Flora 205 (2010) 647–655

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Availability peak of caloric fruits coincides with energy-demanding seasons for resident and non-breeding birds in restinga, an ecosystem related to the Atlantic forest, Brazil Verônica Souza da Mota Gomes a,b,∗ , Marcos S. Buckeridge c,1 , Clóvis Oliveira Silva c,1 , Fábio Rubio Scarano d,e , Dorothy Sue Dunn Araujo d,f , Maria Alice S. Alves b,∗ a

Programa de Pós-Graduac¸ão em Ecologia, Universidade Federal do Rio de Janeiro, CCS, IB, Sala A1 008, CP 68020, 21941-590 Rio de Janeiro, RJ, Brazil Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 Maracanã, 20550-011 Rio de Janeiro, RJ, Brazil c Instituto de Botânica de São Paulo (Sec¸ão Fisiologia e Bioquímica de Plantas), Brazil d Departamento de Ecologia, CCS, IB, Universidade Federal do Rio de Janeiro, Caixa Postal 68020, CEP 21941-970, Rio de Janeiro, RJ, Brazil e Conservation International, Rua Barão de Oliveira Castro 29, 22460-280, Rio de Janeiro, Brazil f Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa Científica, Rua Pacheco Leão 915-CEP 22460-030, Rio de Janeiro, RJ, Brazil b

a r t i c l e

i n f o

Article history: Received 11 September 2009 Accepted 18 November 2009 Keywords: Energy Frugivory Lipids Pulp Scrub vegetation

a b s t r a c t We evaluated temporal variation and quality of food resources available to birds especially in two energydemanding seasons: one when there is a peak of molting residents and another when non-breeding individuals are the bulk of biomass of captured birds. Birds were captured and observed, as well as fruits counted and collected, in two restinga sites for 2 years. Molting resident birds may rely basically on the regularly produced Clusia hilariana and Erythroxylum spp. fruits as lipid-sources, while non-breeders count on Ocotea notata fruits (also rich in lipids) during their passage by the study site. We found that fruits with sugars, lipids or proteins were available throughout the whole period, but a more intense seasonal variation was observed for the before mentioned plant species. The birds studied are known to be potential seed dispersers of these plant species, which are important components of restinga plant community structure. © 2010 Elsevier GmbH. All rights reserved.

Introduction Knowledge of food resources for wild animals is essential for conservation and management decisions (Terborgh, 1986), particularly under aspects of global change scenarios (Walther et al., 2002; Kirby et al., 2008; Williams and Middleton, 2008). However, the uneven distribution of available relevant studies across vegetation types and the paucity of confirmed generalizations are obvious obstacles for practical measures. Mediterranean scrublands and tropical forests studies exist on fruit biology–bird relationships. Herrera (1982, 1984a,b, 1995, 1998) has found that Mediterranean birds were largely independent of variation in abundance and composition of fruits in the vegetation, although the coupling of the birds’ physiological demands and climate seasonality has resulted

∗ Corresponding authors at: Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 Maracanã, 20550-011 Rio de Janeiro, RJ, Brazil. Fax: +55 21 2334 0546. E-mail address: [email protected] (V.S.M. Gomes). 1 Present address: Departmento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matâo, 277-Caixa Postal 11461, CEP 05422-970, Cidade Universitária - Butantâ, SP, Brazil. 0367-2530/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2010.04.014

in a coevolved plant–bird system adapted to ripening seasons. In Neotropical forests, although some general patterns have been described (e.g., 50–90% - mostly 75% - of tree species produce fleshy fruits adapted to bird or mammal consumption; zoochorous fruits tend to be produced during the wet months of the year; Howe and Smallwood, 1982), there is large geographic variation in fruiting phenology and production patterns that challenges most generalizations. Examples can be quoted from Costa Rica (Koptur et al., 1988; Levey, 1988; Loiselle and Blake, 1991) and Brazil (Morellato et al., 2000; Mikich and Silva, 2001; Bencke and Morellato, 2002; Paise and Vieira, 2005; Reys et al., 2005; Marchioretto et al., 2007; Medeiros et al., 2007; Genini et al., 2009). Nevertheless, some general patterns are already wellestablished. It is well-known that most frugivorous birds, during energy-demanding events such as reproduction and molt, increase consumption of both fruits, which are lipid-rich, and insects, which are protein-rich (Fogden, 1972; Herrera, 1982; Moermond and Denslow, 1985; Jordano, 1992; Poulin et al., 1992). Thus, reproduction of resident birds may be tuned to the abundance of nutritious fruits (Skutch, 1980; Moermond and Denslow, 1985). Moreover, migratory bird success at reproductive sites may be influenced by the nutritional quality of food at passage sites (Norris et al., 2004). It is also widely known that some birds change habitats following

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(22◦ 16 13.2 S, 41◦ 38 50.3 W). The latter site has more open, lower vegetation than the former (Gomes, 2006), although they belong to the same plant formation (Pimentel et al., 2007). Similarly to the Atlantic forest, 67.5% of woody plant species of the open Clusia scrub are zoochorous (Pimentel, 2002). Fruiting phenology and Biochemical analyses

Fig. 1. Mean monthly temperature and rainfall at Restinga de Jurubatiba National Park, between 1997 and 2003 (Estac¸ão Vaporimétrica Agropecuárias Carapebus Ltda., approximately 2–3 km from the two study sites). Vertical bars are 95% confidence intervals. Inset: temperature and rainfall fluctuation from January 2002 to August 2004.

peaks of fruit abundance (Morton, 1977; Levey, 1988; Loiselle and Blake, 1991; Kimura et al., 2001; Ottich and Dierschke, 2003; Tellería and Pérez-Tris, 2003). From a plant’s viewpoint, it has often been reported that fruiting phenology is tuned to the passage of migratory bird dispersers, although it is difficult to distinguish evolutionary cause and effect (van Schaik et al., 1993). We aimed to investigate nutritional and temporal aspects of fruit availability for restinga (Brazilian sandy coastal plain vegetation) avifauna. Our specific questions were: (i) Is there a coincidence between birds’ energy-demanding seasons and energetic resource (fruit) availability? (ii) What plant species may support resident or non-breeding birds in energy-demanding seasons? Methods Study area The present study was carried out in the Restinga de Jurubatiba National Park (22◦ 17 S, 41◦ 41 W), on the coast of northern Rio de Janeiro state, southeast Brazil. This region is a Pleistocene sandy plain covered by a mosaic of plant communities collectively called Restinga. It contains many species in common with the Atlantic forest, but presents diverse physiological responses to a drier habitat (Duarte et al., 2005). There is a wet season from October to April and a drier season from May to September. Typically there is one truly dry month per year. Mean annual rainfall and temperature are 1200 mm and 22.6 ◦ C, respectively. During the first year of our study (August 2002 to July 2003) conditions were drier (822 mm) and rainfall fluctuated irregularly, while in the second (August 2003 to August 2004) rainfall was higher and more evenly distributed (1458 mm) (Fig. 1). Besides being drier, the first year was also warmer than the second, with higher maximum and mean temperatures. Thus, the 2 study years were extremes in a period of 7 years (1997–2003). This period of 7 years was in accordance with the long-term climate patterns of the region, as shown by Henriques et al. (1986), although the dry month in the present study was July and not June. The dominant plant formation is an open Clusia scrub, formed by vegetation patches up to 5 m tall that cover 20–48% of the soil, with sparse low vegetation in between. The Park also includes forest formations, an open Ericaceae scrub and herbaceous formations, comprising in total ten plant communities (Henriques et al., 1986; Araujo et al., 1998). The present work was carried out in the open Clusia scrub at two sites: one near Comprida lagoon (22◦ 16 41 S, 41◦ 39 41 W) and the other approximately 2 km to the northeast

Fruiting phenology was studied to estimate variation in the availability of this food resource for frugivorous birds. Although most studies deal with fluctuation in fruit richness rather than fruit abundance, we preferred the latter, a more direct measure of fruit availability to birds. Sampling was area-based, as preferred by Blake et al. (1990), and included plant species in proportion to their abundance. However, we did not sample in square plots or transects, as restinga has much empty space (bare sand with scattered herbs) in between the vegetation patches. Instead, we chose patches of vegetation near the mist nets used to capture birds in order to count fruits regularly. To estimate sample area and volume, each vegetation patch was approximated to a geometric figure (circle or ellipse for the area of projection and cylinder or semi-ellipse for volumes). Total sampled area for each study area was 2184 and 1361 m2 , and volumes were 6332 and 2724 m3 , respectively. Ornithochorous fruits (sensu van der Pijl, 1972) were counted bimonthly on plants included in these patches. For compound fruits, each edible part that could be ingested by birds was counted as one fruit. The number of fruits was estimated whenever counting was imprecise, and although both ripe and unripe fruits were counted, only ripe fruits were used in the analysis of food availability (Blake et al., 1990). The Fruit Abundance Index proposed by Levey (1988) was calculated for each individual, and then summed per species for each month, to minimize large-crop effects, and was taken as a measure of fruit abundance. During the entire study period, fruit samples were collected directly from the plants and used for chemical analyses. We collected at least three intact ripe fruits (no sign of desiccation or herbivory) from each one of three individuals. However, the great difference in fruit abundances and pulp content among species resulted in high variability in number of fruits sampled. The pulp was weighed and then frozen or fixed in 100% ethanol until processing. Seeds were kept in a reference collection for comparison with bird-feces samples. The pulp was vacuumdried, weighed again and then analyzed to quantify soluble sugars, lipids and protein as a percentage of dry mass. A fraction of the dried pulp was submitted to lipid extraction procedure by using methanol–chloroform–water mixture (13:5:2) and the lipids were quantified gravimetrically (Bligh and Dyer, 1959). An aliquot corresponding to 1 mL of the aqueous fraction was vacuum-concentrated and was submitted to sugar quantification by the phenol–sulfuric acid method (Dubois et al., 1956). To estimate protein content, a fraction of the dried pulp was digested with concentrated sulfuric acid, which was titrated (Allen et al., 1974), and the resulting values of nitrogen content were multiplied by 5.64 (Levey et al., 2000). Available energy was calculated per fruit for each plant species following Schmidt-Nielsen (1998): 17.2 kJ g−1 for sugars or protein and 38.9 kJ g−1 for lipids. For 22 of the 30 fruit species consumed by birds (Gomes, 2006), it was possible to obtain dosages of sugars, lipids and protein (73% of the species, which represented 94% of fruits sampled), and therefore, they could be included in the analysis. Some plant specimens were collected and deposited by VSMG (codes 01–87) at Herbarium Bradeanum (Universidade do Estado do Rio de Janeiro). Bird sampling Birds were sampled with mist nets (2.5 m × 12 m; 36 mm mesh) and observations, alternating monthly between the two sampling

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methods. Ten nets were placed in line parallel to the coastline in each area. Nets were spaced 2–50 m apart next to dense vegetation that decreased visibility by the birds. They were opened bimonthly from 0600 to 1000 h and from 1400 to 1700 h, for two consecutive days, totaling 1820 net-hours in each area. Observations also avoided the midday hours and totalled 50 h in each area (for detailed observation methods see Gomes et al., 2008a). Captured birds were individually marked with aluminum bands and examined to determine age (gape mark) and presence of molt or reproduction (brood patch). Molting individuals were those with primary, secondary or rectrix molt (Mallet-Rodrigues and Noronha, 2001), and symmetric, to prevent recording accidental molt. Birds were kept in individual clean cloth bags for at least 15 min to obtain fecal/regurgitate samples. Legitimate frugivorous birds are considered to be those species that eat fruits and eliminate viable seeds according to Snow (1981) and Sick (1997). For the present study, a given bird species mentioned by these authors was included in this category only if it was observed eating fruits or whose fecal samples had fruits or seeds. Non-breeding frugivores were recognized from the literature (Sick, 1997; Gonzaga et al., 2000; Alves et al., 2004). Energy demands were established for the entire bird assembly, not for each species or individual. Given that energetic balance is correlated to body mass in birds (Blem, 2000), total biomass of individuals captured was used to establish energy-demanding months.

Results Non-breeding birds were the main group responsible for peaks in total bird biomass in June and August (Fig. 2A). Biomass of birds more than doubled from April to June 2003 and increased 17-fold from April to June 2004. It was not possible to define a reproduction period for the residents, given that only two individuals were captured with brood patches during the entire study period. The occurrence of juveniles also had no clear seasonality (Fig. 2B). However, biomass of molting individuals showed a tendency to be greater between February and April, possibly including December. The main non-breeding species contributing to the observed pattern was Turdus amaurochalinus (in June–August of all years it was 64–88% of non-breeders mass) and Turdus flavipes (reaching

Fig. 2. Variation in biomass of captured frugivorous birds, resident and nonbreeding birds (A) and residents presenting molt or young individuals (B) at Restinga de Jurubatiba National Park, during the study period.

33% in June 2004), to a lower degree. Still among non-breeders, an endangered species was found: Tangara peruviana (considered “vulnerable” by BirdLife International, 2008). Those three species are largely frugivorous (Table 1). The main resident species was

Table 1 Number of diet samples (feces and observations) containing fruits or arthropods for the frugivorous bird species captured at Restinga de Jurubatiba National Park (species and families following CBRO, 2009—Brazilian committee for ornithological records). Superior part: resident species; Inferior part: non-breeding species. Family

Species

N samples

Fruits (%)

Arthropods (%)

Coerebidae Columbidae Fringillidae Icteridae Mimidae Picidae

Coereba flaveola Leptotila rufaxilla Euphonia chlorotica Cacicus haemorrhous Mimus gilvus Celeus flavescens Picumnus cirratus Nemosia pileata Ramphocelus bresilius Thraupis sayaca Turdus albicollis Elaenia flavogaster Pitangus sulphuratus Tyrannus melancholicus

3 1 20 2 68 1 6 3 1 4 1 38 3 8

33 100 95 100 74 100 17 33 100 100 100 79 100 25

67 0 10 50 40 0 100 67 100 25 0 34 0 88

Cyanerpes cyaneus Tachyphonus coronatus Tangara peruviana Turdus amaurochalinus Turdus flavipes Elaenia sp. Elaenia chiriquensis Elaenia obscura Elaenia parvirostris

7 6 24 81 19 1 1 1 14

100 50 92 89 95 100 100 100 93

14 67 17 23 5 0 100 0 7

Thraupidae

Turdidae Tyrannidae

Thraupidae

Turdidae Tyrannidae

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Table 2 Number of diet samples (feces/regurgitate samples and observations) containing each fruit species for the main resident and non-breeding species during the two energy-demanding seasons. Plant species Anthurium maricense Byrsonima sericea Cassytha filiformis Clusia hilariana Erythroxylum ovalifolium Erythroxylum subsessile Gaylussacia brasiliensis Guapira opposita Humiria balsamifera Maytenus obtusifolia Miconia cinnamomifolia Myrsine rubra Myrsine parvifolia Myrtaceae Norantea brasiliensis Ocotea notata Pilosocereus arrabidae Paullinia weinmanniaefolia Smilax rufescens Unidentified Number of samples

Mimus gilvus (January–May)

Turdus amaurochalinus (May–September) 1

1 1 7 6 4

3 1 1 2

1 1 4 3 1 1 17 1 1

18

2 4 41

Mimus gilvus (38–85% of molting residents mass in February–April, followed by Mimus gilvus, with 0–43%), already shown by Alves et al. (2004). This species is also considered endangered, although at a regional level (Alves et al., 2000). Concerning their feeding preferences during those energy-demanding seasons, T. amaurochalinus fed mainly on Ocotea notata and M. gilvus on Clusia hilariana, Erythroxylum ovalifolium and E. subsessile (Table 2). All four plant species are lipid-rich ones (Table 3). Apparently, there was no season with extremely low abundance of fruits, and they were more abundant from February to August in both study years (Fig. 3A), coinciding with the two energy-demanding bird peaks, although in 2004 fruit abundance was greater than in 2003. Smilax rufescens produced many ripe fruits year-round, but mostly in June and August 2004. Pilosocereus arrabidae strongly influenced the recorded fluctuation of sugars (Fig. 3B), lipids (Fig. 3C) and energy (Fig. 3D) due to its large, heavy fruits. However, both plant species were poorly consumed by the main bird species (Table 2; Gomes 2006). Concerning plant species mostly consumed by the birds, as shown previously, Erythroxylum subsessile, E. ovalifolium and Clusia hilariana followed as important lipid-rich species (energy-rich) between February and April, while Ocotea notata was important in August. Erythroxylum ovalifolium was a particularly important resource in February 2004, when it displayed high values of fruit number and mass, and intermediate values of sugar and lipids, resulting in overall highenergy values. Indeed, total lipid availability was greater between February and August 2004 than in the same period of the previous year. Concerning year-to-year variation in fruit phenology, Erythroxylum ovalifolium and E. subsessile had more individuals fruiting in the second year of study, as well as more fruits per individual (Fig. 4). Ocotea notata had more fruits per individual in August 2002 than in the same month of 2003 and 2004, whereas Clusia hilariana did not show any clear differences between years. Discussion Considering the presented interspecific variation and seasonal fluctuation on nutritional contents of fruit pulp, the most important plant species that are presumably supporting birds during their energy-demanding seasons are the fruiting lipid-rich ones.

Here we discuss those plant species and what is known about their relationship to birds.

(1) Important plant species for resident birds: during energydemanding molting periods, resident bird species may count on the year-to-year regularly produced energetic resources of Clusia hilariana. The number of fruits produced per available female flower of Clusia hilariana is low or high depending on location (Faria et al., 2006; Martins et al., 2007). However, the high abundance of this species (Pimentel et al., 2007) probably results in an overall high number of fruits (Martins et al., 2007). Thus, regularity, abundance and nutritional quality make it an important food resource for birds. This is in harmony with previous papers that reported a key functional role for Clusia hilariana at this restinga site (Scarano, 2002). It is nurse plant to a high diversity of plant species and a hypothesis has been forwarded that this is largely so because it is a preferential resting place, shelter and nesting site for seed-dispersing birds (Liebig et al., 2001; Dias et al., 2005; Dias and Scarano, 2007). Our data therefore shows that the bird species also benefit from this interaction, thus characterizing a typical case of mutualism. Erythroxylum spp. were already described as important foodsources for the avifauna in another dry habitat, in Venezuela (Poulin et al., 1994). (2) Important plant species for non-breeding birds: non-breeding birds, on the other hand, may rely on Ocotea notata for lipids during their passage in the restinga between June and August. Turdus amaurochalinus was the non-breeding bird species whose fluctuation seemed to be most closely related to O. notata. It was present in lower numbers both in 2003 and 2004, when compared to 2002 (Gomes, 2006). Little is known about the travel routes of this species and of other non-breeding birds, although it is established that they perform intra-tropical migratory movements (Alves, 2007). Sick (1997) suspected that they travel from southern to northern Brazil and back in less than 6 months, and also that they barely travel in the hotter years. Indeed, climate may have played a role: in the drier, hotter June–August 2003, fewer non-breeding birds were captured than in the wetter, cooler June–August 2004. Considering weather conditions of the months preceding the peak of non-breeding bird captures, climate differences become more obvious. Therefore, climate is probably more important to the movements of non-breeding birds than fruiting of Ocotea notata alone, although its value as an energetic food resource remains.

Final remarks Our data showed that energy-demanding seasons for birds and energetic fruit production are tuned in restinga. Furthermore, our study suggests that non-breeding birds are part of a more delicate equilibrium of the plant–bird interactions than resident birds, as the main lipid-source has a great variation in fruit abundance among years (O. notata). Molting residents may count on the regular C. hilariana, and also have both Erythroxylum species as a back-up. Both groups of birds have an important role in plant community structure in the long-term through seed dispersal of nurse plant species (Zaluar and Scarano, 2000; Gomes et al., 2008b). Thus, maintenance of ecosystem processes is crucial to support the diversity of both local and regional avifauna, which in turn is essential to maintain plant community structure. Considering human pressure on coastal habitats as the restinga studied, Restinga de Jurubatiba National Park has a remarkable importance in the landscape context, through the preservation of a large area with passage routes of non-breeding birds, including endangered ones.

Table 3 Plant species studied at Restinga de Jurubatiba National Park and their fruit traits. Water is in percent of pulp fresh mass; sugar, lipids and protein are in percent of pulp dry mass; abundance index is the sum of month index (see text for abundance index); pulp dry mass per fruit is in grams; energy is in kilojoules; observations of ripe fruit were made bimonthly. Species

Water

Sugar

Lipids

Protein

Anacardiaceae

Tapirira guianensis Aubl. Xylopia ochrantha Mart. Anthurium maricense Nadruz & Mayo Aechmea nudicaulis (L.) Griseb. Protium icicariba (DC.) Marchand Cereus fernambucensis Lem. Melocactus violaceus Pfeiff. Pilosocereus arrabidae (Lem.) Byles & G. D. Rowley Capparis flexuosa (L.) L. Maytenus obtusifolia Mart. Clusia hilariana Schltdl. Garcinia brasiliensis Mart. Gaylussacia brasiliensis (Spreng.) Meisn. Erythroxylum ovalifolium Peyr. Erythroxylum subsessile (Mart.) O. E. Schulz Humiria balsamifera (Aubl.) A. St.-Hil. Cassytha filiformis L.

81.13

11.39

4.69

3.71

Annonaceae Araceae

Bromeliaceae

Burseraceae Cactaceae

Capparaceae Celastraceae Clusiaceae

Ericaceae

Erythroxylaceae

Humiriaceae

Lauraceae

Malpighiaceae MarcGraviaceae Melastomataceae

Ocotea notata (Nees) Mez Byrsonima sericea DC. Norantea brasiliensis Choisy Miconia cinnamomifolia (DC.) Naudin

Abundance index 50

Pulp dry mass per fruit 0.06

Energy per fruit

Ripe fruit 2002

0.28

5

Ripe fruit 2003

Ripe fruit 2004

February, April

February, April

August

August

86.80

10.16

1.84

3.27

208

0.01

0.02

August, October, December

February, April, June, August

February, April, June, August

76.54

8.28

2.57

3.10

72

0.05

0.16

August, October, December

August, October

August

30.48

14.52

1.27

4.19

75

0.04

0.16

February, December February

February, April

October, December

February

April, October, December

April

6

December

3 82.42

8.51

1.94

8.11

29

3.52

12.71

October, December

2

April, August

81.07

9.75

2.47

3.84

1

0.01

0.04

April

25.00

3.76

21.11

3.44

33

0.09

0.84

April

February, April

8

December

December

February

–

–

–

February, April, December April, June, August, October, December

February, April

8.32

4.02

2.13

–

49.16

10.46

9.80

2.68

195

0.07

0.43

88.02

8.34

11.71

2.99

235

0.03

0.19

August, October, December

50.38

11.78

1.22

1.66

96

0.14

0.39

August, October, December

66.32

9.11

6.16

5.41

62

0.06

0.32

26.23

6.78

21.20

5.42

99

0.04

0.46

August, October, December August, October

77.18

4.75

9.23

2.57

30

0.05

0.22

2 74.76

12.08

2.56

3.60

13

0.02

0.09

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Family

February, April, June, August

February, April, June, August, October, December April, June, August, October August, October

February, April, June, August

February

February

February

February

April, June, August August

February, December

651

652

Table 3 (Continued ) Energy per fruit

Species

Water

Sugar

Lipids

Protein

Myrsinaceae

Myrsine parvifolia A. DC Myrsine rubra M.F.Freitas & L.S.Kinoshita Calyptranthes brasiliensis Spreng. Eugenia umbelliflora O. Berg Myrcia lundiana Kiaersk. Myrciaria floribunda (H. West ex Willd.) Legrand Neomitranthes obscura (DC.) N.Silveira Guapira opposita (Vell.) Reitz Ouratea cuspidata (A. St.-Hil.) Engl. Heisteria perianthomega (Vell.) Sleumer Coccoloba arborescens (Vell.) How. Coccoloba declinata (Vell.) Mart. Chioccoca alba (L.) Hitchc. Paullinia weinmanniaefolia Mart. Manilkara subsericea (Mart.) Dubard Smilax rufescens Griseb.

81.81

10.93

7.40

2.85

88

93.15

3.54

29.50

5.47

–

86.97

8.53

7.49

3.32

29

0.02

0.08

39.05

12.59

4.90

4.58

12

0.23

1.10

56.70

11.13

3.35

3.61

39

0.07

0.28

Myrtaceae

Ochnaceae Olacaceae

Polygonaceae

Rubiaceae Sapindaceae

Sapotaceae

Smilacaceae

Theaceae

Viscaceae

Total 28

Ternstroemia brasiliensis Cambess. Phoradendron crassifolium (Pohl) Eichler 39

0.01

0.06

Ripe fruit 2002

Ripe fruit 2003

Ripe fruit 2004

August, October, Dec –

June, August, October –

June, August

August

June, August

June, August

June, August August, October, December

1

August, October, December

44 116

December, February December

11

48.48

12.05

5.32

10.05

17

0.09

0.50

82.76

8.40

3.14

2.93

3

0.03

0.08

76.51

6.47

11.32

43

0.02

92.15

10.70

1.15

84

0.02

9.09

3.13

2.89

938

0.07

0.23

29

2752

August

February, October, December December, February August, October, December

February, April, June, August

August, December

April, June, August, October April, June

February, April, June, August April, June

December

February, April

February, April

August, October, December

February, April, June, August, October, December April, August

February, April, June, August

December

August

37

31

August

22

February, October, December

April

14

(–) Represents absence of information for species not included in the studied vegetation patches.

August

April, June, August

0.06

27

54.73

August, October February

33

2.55

June

21

April, August

V.S.M. Gomes et al. / Flora 205 (2010) 647–655

Nyctaginaceae

Abundance index

Pulp dry mass per fruit

Family

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Fig. 3. Variation in ripe fruit traits during the study period at Restinga de Jurubatiba National Park. (A) Abundance, (B) total sugar, (C) total lipids, (D) total energy. Main fruiting species are: in gray, Smilax rufescens, in black, Pilosocereus arrabidae, Ch = Clusia hilariana, Eo = Erythroxylum ovalifolium, Es = Erythroxylum subsessile, On = Ocotea notata. (Note: protein variation was similar to sugar variation, although in much lower levels.)

Fig. 4. Mean (± standard deviation) number of ripe fruits per individual during the 13 months of study at Restinga de Jurubatiba National Park. Number of individuals with ripe fruit appears at the top of the error bars.

Acknowledgements We thank the staff of Laboratório de Ecologia de Aves/Universidade do Estado do Rio de Janeiro (UERJ) (especially A. Storni, A. Lagos, V. Tomaz); C. Ozanick, F. Mallet-Rodrigues, K. Amaral, D. Vrcibradic, C.H.P. Oliveira, E.C. Mendonc¸a, M. Janiszewski and R. Freitas for field assistance; M. Souza (Myrtaceae), C.F.C. Sá (plant community comments), M. Nadruz (Araceae), A. Quinet (Lauraceae), M.F. Freitas (Myrsinaceae) and C.H. de Paula (Vis-

caceae) for plant identification; CAPES (Brazilian Agency for Graduate Studies – Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior), FAPERJ (State Agency for Research – Fundac¸ão de Amparo à Pesquisa do Estado do Rio de Janeiro; process # 307213/06-4) and CNPq (Brazilian Agency for Research – Conselho Nacional de Desenvolvimento Científico e Tecnológico) for research grants and scholarships, Instituto Biomas and UERJ for the vehicles used in the field; L. Amaral, LIAPPN/UERJ staff, C. Marinho, the staff at Laboratório de Bioquímica de Insetos/IBioq/UFRJ, P. Mourão,

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