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Seed dispersal and predation in the palm Syagrus romanzoffiana on two islands with different faunal richness, southern Brazil a

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Fernanda R. da Silva , Romualdo M. Begnini , Benedito C. Lopes & Tânia T. Castellani a

Centro de Ciencias Biologicas (CCB), Universidade Federal de Santa Catarina, Florianópolis, Brazil b

Departamento de Ecologia e Zoologia, (CCB), Universidade Federal de Santa Catarina, Florianópolis, Brazil Available online: 29 Sep 2011

To cite this article: Fernanda R. da Silva, Romualdo M. Begnini, Benedito C. Lopes & Tânia T. Castellani (2011): Seed dispersal and predation in the palm Syagrus romanzoffiana on two islands with different faunal richness, southern Brazil, Studies on Neotropical Fauna and Environment, 46:3, 163-171 To link to this article: http://dx.doi.org/10.1080/01650521.2011.617065

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Studies on Neotropical Fauna and Environment Vol. 46, No. 3, December 2011, 163–171

ORIGINAL ARTICLE Seed dispersal and predation in the palm Syagrus romanzoffiana on two islands with different faunal richness, southern Brazil Fernanda R. da Silvaa , Romualdo M. Begninia , Benedito C. Lopesb∗ & Tânia T. Castellanib a

Centro de Ciencias Biologicas (CCB), Universidade Federal de Santa Catarina, Florianópolis, Brazil; b Departamento de Ecologia e Zoologia, (CCB), Universidade Federal de Santa Catarina, Florianópolis, Brazil (Received 13 October 2010; accepted 22 August 2011)

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Palms are considered key species in tropical forests and represent a source of food for the community of frugivores in times of scarcity. Palms have also been used as a model to investigate how the processes of dispersal and seed predation are affected by fragmentation and alteration of tropical forests. This study examines the dispersal and seed predation of Syagrus romanzoffiana in two insular environments of different sizes (1500 ha and 50 ha) and faunal compositions, both located in the Brazilian Atlantic rainforest in Santa Catarina State, Brazil. We recorded 13 species of animals considered consumers and dispersers of fruits and seeds of S. romanzoffiana at the larger study area (Peri Lagoon Municipal Park, Santa Catarina Island) and five species on Campeche Island. In these areas, the rates of dispersal were high (Peri 57.5% to 75.5% and Campeche 81.5% to 93.0%, based on the removal experiments). In the smaller area, despite the low faunal richness, the coatis (Nasua nasua), introduced in the island were important seed dispersers. Only in Peri occurred predation by rodents (rates of 4%) due to the presence of agoutis (Dasyprocta azarae) and there was no post-dispersal predation by insects. The greatest loss of seeds (52% in both locations, based on sampling of seeds accumulated under parent plants) were caused by predation of Revena rubiginosa (Coleoptera, Curculionidae), of which oviposition occurs in the pre-dispersal phase. Besides this factor, about 40% of the seeds showed up without endosperm. However, high seed production seems to compensate for these losses, with significant seedling stock of S. romanzoffiana in both areas. Palmeiras são consideradas espécies-chave em florestas tropicais representando fonte de alimento para a comunidade de frugívoros em épocas de escassez. Palmeiras também têm sido usadas como modelo de estudo na avaliação de como os processos de dispersão e predação de sementes são afetados pela fragmentação e alteração das florestas tropicais. Este estudo examina a dispersão e predação das sementes de Syagrus romanzoffiana em dois ambientes insulares de diferentes tamanhos (1500ha e 50ha) e composições faunísticas, ambos localizados em área de Mata Atlântica no Estado de Santa Catarina, Brasil. Foram registradas 13 espécies de animais considerados consumidores e dispersores dos frutos e sementes de S. romanzoffiana na maior área estudada (Parque Municipal da Lagoa do Peri, Ilha de Santa Catarina) e cinco espécies na Ilha do Campeche. Nestas áreas, as taxas de dispersão foram altas (Peri 57,5% a 75,5% e Campeche 81,5% a 93,0%, com base em experimentos de remoção). Na menor área, apesar da baixa riqueza faunística, os quatis (Nasua nasua), introduzidos nessa ilha, foram importantes dispersores das sementes. Somente ocorreu predação por roedores no Peri (taxas de 4%) devido à presença de cotias (Dasyprocta azarae) e não houve predação pós-dispersão causada por insetos. A maior perda de sementes (52% em ambas as localidades, com base em amostragem de sementes acumuladas sob plantas-mãe) foi causada por predação de larvas de Revena rubiginosa (Coleoptera, Curculionidae), cuja oviposição ocorre na fase de pré-dispersão. Além deste fator, cerca de 40% das sementes mostravam-se sem endosperma. Contudo, a alta produção de sementes parece compensar essas perdas, havendo expressivo estoque de plântulas de S. romanzoffiana em ambas as áreas. Keywords: frugivory; agoutis; coatis; Revena rubiginosa; palm; Atlantic rainforest

Introduction Approximately 50–75% of woody plant species in Neotropical forests produce diaspores adapted to consumption and dispersal by vertebrates (Howe and Smallwood 1982; Peres and Van Roosmalen 2002), and may represent up to 90% of the tree species of these forests (Pimentel and Tabarelli 2004). This dispersal process is very important for tropical trees ∗

Corresponding author. Email: [email protected]

ISSN 0165-0521 print/ISSN 1744-5140 online © 2011 Taylor & Francis http://dx.doi.org/10.1080/01650521.2011.617065 http://www.tandfonline.com

(van der Pijl 1972; Cintra and Horna 1997; Casetta et al. 2002), especially for species with large seeds. These seeds are highly dependent on large frugivores and may be susceptible to extinction, due to high anthropogenic pressures on these animals such as hunting and habitat fragmentation (Chapman and Chapman 1995; Chapman et al. 2003; Donatti 2004; Pires 2006). Hunting and fragmentation are the main

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factors that lead to defaunation, which is the reduction of the animals’ richness and abundance in the forest (Redford 1992; Galetti et al. 2006). The loss of seed dispersers may lead to reduction of seed removal, increasing the mortality caused by pathogens, invertebrate and vertebrate predators, thus reducing seedling establishment and, consequently, the recruitment of species (Chapman and Chapman 1995; Cordeiro and Howe 2001; Donatti 2004; Galetti et al. 2006). The seeds and seedlings that remain near the parent plant are most affected by density and/or distancedependent mortality, and thus seed dispersal allows the escape from such high levels of predation (Janzen 1971a; Hubbell 1979; Howe and Smallwood 1982; Schupp 1992; Von Allmen et al. 2004; Guix 2006; Jordano et al. 2006). Palms are often considered as key resources for the frugivorous community in times of food scarcity (Bodmer 1990; Peres 1994, 2000; Henderson et al. 2000; Reis and Kageyama 2003). Studies have identified that rodents (Smythe 1989; Forget et al. 1994; Brewer 2001; Pimentel and Tabarelli 2004), primates (Peres and Van Roosmalen 2002), ungulates (Fragoso 1998) and birds (Zona and Henderson 1989; Reis and Kageyama 2000) are among the principal seed dispersers of these plants. Many papers also highlight the role of scatter-hoarding rodents as major primary and secondary dispersers of palms (Wright et al. 2000; Brewer and Webb 2001; Vieira et al. 2003; Pimentel and Tabarelli 2004). Although palm trees have many dispersers they may be considered vulnerable to fragmentation and loss of these agents when compared to species with small seeds, since the latter have more generalist dispersers (Silva Matos and Watkinson 1998; Wright et al. 2000; Donatti 2004; Pimentel and Tabarelli 2004; Pires 2006). Palms may also suffer from high levels of seed predation by beetles, especially bruchine beetles (Johnson et al. 1995), and seed loss can be up to 100% due to these agents (Smythe 1989; Cintra and Horna 1997; Vallejo-Marin et al. 2006). Seed removal rates are expected to be lower in forests with a low number of disperser species (Bleher and Böhning-Gaese 2001; Cordeiro and Howe 2001; Chapman et al. 2003), generating a greater accumulation in the vicinity of reproductive plants. Galetti et al. (2006) found that in small and more defaunated sites, seeds of Astrocaryum aculeatissimum presented a lower probability of being removed and/or stored, compared to larger and more preserved sites. Andreazzi et al. (2009) reviewed 74 studies about predation and seed dispersal of palms by mammals. It was found for the majority of studies concerning defaunation that the rates and distances of seed removal were lower in forest fragments or defaunated

sites, resulting in more seeds accumulated in the vicinity of parental plants. This accumulation resulted in increased predation by insects and small mammal seed predators. However, one exception was the study of Syagrus romanzoffiana in fragments of semideciduous forest, where predation by vertebrates was not affected by removal of large and medium-sized mammals. Also, the accumulation of seeds in the vicinity of these palms trees and the proportion of viable seeds were not affected by the degree of defaunation (Alves-Costa 2004). Syagrus romanzoffiana is a palm whose fruits are consumed by a wide variety of mammals, birds and invertebrates (Johnson et al. 1995; Guix and Ruiz 1997; Galetti et al. 2001; Alves-Costa 2004; Fleury and Galetti 2004; Rocha et al. 2004; AlvesCosta and Knogge 2005; Guimarães et al. 2005; Silva et al. 2007). The main predators of S. romanzoffiana seeds are the squirrel Sciurus ingrami (Bordignon and Monteiro-Filho 1999), the agouti (Alves-Costa 2004), and the insects Revena rubiginosa (Curculionidae; see Figure S2 of the Online Supplementary Material) and Pachymerus cardo (Chrysomelidae, Bruchinae). Oviposition of R. rubiginosa into the fruits occurs during the pre-dispersal phase (Alves-Costa and Knogge 2005; Brancalion et al. 2011) whereas the oviposition of P. cardo occurs in the post-dispersal phase (AlvesCosta 2004). On Santa Catarina Island, southern Brazil, large herbivorous seed dispersers such as tapir (Tapirus terrestris), white-lipped peccary (Tayassu pecari), collared peccary (Tayassu tajacu), deer (Mazama spp.) and capybara (Hydrochaeris hydrochaeris) are extinct (Olimpio 1995). However, there are still large fragments of Atlantic rainforest on the island, such as in Peri Lagoon Municipal Park (1500 ha), which host species of mammals including the crab-eating fox (Cerdocyon thous), the agouti (Dasyprocta azarae), the lowland paca (Cuniculus paca), the black-eared opossum (Didelphis aurita) (Graipel et al. 2001) and medium-sized birds such as toucans (Ramphastos dicolorus and R. vitellinus) and chachalacas (Ortalis guttata) (Naka and Rodrigues 2000). On the other hand, Campeche Island, a small island with 50 ha and distant 1.5 km from Santa Catarina Island, presents a particularly impoverished mammal fauna. Coatis (Nasua nasua) were introduced to the island in the 1950s and nowadays form groups up to 30 individuals (Bonatti 2006). There are no records of large bird species such as toucans (Ramphastidae) and cracids (Cracidae) on this island (Naka and Rodrigues 2000) and on both islands there are no squirrels present (Graipel et al. 2001). In spite of the differences between Peri Lagoon Municipal Park and Campeche Island concerning the

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Studies on Neotropical Fauna and Environment potential consumer and disperser of S. romanzoffiana, we expected: (1) similar rates of removal and consumption of fruits in both areas, resulting in similar seed accumulation near the parent plant; (2) greater proportion of seed predation by rodents in the Peri Lagoon Municipal Park, due to the presence of agoutis in this area; and (3) similar rates of postdispersal predation by insects considering similar rates of seed removal. This study intends to evaluate the processes of seed dispersal and predation of S. romanzoffiana in these areas by answering the following questions: (1) which vertebrate species are consumers and dispersers of its fruits? (2) What are the proportions of seeds consumed, predated, dispersed and accumulated near the parent plant? (3) Are the losses by predation affecting the species’ recruitment potential? Materials and methods Study species Syagrus romanzoffiana (Chamisso) Glassman (Arecaceae) occurs throughout the coastal states of Brazil from Bahia to Rio Grande do Sul, Paraguay, Argentina and Uruguay (Guix and Ruiz 2000; Lorenzi et al. 2004). Trees grow up to 10–15 m high and produce one to four infructescences (Figure S1, Online Supplementary Material), each with approximately 800 fruits (Galetti et al. 1992; Olmos et al. 1999). The fruit is a drupe with a fleshy and fibrous yellow pulp and a woody endocarp (Galetti et al. 1992; Olmos et al. 1999) and measures about 2.5 cm by 1.6 cm (Lorenzi 2002). Study sites Peri Lagoon Municipal Park (hereafter Peri) is located in the southern part of Santa Catarina Island (27◦ 42 30 –27◦ 46 30 S, 48◦ 30 00 –48◦ 33 30 W). Peri has a forested area of 1500 ha, being one of the best preserved forest remnants of the island. Secondary Atlantic rainforest predominates in larger portions of the area (CECCA 1997). Campeche Island (hereafter Campeche, 28◦ 40 23 – ◦ 28 40 28 S, 48◦ 28 42 –48◦ 27 37 W) measures 1580 × 600 m (53 ha) and has rocky shores, sand coastal (“restinga”) vegetation and secondary tropical rainforest (IPHAN 1998, Mazzer 2001). Peri and Campeche belong to the municipality Florianópolis in Santa Catarina State, Brazil. In both areas, a sector of secondary Atlantic rainforest in a late stage of succession with similar physiognomic characteristics was chosen. In Peri a pre-established trail with 2 km long and 1 m wide was used to access the palms. In Campeche three trails were used making up 2 km

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in total length. The distance between these trails was approximately 200 m. Survey of consumer and disperser species of S. romanzoffiana We evaluated the consumers of S. romanzoffiana fruits and their potential as dispersers through focal observations, camera traps, presence of seeds in feces and observation of seed marks. A total of 28 hours of focal observation was done per area on plants with high fruit production and on infructescences at 10 m height. Observations were performed alternating morning and afternoon periods on plants about 200 m away from each other. The observer was at least 10 m away from the palms. With binoculars (Tasco® 10×25) we recorded the frugivore species and their feeding habits, i.e. whether they swallowed the fruit or just consumed the pulp; whether they dropped the fruits or transported them in their beak away from the parent plant. Additional observations were made during walks on trails, totaling 60 h of fieldwork. During these walks it was possible to observe the interactions between the fauna and the fallen fruits, to find animal’s feces (which were searched S. romanzoffiana seeds) and find seeds on the ground (which were examined for tooth marks). Three camera traps (Tigrinus® conventional model 4.0C) were installed in each area to record the faunal consumers. The distance between cameras was 100 m. They were set with a 16-minute time delay between photographs and remained installed in the field for nine weeks during part of the fruiting period (June–August). Each camera was placed 50 cm above the ground, 4 m distant from a reproductive plant of S. romanzoffiana and was directed towards the fruits on the ground. Six reproductive plants were monitored in each area. In this study the following definitions were used: (a) seed – the seed itself together with the woody endocarp; (b) consumers – species that used the fruit pulp and/or the seed endosperm; (c) predators – species that damaged the endosperm causing the death of the embryo; (d) dispersers – species capable of carrying intact seeds and moving them away from the parent plant for distances of at least 50 cm. Assessing secondary removal of the fruits In order to evaluate fruit consumption and removal both under and away from the parent plants a field experiment was performed in June 2007. The mesocarp of ripe fruits was marked with stitching lines to enable the differentiation between experimentally deposited fruits and those naturally fallen to the

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ground (Figure S3, Online Supplementary Material). The marked fruits were visually checked for scars in the pulp that indicate the presence of beetle larvae (Alves Costa and Knogge 2005). Gloves were used while manipulating the fruit to prevent marking them with human scent. In each area, the rate of secondary removal was estimated using 40 plots of 10 fruits as described by Alves-Costa (2004). Twenty of these 40 plots were randomly distributed at a distance of 50 cm from the stems of 20 fruiting palms and the other 20 plots at a distance of 5 m from the same plants (totaling 400 fruits/area). Each of the fruit plots was marked with a small stake for later identification in the field. The fruits were monitored weekly, for four weeks, and none of them were replaced. At the end of the experiment the fruits were classified into four categories: (1) Intact: fruit was not removed and did not show any sign of use; (2) Pulp used by vertebrates: pulp partially or completely removed but endocarp undamaged; (3) Endocarp damaged by vertebrates: pulp partially or completely removed and teeth marks on the endocarp; and (4) Dispersed: fruit displaced for at least 50 cm or not found at all. The fruits not dispersed after 28 days of exposure were collected and taken to the laboratory for evaluation of post-dispersal predation. The randomized block analysis of variance was used to evaluate differences in the percentages of dispersed fruits near and far from the parent plant in each study area. These data were Arcsine transformed (Zar 1999) and the analyses were done using BioEstat 3.0 (Ayres et al. 2003). Assessing the accumulation of seeds around the parent plant In order to evaluate the differences regarding the accumulation and viability of seeds close to the parent plants, 10 individuals of S. romanzoffiana were sampled in each area. These individuals were at least 100 m distant from each other and at least 5 m from other conspecific adults. The selected palms were standing on flat ground and showed signs of at least five previous inflorescences. The samples were collected in the summer of 2007, after the 2006 fruiting period. The area around the palm crown was divided into four quadrants and one of these was randomly selected for the plot establishment. These plots measuring 50 × 50 cm were established 50 cm from the palm stem under the canopy of each individual. All fruits and seeds found within these plots were collected to a maximum depth of 10 cm. The material was sieved in the laboratory and the rotting seeds were discarded. The remaining seeds (free or still with adhering pulp) were counted and categorized

as: (1) preyed on by insects; (2) preyed on by vertebrates; (3) intact (intact endocarp) and presenting an endosperm (deemed viable); (4) intact but not presenting endosperm; (5) germinated; and (6) damage not identified. Predation by insects was recognized by exit holes and predation by vertebrates was recognized by teeth marks on the endocarp. When no external marks were found, the seeds were opened to check for the presence of insect larvae and endosperm. Seeds were kept in a terrarium in the laboratory until the emergence of adult insects, which were identified by Sérgio Vanin (MZUSP). The t-test (Zar 1999) was performed to evaluate whether the number of seeds/m2 and the percentage of damaged and viable seeds differed between the areas. Logarithmic transformation was employed to the data of number of seeds and arcsine transformations were employed to the data related to percentage of damaged and viable seeds (Zar 1999). The analyses were done using BioEstat 3.0 (Ayres et al. 2003).

Assessing the potential for recruitment in S. romanzoffiana The density of seedlings of S. romanzoffiana and their recruiting potential in the areas were evaluated in three plots (50 m × 10 m), which were randomly selected along the trails, totaling 1500 m2 (0.15 ha) at each study site following the main course of the trails. All S. romanzoffiana individuals within plots were assigned to one of the following classes of development: (1) seedlings with entire leaves only; (2) juveniles with entire and pinnate leaves; (3) juveniles with pinnate leaves only; (4) non-reproductive adult with exposed stem at 1.30 m and absence of reproductive signs; (5) reproductive adult with exposed stem at 1.30 m and presence of reproductive signs. The Kolmogorov–Smirnov (KD) test (Zar 1999) was performed to compare the distribution of plants in the different classes of development between the two study areas. Results Consumers and dispersers of S. romanzoffiana fruits A total of 13 species, eight birds and five mammals were observed visiting the infructescences or fallen fruits of S. romanzoffiana. Of these species, 11 were found in Peri and five in Campeche (Table 1). The bananaquit (Coereba flaveola), the violaceous euphonia (Euphonia violacea), the Brazilian tanager (Ramphocelus bresilius) and the tropical parula (Parula pitiayumi) fed on fruit pulp. During feeding these birds may drop fruits near the parent plant. Azure jays picked the fruits directly in the infructescence or on the

Studies on Neotropical Fauna and Environment Table 1. Vertebrate species identified as consumers of fruits of Syagrus romanzoffiana at Campeche Island and at Peri Lagoon Municipal Park, Florianópolis, Santa Catarina State, Brazil. Fruit consumption was either observed in the field (O), inferred by photographs (P), tooth marks (M) or the presence of seeds in feces (F). Type of record

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Taxon Cracidae Ortalis guttata Ramphastidae Ramphastos vitellinus Ramphastos dicolorus Thraupidae Coereba flaveola Euphonia violacea Ramphocelus bresilius Corvidae Cyanocorax caeruleus Parulidae Parula pitiayumi Procyonidae Cerdocyon thous Nasua nasua Didelphidae Didelphis aurita Dasyproctidae Dasyprocta azarae Muridae Euryoryzomys russatus

Campeche

Peri

F O O O

O O

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p > 0.05). The fruits not dispersed were all consumed (near = 24.5% ± 31.0; far = 42.5% ± 36.7) and 4% of those near the parent plant presented signs of predation by agoutis. None of the fruits showed predation by insects. A similar situation was found on Campeche with no significant differences between the percentage of fruits dispersed near (93.0% ± 10.3) or far (81.5% ± 26.0) from the parent plant (F = 2.07; p > 0.05). The fruits not dispersed were all consumed (near = 7.0% ± 10.3; far = 18.5% ± 26.0), and showed no marks of predation by vertebrates. In general, the values obtained for the dispersed fruits were higher in Campeche, with almost 17.5% more fruit dispersed near the parent plant and 24.0% far from this.

O O

O, P

O

O F, P

O, P P O, P, F, M P

ground (Figure S4, Online Supplementary Material). They either swallowed the fruits in situ or transported them in the beak away from the parent plants. Chachalacas and toucans picked the fruits directly on the infructescences. The seeds were found in feces of chachalacas whereas the toucans regurgitated them. Fruit consumption by agoutis was observed in Peri (Figure S5, Online Supplementary Material) and for coatis in Campeche (Figure S6, Online Supplementary Material). These species used the fruits dropped on the ground, but the coatis also fed on fruits on the infructescences. In burrows of agoutis we found seeds of S. romanzoffiana in Peri, and were observed seeds with agouti teeth marks. The black-eared opossum and Russet rice rat were only registered by photo next to the fruits on the ground. The crab-eating fox was also registered by photo and seeds of S. romanzoffiana were found in its feces.

Accumulation of seeds around the parent plant The seed density near the parent plants did not differ between areas (Peri: 1624.8 ± 1729.9/m2 , Campeche: 1117.6 ± 883.7/m2 , t = 0.55; p > 0.05). Over 50% of the seeds collected had signs of predation by insects (Table 2) with similar proportions in both areas (t = 0.02; p > 0.05). Larvae of R. rubiginosa were identified as seed predators (Figure S2, Online Supplementary Material). The percentages of intact seeds without endosperm were also high (Table 2) but not significantly different between areas (t = 1.12; p > 0.05). These two factors were responsible for the loss of 88.1% of the seeds in Peri and 95.4% in Campeche. Predation by vertebrates was significantly higher in Peri (t = 3.16; p < 0.01) (Table 2). The percentages of germinated seeds were low and did not differ among areas (t = 0.29; p > 0.05). The percentage of seeds that remained viable was low, but significantly higher in Peri (t = 2.16; p < 0.05) (Table 2). A greater proportion of seeds would act in the regeneration of the population in Peri (8.0%) in comparison to Campeche (2.9%), considering the amount of seeds that remained viable and germinated (Table 2). Table 2. Comparison of seed condition in plots around fruiting Syagrus romanzoffiana palms (in %, mean ± SD) between Peri Lagoon Municipal Park (n = 10) and Campeche Island (n = 10), Florianópolis, Santa Catarina State, Brazil. Seed fate

Removal of the fruits by consumers All the 800 fruits of the removal experiment were found by frugivores and suffered some kind of interaction with animals, so no intact seeds were found. At Peri there was no difference between the percentage of fruits dispersed either near (75.5% ± 31.0) or far (57.5% ± 36.7) from the parent plant (F = 3.76;

Preyed on by insects Preyed on by vertebrates Damage unidentified Intact but no endosperm Germinated Intact with endosperm (viable)

Peri

Campeche

52.3 ± 12.9 2.1 ± 2.3 1.7 ± 2.2 35.8 ± 12.5 1.8 ± 2.5 6.2 ± 6.2

52.1 ± 16.7 0.3 ± 0.6 1.4 ± 2.1 43.3 ± 16.6 1.3 ± 1.7 1.6 ± 2.7

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Assessing the potential for recruitment in S. romanzoffiana In Peri 725 individuals corresponding to a density of 4833 individuals/ha were sampled, while in Campeche 693 individuals corresponding to a density of 4620 individuals/ha were classified. Class I comprised 92% of the individuals in Peri and 94.9% in Campeche (Figure 1). No differences were found between the areas regarding the distribution of plants in the proposed classes of development (KD = 0.03, p > 0.05).

In the present study the fruits of S. romanzoffiana were consumed by several bird and mammal species as reported by Frisch and Frisch (2005) and Andreazzi et al. (2009). All species of birds recorded were considered dispersers. Four of them may promote seed dispersal over long distances: the chachalacas and the two species of toucan that swallow and defecate or regurgitate the seeds after eating the pulp and the azure jay that carries the seeds away in the beak (Guix and Ruiz 2000; Reis and Kageyama 2000). The other four bird species may promote seed dispersal over short distances. These small birds may drop fruits during pulp feeding and according to Reis and Kageyama (2000) can be considered seed dispersers. PERI

100

CAMPECHE

90 Proportion of indivisuals (%)

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Discussion Consumers and dispersers of S. romanzoffiana fruits

80 70 60 50 40 30 20 10 0

1

2

3 4 5 Classes of palm development

Figure 1. Proportions (in %) of individuals of Syagrus romanzoffiana in different classes of development in Atlantic rainforest in Peri Lagoon Municipal Park and Campeche Island, Florianópolis, Santa Catarina State, Brazil. Class 1: seedlings with entire leaves; Class 2: juveniles with entire and pinnate leaves; Class 3: juveniles with pinnate leaves; Class 4: non-reproductive adult; Class 5: reproductive adult.

The five species of mammals were also considered dispersers in this study. Field observations confirm the potential to seed dispersal for the crab-eating fox, the coati and the agouti. The crab-eating fox and the coati are generalist mammals and can consume fruits of various palm trees, including S. romanzoffiana, and may act as seed dispersers (Rocha et al. 2004; Andreazzi et al. 2009). Coatis are important dispersers as they forage in groups, use a large number of fruits, defecate intact seeds, and have the ability to forage in a variety of habitats and move across great distances, thereby promoting the dispersal of seeds in different microhabitats (Alves-Costa and Eterovick 2007). Agoutis prey on the seeds of S. romanzoffiana but can be considered occasional dispersers due to the behavior of scatter-hoarding (Andreazzi et al. 2009), i.e. if seeds that were buried but not rediscovered later escape from predation (Henry 1999). There were no field records of the black-eared opossum and the Russet rice rat acting as S. romanzoffiana seed dispersers; however, several rice rats can disperse palm seeds by acting as scatter-hoarder for nine species of Syagrus (Andreazzi et al. 2009). We suggest that the black-eared opossum can move seeds at least over short distances during removal of the pulp. There is no evidence that this species swallows and defecates seeds of S. romanzoffiana since there are only records of pulp fibers after analysis of feces (Cáceres 2002; Cáceres et al. 2009). This study confirms a smaller number of dispersers of S. romanzoffiana in Campeche, mostly small birds. In Peri most of the animals are capable of dispersing the seeds over long distances. Seeds consumed, predated, dispersed and accumulated near the parent plant In our study the differences in the spectrum of potential dispersers between the studied areas did not interfere with seed accumulation, although the seed removal experiment showed slightly higher rates in Campeche, probably due to the introduced coatis. These results agree with the data of Alves-Costa (2004) that the degree of defaunation does not affect the accumulation of seeds in the vicinity of this palm species. In the absence of large mammals in both study areas, other dispersers such as small and medium-sized mammals and birds are promoting seed removal. In the two study areas the probability of detection of S. romanzoffiana fruits by frugivores was high both near and far from the parent plant, demonstrating the existence of animals that are sparsely present in the forest and that easily detect the presence of food on the ground (Reis and Kageyama 2000). In Peri, as expected, there were higher proportions of seeds with signs of predation by vertebrates due to

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Studies on Neotropical Fauna and Environment the agoutis in this area. However, predation was low in relation to the total amount of seeds produced and especially in relation to the proportion of seeds lost due to predation by Revena rubiginosa. The failure of embryo development (intact seeds without endosperm) was also an important mortality factor in this study. Besides predation, insufficient pollination, resource deficiency and development failure due to deleterious genetic combinations are the main causes of mortality of ovules and seeds during the pre-dispersal phase (Bawa and Webb 1984; Fenner and Thompson 2005). Also, seedless fruits and fruits with empty seeds may represent an escape from predation by insects, as originally proposed by Janzen (1971a, 1971b) and verified in later studies (Verdú and García-Fayos 1998). This idea is related to the inability of insect predators to discriminate between deceptive fruits and those containing filled seeds (Verdú and García-Fayos 2001).

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• Figure S2. Larvae of Revena rubiginosa (Curculionidae), a pre-dispersal seed predator of Syagrus romanzoffiana (Photo: Fernanda R. da Silva). • Figure S3. Fruits of Syagrus romanzoffiana in removal experiments (Photo: Romualdo M. Begnini). • Figure S4. The azure jay (Cyanocorax caeruleus) picking fruits of Syagrus romanzoffiana directly on the ground at Peri Lagoon Municipal Park (Photo: Romualdo M. Begnini). • Figure S5. The agouti (Dasyprocta azarae) eating fruit of Syagrus romanzoffiana at Peri Lagoon Municipal Park (Photo: Romualdo M. Begnini). • Figure S6. The coatis (Nasua nasua) picking fruits of Syagrus romanzoffiana at Campeche Island (Photo: Fernanda R. da Silva). Acknowledgments

Potential for recruitment in S. romanzoffiana The studied populations showed a low proportion of viable seeds due to pre-dispersal seed predation and failure of embryo development. Just 1.6% to 6.2% of the seeds accumulated near the parent plants were viable. Alves-Costa (2004) also found low rates of viable seeds in the vicinity of S. romanzoffiana, which ranged from 0.5 to 3.5%, irrespective of the level of defaunation of the evaluated fragments. Despite the high rates of seed loss observed in these populations, they showed a high proportion of seedlings and juveniles relative to adults, presenting potential for regeneration. We suggest that the high seed production of S. romanzoffiana may compensate for these losses, maintaining a seedling stock in both areas. Like other species of palms (Sarukhán et al. 1984; Rosa et al. 1998), S. romanzoffiana presents temporal variation in seed production. So, in years of high seed production there is a great number of seeds that escape predation (Silva 2008). According to Kolb et al. (2007) this is a common pattern in plants that suffer pre-dispersal predation and these populations may present an erratic recruitment.

Online Supplementary Material Additional illustrating material may be found in the online version of this article: • Figure S1. Syagrus romanzoffiana at Peri Lagoon Municipal Park (Photo: Romualdo M. Begnini).

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