H., Stout J., Risch S., Seed dispersal of a common Costa Rican rain forest palm (Welfia georgii), Trop. Ecol. 20 (1979) 17–26. [47] Veloso H.P., Rangel-Filho A.L.R., Lima J.C.A., Classificação da Vegetação Brasileira Adaptada a um Sistema Universal, IBGE, Rio de Janeiro, 1991. [48] Wenny D., Two-stage dispersal of Guarea glabra and G. kunthiana (Meliaceae) in Monteverde, Costa Rica, J. Trop. Ecol. 15 (1999) 481–496. [49] Wilkinson L., SYSTAT, version 6.0., SPSS, Chicago, Illinois, USA, 1996. [50] Wright S.J., The dispersion of eggs by a bruchid beetle among Scheelea palm seeds and the effect of distance to the parent palm, Ecology 64 (1983) 1016–1021.
Seed dispersal, plant recruitment and spatial distribution of Bactris acanthocarpa Martius (Arecaceae) in a remnant of Atlantic forest in northeast Brazil Maria G. Silva, Marcelo Tabarelli* Departamento de Botânica, Universidade Federal de Pernambuco, CEP: 50670–901 Recife, PE, Brazil
Received 6 October 2000; revised 4 August 2001; accepted 21 August 2001
Abstract – Seed dispersal ecology of Bactris acanthocarpa Mart. (Arecaceae), an Atlantic forest understory palm, was investigated during two years as an attempt to test the following predictions: (i) seeds of Bactris are dispersed by mammals and large-gaped birds; (ii) Bactris benefits from seed dispersal in terms of seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults is related to patterns of seed dispersal. The study was conducted at Dois Irmãos Reserve, a 387.4-ha reserve of Atlantic forest in northeastern Brazil (8º S–35º W). Black–rumped agoutis (Dasyprocta prymnolopha) and Guianan squirrels (Sciurus aestuans) were identified as the seed dispersers/predators, moving seeds short distances (< 4 m from parents) and at low rates (0.04-0.05 diaspore/palm/day). Pyrene burial prevented seed predation by vertebrates and reduced by half seed infestation by Scolytidae beetles. Only buried pyrenes germinated. Pyrene predation was not correlated with distance from conspecific adults. In contrast, early seedling mortality was higher near conspecific adults. Most adults (64%) had their nearest conspecific adult neighbour > 4 m away in contrast to 96% of seedlings that occurred concentrated within 4 m from adults (77% under the palm crowns). Here, we present evidence that spatial distribution of B. acanthocarpa is partly due to low rates of seed removal, short-distance seed dispersal by agoutis and squirrels, and early seedling mortality associated with presence of seedlings under palm crowns. © 2001 Éditions scientifiques et médicales Elsevier SAS Atlantic forest / Bactris / plant demography / rodents / seed dispersal
1. INTRODUCTION Seed dispersal has been recognised as one of the most important factors affecting plant recruitment, spatial distribution and long term viability of populations [2, 23, 26]. Benefits of seed dispersal usually include reduction in levels of seed predation, improvement of seed germination and colonisation of new habitats [9, 39]. Studies on palm dispersal ecology have identified rodents [17, 22, 32, 43], primates [8], birds [38] and ungulates [5, 18] as seed dispersers. Although some rodents and ungulates can function as both seed predators and dispersers, there are important benefits in terms of seed predation avoidance, seed germination and seedling survival associated with seed dispersal by
*Correspondance and reprints: Fax: +055 2181 2718350. E-mail address: [email protected] (M. Tabarelli).
vertebrates for palm species. For example, spiny rats (Proechimys semispinosus) may function as effective seed dispersers of Astrocaryum standleyanum if seeds are removed to favourable germination sites unavailable to other seed predators [22]. A similar situation is observed in seeds of A. mexicanum, which are protected from predation by other animals if they are scatterhoarded by Heteromys desmarestianus and agoutis (Dasyprocta punctata) [6]. In addition to these benefits, seed dispersal can affect the spatial distribution of palms. The small seeds (< 2 cm length) of Euterpe edulis, an Atlantic forest understory palm, are dispersed by toucanets, cracids and agoutis, at short and long distances [35]. Euterpe edulis can show both clumped or random distribution if rodents or birds act as dispersers [37]. In contrast, Astrocaryum paramaca is dispersed at short distances (< 50 m) only by spiny rats (Proechymis spp.) and acouchis (Myoprocta exilis) [14]. Evidence from other
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tree species also suggests that seed dispersal by rodents may result in clumped distribution of adult plants [33]. Bactris acanthocarpa Martius is an understory palm species that occurs in both the Amazonian and Atlantic rain forest of Brazil. It has small (< 15 mm diameter), orange to red fruits attached to exposed infructescences near the ground level [30]. Several species of Bactris have been described in the literature as gutdispersed species, specially large-gaped birds [38]. In addition other palm species with fruit morphology similar to Bactris (i.e., orange to red/purple-black fruits < 15 mm diameter) have mammals and largegaped birds as effective seed dispersers [37, 38]. Therefore the following predictions can be made about B. acanthocarpa: (i) seed dispersal is carried out by mammals and large-gaped birds; (ii) benefits of seed dispersal will include seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults will be related to patterns of seed dispersal. Seed dispersal ecology of B. acanthocarpa was investigated during two years in a remnant of the Brazilian Atlantic forest to test these predictions. In particular, we identify the seed dispersers/predators, rates of fruit/pyrene removal, and also analyse the benefits of seed burial relative to predation and germination. Furthermore, we test the correlation between seed predation, seedling mortality and distance from conspecific adults. Finally, we discuss possible effects of dispersal by rodents upon spatial distribution of B. acanthocarpa. 2. METHODS 2.1. Study site This study was conducted at Dois Irmãos Reserve (8ºS–35ºW), a 387.4-ha reserve of Atlantic forest, in the State of Pernambuco, northeastern Brazil (figure 1). At present Dois Irmãos is isolated from other forest remnants by sugar cane an by urban areas [31]. The study site is located on low altitude plateaus (10-100 m a.s.l.) of Formação Barreiras, where prevailing soils are latosols [25]. The climate matches Koeppen’s tropical (As’), with a 3-month dry season [10]. The annual rainfall is around 2460 mm, with the wettest period between March and August [10]. The vegetation can be classified as tropical lowland rain forest (terra firme forest), one of the Brazilian Atlantic forest types that occurs at 50-100 m altitude [47]. The study site presents a plant community similar to other Atlantic lowland forests described in the literature, with Leguminosae, Lauraceae, Euphorbi-
aceae, Melastomataceae and Sapotaceae as the richest families [20]. Detailed information on plant species, birds and mammals in the study site is available in the literature [31]. 2.2. Bactris acanthocarpa Martius Bactris acanthocarpa is an understory palm species that occurs in the Amazonian and lowland Atlantic forest [21]. Stems are medium-sized (< 2 m tall), spiny, solitary or clustered. Leaves (5-15) are pinnate and densely covered with black spines [30]. Fruits are one-seeded obovoid drupes. In the study site they are 12.3 ± 1.5 mm (mean ± SD, n = 50) diameter, orange to red and covered with short spinules (figure 2). Pericarp is thin (< 1 mm) and the mesocarp is pulpy (1-2 mm). Pyrenes are globular with a coconut-like endosperm [21]. Infructescences are usually exposed near ground level (< 1 m height) and contain over 100 fruits (54-196, n = 10). Ripening fruits are not dropped beneath the parents, therefore not producing “seed shadows”. 2.3. Diaspore dispersers In order to identify diurnal fruit removers 14 focal adults bearing ripening fruits were selected in six different areas in the study site. Observations were carried out using 10 × 40 binoculars during 3 h intervals of daylight early in the morning (06400-09400 h) and at dusk (16400-19400), periods which usually overlap the foraging peak of agoutis and squirrels [32, 33]. Observations were conducted 25-30 m distant from focal adults, which were observed during a one-year period (January-December 1998), totalling 400 h of palm observation. Agoutis and squirrels were censused in the study site by line transect sampling [7]. A straight trail of 1000 m length and 1 m wide was cut in the best preserved tract of forest. Distance of sighting was limited to 20 m outward transect. Diurnal censuses started before sunrise or early morning and terminated before1 h of survey. Effort was made to keep the walking speed as constant as possible at ca. 1 km h–1. Thirty five censuses were carried out, totalling 35 km walked, over 35 h of sampling during five months (February-August 2000). We estimated agouti density by dividing the number of individuals recorded by the total area sampled (transect length × number of censuses × 40 m). Nocturnal surveys were not carried out since there was no evidence for nocturnal activity of medium to large-bodied nocturnal rodents that act as seed dispersers in the study site [11, 12]. To identify small-bodied nocturnal fruit removers 30 traps (similar to Tomahawk 16” × 5” × 5”) were placed in 1-ha grid in a Bactris palm stand. Ripening fruits of Bactris, peanut butter and fresh cassava roots
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20 adults were selected. Beneath these adults artificial
Figure 1. Location of the study site- Dois Irmãos Reserve, Brazil.
were used as baits. Trapping was conducted during a three-month period (July-September 1999). 2.4. Rate of diaspore removal and seed fate
2.4.1. Fruit primary dispersal In order to estimate rates of fruit removal from parents, 25 adults bearing ripening fruits were selected inside a 2-ha plot. Fruit removal was censused three times a week during a 10-month period including dry and wet season (December 1998-September 1999). Fruits removed were classified in the following categories: (i) predated by vertebrates (crushed pyrenes); (ii) infested by bruchid and Scolytidae beetles (pyrenes with small one-to-three 2-3 mm opercules and endosperm absent); (iii) left under the crowns; and (iv) removed away from parents.
2.4.2. Pyrene secondary dispersal To estimate the rates of secondary dispersal and fate of secondarily dispersed pyrenes (seed plus endocarp),
Figure 2. Infructescence (a) and fruits (b) of Bactris acanthocarpa Mart. (Arecaceae).
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piles of 10 pyrenes (one pile per adult) were placed. Removed pyrenes were classified according to the same categories described above. This method was used because we previously observed that ripening fruits not removed from adults usually dried and dropped under the palm crowns. Removal of pyrenes was investigated from February to September 1999. Dispersal trials with tagged pyrenes were conducted during 16 months. These were based on a set of a 96 pyrenes which had been cleaned to allow adherence of an inconspicuous piece of epoxy used to cement the end of a 30 cm long copper filament (0.2 mm diameter). A small piece (5 cm) of bright-orange Vinyl flag numbered with permanent ink was then tied to the opposite end of the filament. Marked pyrenes were placed at 16 seed stations (piles of 6 pyrenes) near Bactris adults. This marking technique has been successfully used elsewhere [33, 40]. 2.5. Effects of burial on seed germination In order to evaluate the effects of pyrene burial on seed germination, post-dispersal infestation by beetles, and predation by vertebrates, we conducted experiments in a green-house and in the field. In the green-house, three treatments with 17 replicates were used: (i) buried pyrenes; (ii) pyrenes on the soil surface; and (iii) pyrenes on the soil surface covered by litter. For each treatment we used 50 pyrenes distributed in groups of 2-3, placed on 17 plastic pots (8 cm × 5 cm). Pots were protected against direct sunlight. Soil, litter and ripening fruits were collected in the study site. The experiment was followed during 16 months (September 1998-January 2000) and pyrenes were classified as intact or germinated. In the forest understorey, three treatments with 14 replicates were established: (i) pyrenes on the ground and protected from vertebrates by an exclosure (20 cm tall, 10 cm diamenter) built from galvanized wire cloth (mesh squares 5 mm each side); (ii) free-of-exclosure pyrenes on the ground; and (iii) buried pyrenes (23 cm deep). Piles of 6 pyrenes, obtained from ripening fruits in the study site, were placed at each station. This experiment was conducted by over 16 months (September 1998-January 2000), and pyrenes were classified as: (i) predated by vertebrates; (ii) infested by beetles; (iii) intact; (iv) removed; and (v) germinated. Beetle specimens were collected and identified by specialists at Universidade Federal do Paraná, Brazil. Specimens are available in the collection of the Invertebrate Laboratory, Universidade Federal de Pernambuco, Brazil. In order to confirm the effects of burial on seed germination we measured the depth of pyrene burial of 100 one-leaf seedlings sampled haphazardly in the
study site. Buried pyrenes were classified in three depth classes: (i) 0-2 cm; (ii) 2-4 cm; and (iii) > 4 cm deep. 2.6. Effects of distance from conspecific adults on post-dispersal seed predation We evaluated the effects of distance from conspecific adults on post-dispersal seed predation by using 10 focal adults of Bactris bearing fruits. For each adult, we set out three 10 m lines (in three cardinal directions). Each line received 10 pyrenes 1 m apart from each other, totalling 30 pyrenes per adult and 300 pyrenes offered. Seed fate was monitored for 6 months (March-September 1999). We limited the evaluation of seed predation to 10 m from conspecific adults due to the high local aggregation of Bactris. 2.7. Effects of distance from conspecific adults on seedling mortality In order to evaluate the effects of distance from conspecific adults on seedling mortality we selected one hundred one-leaf seedlings (5-10 cm tall) and measured their distances to the nearest conspecific adult. Mortality was followed weekly during 9 months (February-October 1999). Dead seedlings were classified in two broad classes of causes of mortality: herbivory (i.e., complete or partial removal of leaves and stems), and unknown causes. Based on 50 adults, we estimated the average crown diameter of adults by the following procedure: the largest plus the smallest crown diameter/2. This information was used to estimate the rate of seedling mortality under the adult crowns. 2.8. Spatial distribution of adults and seedlings of Bactris In order to assess the spatial distribution of Bactris in the study site, line-transect censuses were conducted along two trails 500 m long (each transect segment of 20 m). All individuals > 1 m tall detectable to 20 m from the transect were counted. We also recorded all adults in a 1 ha grid (25 plots, each 20 m × 20 m). We used the data from transects to produce two estimations of Bactris density in the study site. Morisita’s index of dispersion [29] was used to measure the extent to which Bactris adults were spatially clumped within the study plots, given a specified quadrat size. Thus, we considered two levels of analysis for spatial distribution: local (selected grove: 1 ha plot) and landscape (study area: 2 transects). The average nearest neighbour distance [29] was also estimated measuring the distance of the four nearest adults to 50 adults randomly selected. Seedling distribution around parents was investigated by measuring the distance
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between 100 one-leaf seedlings and the adult nearest to each of them. 2.9. Statistical analysis G-tests for independence [44] were used to compare differences in the proportion of: (i) fruits and pyrenes within categories of seed fate; (ii) pyrenes within categories of germination; (iii) seedlings within categories for depth of buried pyrenes; (iv) predated pyrenes within classes of distance from conspecific adults; (v) dead seedlings within classes of distance from conspecific adults; (vi) dead seedlings within causes of mortality; (vii) seedlings within classes of distance from conspecific adults; and (viii) adults within classes of distance from the nearest neighbour. All analyses were carried out using the SYSTAT 7.0 software package [49].
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predated by vertebrates, 8 (5.6%) disappeared and 4 (2.8%) were left intact. Fruits removed directly from infructescences and taken away from palms prevailed (G = 132.7, df = 3, P < 0.001). Among those left under the crowns, predation and infestation prevailed (G = 226.7, df = 1, P < 0.001). Thus, from 423 removed fruits, at least 129 (30.4%) were predated near the parents. In the study of secondary dispersal, among the 200 pyrenes piled near the palms, 121 (60.5%) were removed away from piles, 51 (25.5%) were predated by vertebrates, and 28 (14%) were infested by beetles. Removed pyrenes prevailed (G = 34.1, df = 2, P < 0.001). This represented a removal rate of 0.04 pyrene/palm/day. Unfortunately 90 marked pyrenes had the copper filament cut off, which prevented us from evaluating their fate. We retrieved 6 pyrenes, all of which were buried 2-3 cm deep and 0.12-5.3 m distant from the seed stations.
3. RESULTS 3.3. Effects of burial on seed germination 3.1. Diaspore dispersers/predators During the 400 h of palm observation black–rumped agoutis (Dasyprocta prymnolopha Wagler, 1831) were observed once scatterhoarding seeds. More specifically, an agouti manipulated ripening (completely red) fruits during ca. 30 min, picking and dropping ca. 30 fruits direct from one infructescence (40 cm above ground level), some of which were eaten (gnawed) immediately, whereas others were buried (2-3 cm deep) < 2.5 m from the palm. Fruits which were either eaten or buried had first their skin separated from the pulp. Guianan squirrels (Sciurus aestuans Linnaeus, 1766) were observed (n = 3) picking up ripening fruits directly from infructescences and subsequently eating them perched in small trees near the parents (< 4 m distant). During the 35 km of censuses seven sightings of agoutis were recorded, totalling 12 individuals (seven adults and five young). Density of agoutis was 8.5 individuals km–2. No rodents of any kind were trapped during nocturnal surveys. 3.2. Diaspore removal and seed fate In the study of primary dispersal, from 874 monitored ripening fruits, 423 (48.4%) were removed from adults and 451 (51.6%) remained attached to the infructescences (few dropped during fruit counts) in the 10 month period. This represented a fruit removal rate of 0.05 fruit/palm/day, which was similar among the twenty five palms recorded. Among the 423 fruits removed, fate of 321 was followed: 180 (56.1%) were removed away from palms and 141 (43.9%) were recorded under the crowns. Among the latter, 69 (48.9%) were infested by beetles, 60 (42.5%) were
Pyrenes left on the ground without exclosure were intensively predated (42%) by vertebrates (G = 59.8, df = 1, P < 0.001, seed fate comparison) (figure 3). Those protected by the vertebrate-exclosures were mostly attacked by beetles (54%) (G = 24.7, df = 2, P < 0.0001, seed fate comparison). Only seeds of buried pyrenes germinated (n = 4) after a 10-month period. In the green house, 11 seeds (7.3%) germinated (seven from buried and four from unburied pyrenes) after a 16-month period. Considering all pyrenes (forest and green-house) seed germination occurred preferentially in buried pyrenes (G = 4.56, df = 1, P = 0.03). Infestation by beetles was 28% in buried pyrenes and 54% in unburied pyrenes, a significant difference (G = 8.9, df = 1, P < 0.003). Pachymerus cardo Fahraeus, 1839 (Bruchidae) and Coccotrypes palmarum Eggers, 1933 (Scolytidae) were recorded infesting seeds, pre- and post- dispersal, respectively. Among the 100 seedlings sampled, 10 had pyrenes buried < 2.0 cm deep; 67 in the 2-4 cm deph class, and 23 had pyrenes buried > 4 cm deep. Thus, pyrenes buried > 2 cm deep prevailed (G = 11.3, df = 1, P = 0.001). 3.4. Effects of distance from conspecific adults on post-disperal seed predation and seedling mortality Among the 300 pyrenes piled around palms, only 11 were predated by vertebrates, whereas 138 were removed away from piles (46%). No significant relationship was found between predation or removal of pyrenes and distance from conspecific adults. In contrast, 30% of the one-leaf seedlings died during the
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Figure 3. Fate of Bactris pyrenes (n = 252) at Dois Irmãos Reserve, Brazil.
9-month period and seedling mortality was higher near the adults (< 4 m) than far (> 4 m) from them (G = 3.13, df = 1, P = 0.07) (figure 4a). Palm crown diameter varied between 1.3 m and 3.3 m, averaging 2.1 ± 0.49 (n = 30, mean ± SD), and most adults (96%) had crown diameter < 3 m (figure 4b). Thus, 80% of seedling mortality occurred under the adult crowns. Herbivory killed 5% of the one-leaf seedlings, less than mortality due to unknown causes (25%) (G = 29.1, df = 1, P < 0.001). 3.5. Spatial distribution of adults and seedlings of Bactris Adults of Bactris presented a clumped distribution in the study site and inside the grove (IP = 0,5: P < 0,001). Density of individuals > 1 m tall ranged from 8.7 ± 7.3 individuals 400 m–2 (mean ± SD, transect 1) to 15.8 ± 10.1 (transect 2), i.e., between 218 and 397 individuals ha–1. The spatial distribution of Bactris is thus best described as clumped at a local and landscape level. Most of the seedlings (96%) were within 4 m of adults (G = 186.1, df = 1, P < 0.001). The average nearest neighbour distance was 5.08 ± 2.3 m (n = 50, mean ± SD), and 64% of adults had the nearest neighbour > 4 m away (G = 10.4, df = 3, P < 0.01) (figure 5). These two patterns of spatial distribution (seedlings vs. nearest neighbours among adults) were significantly different (G = 99.1, df = 3, P < 0.001). 4. DISCUSSION 4.1. Seed dispersers/predators, seed-removal rate and seed fate Our results suggest that, among vertebrates, seeds of Bactris acanthocarpa are dispersed/predated exclu-
Figure 4. Percentage of early seedling mortality within classes of distance from conspecific adults (n = 100) (a), and of palms within classes of crown diameter (n = 50) (b) at Dois Irmãos Reserve, Brazil.
sively by agoutis (D. prymnolopha) and squirrels (S. aestuans). It is also suggested that seed removal is low (0.04-0.05 diaspore/palm/day), most seeds are predated and few are buried, always near the parents. Based on fruit morphology (red fruits < 15 mm length), we also expected Bactris seeds to be dispersed by large frugivorous birds (gape > 15 mm) and other partly-frugivorous vertebrates such as ungulates and primates. Bactris and other palms with fruits < 1.5 cm length (e.g., Euterpe, Geonoma) are referred to in the literature as endozoochorous, especially birds [37, 38]. The hypothesis of dispersal by birds in B. acanthocarpa is also reinforced by our observations in the study site which suggest that if ripening fruits are not directly removed from infructescences they remain attached to them more than 12 months before falling under the crowns. During this time, the pulp dries
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Figure 5. Percentage of Bactris seedlings within classes of distance from conspecific adults (n = 100), and of adults within classes of distance from the nearest neighbour (n = 50) at Dois Irmãos Reserve, Brazil.
(6 months after fruit ripening) and pyrenes are infested by beetles (Coccotrypes palmarum). Some seeds germinate and after that seedlings die trapped in the palm foliage above the ground. Effective palm seed dispersal by scatterhoarding rodents is usually associated with the presence of “seed shadows” in the ground [14, 43]. There are 19 large-gaped birds (e.g., cotingas, curassaws, guans, trogons) in the Atlantic forest of northeastern Brazil [41]. Many of them were recorded in the study site or in adjacent forest remnants in the first half of last century [4, 35]. However, recent studies in our study site [3, 11] have not recorded such birds, as well as ungulates (deer, tapir, peccaries) and red-handed howler monkeys- typical animals from this tract of the Atlantic forest [12]. Other rodents recognised as seed dispersers of palms, e.g. Proechimys, Myoprocta and Heteromys [8, 14, 22, 43], were not recorded in this tract of the Atlantic forest (i.e. north of São Francisco River) [12]. Therefore, only agoutis and squirrels remain in the study site, but they appear not to be abundant. In some tracts of Amazonian forest, for instance, agouti density can reach 44 individuals km–2 [34]. The pattern of seed dispersal we found at Dois Irmãos may be typical of Bactris even in pristine forest. However, we hypothesise that dispersal of Bactris in the vertebrate-impoverished remnants of Atlantic forest is restricted to agoutis and squirrels. In those remnants with a pristine frugivorous-vertebrate fauna, in contrast, seed dispersal is carried out by a myriad of other rodents and large-gaped birds promot-
ing higher rates of seed removal and to greater distances that those reported here. 4.2. Benefits of seed dispersal We found evidence that seed burial enhances seed germination as germination was much more frequent among the buried seeds and most of the one-leaf seedlings had pyrenes that had been buried > 2 cm deep. Advantages of seed burial by agoutis for germination have been widely documented in the literature [6, 13, 15, 42, 43, 45, 48], and burial is usually associated with seed protection against predation (by vertebrates and invertebrates) and better microclimatic conditions for germination. For instance, seed burial of Vouacapoua americana by agoutis and acouchis (Dasyprocta leporina and Myoprocta exilis) accelerates germination because microclimatic features prevent germination of unburied seeds during the short dry season [13]. In Astrocaryum standleyanum fruit peeling by agoutis (Dasyprocta punctata) removes invertebrate larvae before they have time to penetrate the endocarp of seeds [43]. In this study we recognised infestation of Bactris seeds by two beetle species. The first one is Pachymerus cardo, a 10 mm bruchid that infests fruits before they ripen. The second is Coccotrypes palmarum, a 1 mm beetle that infests fruits after seed dispersal. In buried pyrenes infestation by beetles was reduced by half and predation by vertebrates was not recorded. Thus, scatterhoarding of Bactris seeds by agoutis probably reduces seed infestation by beetles and seed predation by other vertebrates. High rates of pre- and
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post-dispersal seed predation by beetles (mainly bruchids) have also been recorded for other palms, such as Astrocaryum paramaca [14], A. macrocalyx [28], Scheelea zonensis [50] and S. rostrata [27]. Differences in seed removal or predation associated with distance from conspecific adults were not found in this study. In contrast, early seedling mortality was associated with the area covered by the palm crowns. Other results also reinforce the hypothesis that seedlings suffer higher mortality near parents (under the crowns vs. outside crowns): seedlings occurred preferentially < 2 m from adults, whereas adults were on average 5 m apart, and no saplings were observed under palm crowns. The source of this pattern of mortality (e.g., herbivores, competition) is not yet clear. There is, though, direct and indirect evidence that seed dispersal by agoutis and squirrels is advantageous to Bactris in relation to both seed and seedling survival. 4.3. Spatial distribution of B. acanthocarpa Our results confirmed previous accounts that Bactris has a clumped distribution, forming groves in the study site. Such groves of Bactris, in which adult nearest-neighbour distance averages 5 m and palm density can reach 397 individuals (> 1 m tall) in a single hectare, may be accounted for by three processes: low rates of seed removal, short-distance seed dispersal by agoutis and squirrels, and early seedling mortality beneath palm crowns. For several species of palms and other trees and shrubs, seed dispersal by agoutis has been identified as an important process affecting plant recruitment and spatial distribution [2, 13, 17, 45, 46]. There is also evidence that scatterhoarding by neotropical squirrels can affect plant distribution and recruitment [16, 19]. Agouti and other caviomorph rodents are usually short-distance seed dispersers (1-50 m), although some seeds may be removed > 50 m apart from parents [14, 17]. Dasyprocta leporina scatterhoards Bertholletia seeds to an average distance of 5 m, and rarely beyond 20 m [33]. Bertholletia tree groves in Amazonian forest can be largely accounted for by the quantitatively dominant effect of short distance dispersal by caviomorph rodents [33]. Although we have evidence that clumped distribution of Bactris is in part due to low rates of shortdistance seed dispersal by rodents, we are not able to conclude that this pattern would be typical of Bactris in pristine forest. Higher densities of agoutis and squirrels, and long distance seed dispersal by other mammals and by large-gaped frugivorous birds probably would modify plant recruitment and spatial distribution of Bactris in the study site. Unfortunately, local extinction of large frugivorous vertebrates is a
widespread situation in the remnants of the Atlantic forest of northeastern Brazil [1, 41]. It includes the large-gaped cracids, recognised as one of the most important groups of seed dispersers in neotropical forests [36], and caviomorph rodents (pers. obs.). Therefore, clumped distribution or within-grove high density of Bactris may just reflect the scarcity or ultimately the absence of long-distance dispersal events. Recent studies have predicted local extinction of plants by disruption of seed dispersal processes due to extirpation of frugivorous vertebrates [24, 36, 41]. However, we predict that some plant species might become spatially aggregated before they face local extinction if seed dispersal is diminished. 5. CONCLUSIONS Three general predictions were addressed at the beginning of this paper. It was expected that in B. acanthocarpa: (i) seed dispersal is carried out by mammals and large-gaped birds; (ii) benefits of seed dispersal include seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults would be influenced by seed dispersal patterns. In general these three predictions were confirmed, although seed dispersal in Bactris in the site we studied was restricted to two species of rodents. Extremely important is the fact that both seed dispersal ecology and demography of Bactris acanthocarpa may be at present affected by the local extirpation of large-gaped birds and other frugivorous vertebrates. Our conclusions and stated hypotheses require verification in the near future as they have important implications for species conservation in the Brazilian Atlantic forest. Acknowledgments. We thank the Brazilian Science and Research Council (Conselho Nacional Científico e Tecnológico, CNPq) for funding this study. We are also grateful to two anonymous reviewers that offered constructive criticisms on the manuscript.
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