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1 December 2010 Predation of Adult Palms by Blackcapuchin Monkeys (Cebus nigritus) in the Brazilian Atlantic Forest
Carlos Rodrigo Brocardo, Henrique Santos Gonçalves, Valesca Bononi Zipparro, Mauro Galetti
Author Affiliations +

Introduction

Neotropical primates affect plant population through mutualistic intetactions, such as seed dispetsal, and antagonist interactions such as seed predation and hetbivoty (Peres, 1993; Russo and Augspurger, 2004; Mourthé et al., 2008). Primates killing trees through hetbivoty is rarely documented (Rocha, 2000; Santos et al., 2007). The genus Cebus (Erxleben, 1777) is considered as having the widest diet plasticity among neotropical primates, eating leaves, seeds, fruits, invertebrates and even vertebrates (Fedigan, 1990; Galetti and Pedroni, 1994; Susan and Rose, 1994; Rose, 1996; Ludwig et al., 2005; Carretero-Pinzón et al., 2008; Freitas et al., 2008). In this paper, we documented the predation of two palm species through the consumption of palm heart (apical meristem) by black-capuchin monkey (Cebus nigritus Goldfuss, 1809).

Materials and methods

Our observations were carried out between June 2009 and June 2010 in “Carlos Botelho” State Park (CBSP) (24°06′ and 24°14′S; 47°47′ and 48°07′W, in São Paulo State, Brazil. The CBSP has an area of 37,644 ha of Atlantic Forest, and it is located in the Forest Continuum of Paranapiacaba massif. The annual average temperature vatied from 15 to 19 °C, and the annual precipitation varied from 1700 to 2400 mm (Instituto Florestal, 2008). The density of black-capuchin monkeys in this site is estimated at 10.5 (± 2.4 SE) individuals/km2, and the average group size is 5.16 (±0.55 SE) individuals (Galetti et al., unpub. data).

The records of palm heart predation (directly and indirectly) were taken during line transects of mammal survey (430 km, approach 500 hours) and during the displacements to line transects in the forest (about 200 field hours). Despite that the C. nigritus groups were not accompanied directly, the animals are relatively habituated to observers. The line transects surveys were carried monthly (10–15 days per month), when we encounter predation events, ad libitum observations were made (with binoculars or naked eye), each predation event was recorded by a single observer. We sampled adult trees through randomized 15 0.04-ha plots, and juvenile trees through 15 0.01-ha plots to estimate the capuchin-monkey palm ptedation (sampling tree adapted from Durigan, 2003). Chi-square analysis was used to estimate differences in predation intensity between seasons.

Results

We observed capuchin-monkeys preying upon palm hearts of Euterpe edulis Mart. in 14 occasions, being 12 times in the Winter (May–August), once in the Summet (November–February), and once in the Autumn (February–May). We recorded from one to four capuchinmonkeys (sub-adult and adult) feeding simultaneously on apical meristem, but each animal on a different palm. The group size in these events varied from 3 to 12 blackcapuchin monkeys. Capuchin monkeys spend between 10 to 40 minutes (mean 25 ± 4 SE) to open the palm heart, varying principally with palm diameter. Initially, the monkeys bite the outer leaves, forcing them down using both hands, remaining supported with tail and posterior members on the palm stipe, then they repeat this process until liberate the apex of most leaves. After that, the animals bite the apex basis, to release it from the stipe, and consumed the apical metistem on other tree.

Figure 1.

A) Remains of consumed apical meristem by C. nigritus in CBSP. B) Recently withdrawn leaves of E. edulis on the ground.

f01_70.jpg

We found other 44 E. edulis killed by capuchins along the forest trails, of which 38 palms were killed in the Winter, four in the Summet, and two in the Autumn. The presence of recently signals permitted the identification of predation period (recently withdrawn leaves on the ground, recently destroyed apices and remains of consumed meristems; Fig. 1A and 1B). Other 12 palms were too old to determine the season of the predation (resting only the old destroyed apices). Considering direct and indirect observations of palms predation (only events where was possible determining the period of predation), the consumption of E. edulis differed significantly between seasons (χ2 = 73.0, df = 2, p < 0.001), being 10 times higher in the Winter than Summer, and 18 times greater than in the Autumn. The E. edulis palms killed had diameter at breast height from 8.6 to 15.4 cm (mean 12.8 ± 0.55 SE) and height from 7 to 20 m (mean 12.2 ± 0.94 SE). E. edulis is the most abundant arboreal plant in the study area, with a mean density of 93.3 (± 22.8 SE) adults/ha and 706.6 (± 90.7 SE) juveniles/ha. We estimated E. edulis adult mortality by capuchin monkeys at 1.7 (± 1.6 SE) individuals/ha per year (1.8 % of adult population).

Moreover, for the first time, we observed the predation of palm heart of Geonoma gamiova Barb. Rodr., an understory palm species, with height up to 4 m. Two adults G. gamiova were upon preyed by two adult capuchin monkeys (in the Winter). The process is similar to E. edulis, but beyond the animals supported on the palm, they supported in near lianas, taking for predation 8 minutes for a palm and 9 minutes for other.

Discussion

The distribution of E. edulis and C. nigritus overlaps in most part of their occurrence in the Brazilian Atlantic Forest (Vilanova et al., 2005; Herderson, 2000) (Fig. 2A). But, the palm heart predation by capuchin monkeys has been reported in a few places (Fig. 2B). In others areas we have worked, as the Iguaçu National Park (Araucaria Forest and Semidecidual Atlantic Forest, 185,262 ha continuous area, Paraná state, Brazil) and Semidecidual Atlantic Forest fragments in São Paulo state (“Mata São José” and “Mata Santa Genebra”, both approximately 250 ha), this behavior or predation signals were never recorded. It is possible that the use of this resource may be related to the group cultural inheritance, such as tool use and food-processing (Antinucci and Visalberghi, 1986; Rocha et al., 1998; Fragaszy et al., 2004; O'Malley and Fedigan, 2005; Canale et al., 2009). The group cultural inheritance in Cebus species, as well as other primate species, involves social learning, when the animals observe and interact with other group members, acquiring behaviors (Panger et al., 2002; Dindo et al., 2008; Dindo et al., 2009). The removal of the apical meristem demands dexterity and physical effort, being not accomplished by all members of a group, commonly this is done by some adults and sub-adults, and is observed for young animals.

Except humans, C. nigritus seems to be one of the only vertebrate able to prey upon apical meristem of adults E. edulis, since white-lipped peccaries (Tayassu pecari Link, 1795) prey upon apical meristem of saplings (F. Rocha-Mendes unp. data), and one of the few primates killing an atboreal plant (see Santos et al., 2007; Rocha, 2000). E. edulis is a palm with single stipe (differently of Euterpe oleracea), and removal of apical meristem leads to the death of individual. In forest fragments the main cause of mortality of E. edulis and Geonoma brevispetha (adult and juvenile palms) is the impact of meristem ptedation by black-capuchin monkeys (Souza and Martins, 2006; Santos et al., 2007; Portela, 2008; Portela et al., 2010). In areas where this behavior occuts, the capuchin monkeys may be helping to modeling the forest structure, similar to observed for ungulates (Silman et al., 2003; Wyatt and Silman, 2004; Beck, 2007). The palm heart predation by capuchins may have consequences for other species, especially birds, rodents and ungulates that depend on E. edulis fruits during the Winter (Galetti et al., 1999; Mikich, 2002). Nevertheless, this impact is much smaller than the one caused by human extraction, which may extirpate locally entire adult populations, being the higher threat to conservation of E. edulis (Galetti and Aleixo, 1998; Galetti and Fernadez, 1998; Pizo and Vieira, 2004).

Figure 2.

A) Distribution of Cebus nigritus (triangles) and Euterpe edulis (circles) in Brazil (adapted from Vilanova et al., 2005 and Herderson, 2000); B) Areas with records of apical meristem predation of E. edulis by C. nigritus: 1 -Poços das Antas Biological Reserve, fragment (Portela, 2008; Portela et al., 2010); 2 - Caetetus Ecological Station, fragment (R. Lázara pers. com.); 3 - CBSP, continuous (this paper, Taira, 2007); 4 -Intervales State Park, continuous (Zipparro and Galetti pers. ob.); 5 -Juréia-Itatins Ecological Station , continuous (P. Rubim pers. com.); 6 - “Mata” Doralice, fragment (Ludwig et al., 2005); 7 -Vila Rica do Espírito Santo State Park, fragment (Santos et al., 2007).

f02_70.jpg

Taira (2007) suggests that the consumption of palm heart in the Winter is an alternative source to insect scarcity, but not to fruit scarcity, which also occurs in the Winter at CBSP (Nakai, 2007). On the other hand, several papers concerning the diet of C. nigritus and congeners reported the use of alternative food resource in period of scarcity of fruits which normally constitute the main part of Cebus diet (Galetti and Pedroni, 1994; Peres, 1994; Freitas et al., 2008). Therefore, we suggest that palm heart of E. edulis and, at a lesser extent, of G. gamiova, might be considered as a fallback food of C. nigritus. Indeed, fallback foods are defined as “foods consumed during seasons when preferred foods are unavailable” (Altman, 1998) or as “foods whose use is negatively correlated with the availability of preferred foods” (Marshall and Wrangham, 2007; reviewed in Lambert, 2009). E. edulis is known as a keystone-species, providing fruits and seeds for several animal species during the time of greatest shortage (Galetti et al., 1999; Mikich, 2002). The consumption of meristem apical by C. nigritus, especially in the Winter, highlights another aspect of importance of this palm.

Acknowledgements

We thank the direction of CBSP and Fundação Flotestal do Estado de São Paulo for allowing to carry out this study. We thank F. Rocha-Mendes, P. Rubim and R. Lázara for sharing their data with us. This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) through the process BIOTA - FAPESP 2007/03392-6. C. R. B. and M. G. receives a CNPq fellowship (Conselho Nacional para o Desenvolvimento Científico e Tecnológico). V. B. Z. and H. S. G. received a FAPESP fellowship. We thank L. Culot and R. S. B. Gavira for improving the revision of manuscript. We thank referees for their comments and suggestions.

References

1.

S. A. Altmann 1998. Foraging for survival: yearling baboons in Africa. Chicago: University of Chicago Press. Google Scholar

2.

F. Antinucci and E. Visalberghi 1986. Tool use in Cebus apella: A case study. Int. J. Primatol. 7 (4): 351–363. Google Scholar

3.

H. Beck 2006. A review of peccary-palm interactions and their ecological ramifications across the Neotropics. J. Mammal. 87 (3): 519–530. Google Scholar

4.

G. R. Canale , C. E. Guidorizzi ,. M. C. M. Kierulff and C. A. F. R. Gatto 2009. First record of tool use by wild populations of the yellow-breasted capuchin monkey (Cebus xanthosternos) and new records for the bearded capuchin (Cebus libidinosus). Am. J. Primatol. 71:366–372. Google Scholar

5.

X. Carretero-Pinzón; T. R. Defler and S. F. Ferrari 2008. Observation of black-capped capuchins (Cebus apella) feeding on an owl monkey (Aotus brumbacki) in the Colombian llanos. Neotrop. Primates , 15 (2): 62–63. Google Scholar

6.

M. Dindo; B. Thierry and A. Whiten 2008. Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). P. R. Soc. B. 275: 187–193. Google Scholar

7.

M. Dindo , A. Whiten and F. B. M. de Waal 2009. Ingroup conformity sustains different foraging traditions in capuchin monkeys (Cebus apella). PLoS ONE , 4 (11): e7858. doi:10.1371/journal.pone.0007858. Google Scholar

8.

G. Durigan 2003. Métodos para análise da vegetação arbórea. In: Métodos de estudo em biologia da conservação e manejo da vida silvestre. L. Cullen ; C. Valladares-Paduá ; R. Rudran (Eds.). Curitiba: Universidade Federal do Paraná; Fundação O Boticátio de Proteção à Natureza, p.455–479. Google Scholar

9.

L. M. Fedigan 1990. Vertebrate predation in Cebus capucinus: meat eating in a neotropical monkey. Folia Primatol. 54: 196–205. Google Scholar

10.

D. Fragaszy , P. Izar , E. Visalberghi E.B. Ottoni and M. G. Oliveira 2004. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am. J. Primatol. 64:359–366. Google Scholar

11.

C. H. Freitas , E. Z. F. Setz , A. R. B. Araújo and N. Gobbi 2008. Agricultural crops in the diet of bearded capuchin monkeys, Cebus libidinosus Spix (Primates: Cebidae), in forest fragments in southeast Brazil. Rev. Bras. Zool. 25 (1): 32–39. Google Scholar

12.

M. Galetti and F. Pedroni 1994. Seasonal diet of capuchin monkeys (Cebus apella) in a semideciduous forest in south-east Brazil. J. Trop. Ecol. 10: 27–39. Google Scholar

13.

M. Galetti and A. Aleixo 1998. Effects of palm heart harvesting on avian frugivores in Atlantic rain forest of Brazil. J. Appl. Ecol. 35: 286–293. Google Scholar

14.

M. Galetti and J. C. Fernadez 1998. Palm heart harvesting in the Brazilian Atlantic Forest: Changes in industry struture and the ilegal trade. J. Appl. Ecol. 35: 294–301. Google Scholar

15.

M. Galetti , V. B. Zipparro and P. C. Morellato 1999, Fruiting phenology and frugivory on the palm Euterpe edulis in a lowland Atlantic forest of Brazil. Ecotropica , 5: 115–122. Google Scholar

16.

A. Henderson 2000. The Genus Euterpe in Brazil. Itajaí. In: Euterpe edulis Martius (Palmiteiro): biologia, conservação e manejo. M.S. Reis and A. Reis (Eds.). Itajaí: Herbário Barbosa Rodrigues, p. 1–22. Google Scholar

17.

Instituto Florestal. 2008. Parque Estadual Carlos Botelho: piano de manejo. São Paulo: Instituto Florestal. Google Scholar

18.

J. E. Lambert 2009. Summary to the symposium issue: primate fallback strategies as adaptive phenotypic plasticity-scale, pattern and process. Am. J. Phys. Anthropol. 140:759–766. Google Scholar

19.

G. Ludwig , L. M. Aguiar and V. J. Rocha 2005. Uma avaliação da dieta, da área de vida e das estimativas populacionais de Cebus nigritus (Goldfuss, 1809) em um fragmento florestal no norte do estado do Paraná. Neotrop. Primates 13 (3): 12–18. Google Scholar

20.

A. J. Marshall and R. W. Wrangham 2007. Evolutionary consequences of fallback foods. Int. J. Primatol. 28: 1219–1236. Google Scholar

21.

S. B. Mikich 2002. A dieta frugívora de Penelope superciliaris (Cracidae) em remanescentes de Floresta Estacional Semidecidual no Centro-Oeste do Paraná, Brasil e sua relação com Euterpe edulis (Arecacae). Ararajuba 10 (2): 207–217. Google Scholar

22.

I. M. C. Mourthé; K. B. Strier and J. P. Boulbi 2008. Seed predation of Mabea fistulifera (Euphorbiaceae) by northern mutiquis (Brachyteles hypoxanthus). Neotrop. Primates 15 (2): 40–45. Google Scholar

23.

É. S. Nakai 2007. Fissão-fusão em Cebus nigritus: Flexibilidade social como estratégia de ocupação de ambientes limitantes. MSc thesis. Instituto de Psicologia. Universidade de São Paulo, São Paulo. Google Scholar

24.

R. C. O'Malley and L. Fedigan 2005. Variability in food-processing behavior among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am. J. Phys. Anthropol. 128: 63–73. Google Scholar

25.

M. A. Panger; S. Perry; L. Rose; J. Gros-Louis; E. Vogel; K. C. Mackinnon and M. Baker 2002. Cross-site differences in foraging behavior of white- faced capuchins (Cebus capucinus). Am. J. Phys. Anthropol. 119:52–66. Google Scholar

26.

C. A. Peres 1994. Primates responses to phenological changes in an Amazonian Tetra Firme Forest. Biotropica 26 (1): 98–112. Google Scholar

27.

C. A. Peres 1993. Notes on the ecology of buffy saki monkeys (Pithecia albicans, Gray 1860): A canopy seed-predator. Am. J. Primatol. 31:129–140. Google Scholar

28.

M. A. Pizo and E. M. Vieira 2004. Palm harvesting affects seed predation of Euterpe edulis, a threatened palm of the Brazilian Atlantic Forest. Braz. J. Biol. 64(3B): 669–676. Google Scholar

29.

R. C. Q. Portela 2008. Ecologia populacional de três espécies de palmeiras em uma paisagem fragmentada no domínio Mata Atlântica, RJ. Doctoral thesis. Universidade Estadual de Campinas, Campinas. Google Scholar

30.

R. C. Q. Portela , E. M. Bruna and F. A. M. Santos 2010. Demography of palm species in Brazil's Atlantic forest: a comparison of harvested and unharvested species using matrix models. Biodivers. Conserv. 19:2389–2403. Google Scholar

31.

V. J. Rocha 2000. Macaco-prego, como controlar esta nova praga florestal? Floresta 30 (1/2): 95–99. Google Scholar

32.

V. J. Rocha , N. R. Reis and M. L. Sekiama 1998. Uso de ferramentas pot Cebus apella (Linnaeus) (Primates, Cebidae) para obtenção de larvas de Coleoptera que parasitam sementes de Syagrus romanzoffianum (Cham.) Glassm. (Arecaceae). Rev. Bras. Zool. 15 (4): 945–950. Google Scholar

33.

L. M. Rose 1997. Vertebrate predation and food-sharing in Cebus and Pan. Int. J. Primatol. 18 (5): 727–765. Google Scholar

34.

S. E. Russo and C. K. Augspurger 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol. Lett. 7: 1058–1067. Google Scholar

35.

C. V. Santos , M. M. Morais Jr, M. M. Oliveira , S. B. Mikich , C. R. Ruiz-Miranda and K. P. da L. Moore 2007. Ecologia, comportamento e manejo de primatas invasores e populações-problema. In: A Primatologia no Brasil. J. Bicca-Marques (Ed.), Vol. 10, Sociedade de Brasileira Primatologia, Porto Alegre. Pp. 101–108. Google Scholar

36.

A. F. Souza and F. R. Martins 2006. Demography of the clonal palm Geonoma brevispatha in a Neotropical swamp. Austral Ecol., 31: 869–881. Google Scholar

37.

M. R. Silman , J. W. Terborgh and R. A. Kiltie 2003. Population regulation of a dominant rain forest tree by a major seed predator. Ecology 84 (2): 431–438. Google Scholar

38.

P. Susan and L. Rose 1994. Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates 35(4): 409–415. Google Scholar

39.

J. T. Taira 2007. Consumo de palmito-juçara (Euterpe edulis Mart.) pot macacos-pregos (Cebus nigritus): Esttatégia de forrageamento ótimo ou requinte de um goumert? MSc Thesis. Instituto de Psicologia. Universidade de São Paulo, São Paulo. Google Scholar

40.

R. Vilanova , J. S. Silva Júnior , C. E. V. Grelle, G. Marroig and R. Cerqueira 2005. Limites climáticos e vegetacionais das distribuições de Cebus nigritus e Cebus robustus (Cebinae, Platyrrhini). Neotrop. Primates 13 (1): 14–19. Google Scholar

41.

J. L. Wyatt and M. R. Silman 2004. Distance-dependence in two Amazonian palms: effects of spatial and remporal variation in seed predator communities. Oecologia 140: 26–35. Google Scholar
Carlos Rodrigo Brocardo, Henrique Santos Gonçalves, Valesca Bononi Zipparro, and Mauro Galetti "Predation of Adult Palms by Blackcapuchin Monkeys (Cebus nigritus) in the Brazilian Atlantic Forest," Neotropical Primates 17(2), 70-74, (1 December 2010). https://doi.org/10.1896/044.017.0205
Published: 1 December 2010
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