Frugivory and Seed Dispersal by Birds in Cereus Jamacaru DC. Ssp. Jamacaru (Cactaceae) in the Caatinga of Northeastern Brazil
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DOI: http://dx.doi.org/10.1590/1519-6984.15312 Frugivory and seed dispersal by birds in Cereus jamacaru DC. ssp. jamacaru (Cactaceae) in the Caatinga of Northeastern Brazil Gomes, VGN.a,b*, Quirino, ZGM.b and Araujo, HFP.c aPrograma de Pós-graduação em Biologia Vegetal, Departamento de Botânica, Universidade Federal de Pernambuco – UFPE, Rua Prof. Nelson Chaves, s/n, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil bLaboratório de Ecologia Vegetal, Departamento de Engenharia e Meio Ambiente, Centro de Ciências Aplicadas e Educação, Universidade Federal da Paraíba – UFPB, Rua da Mangueira, s/n, Centro, CEP 58297-000, Rio Tinto, PB, Brazil cDepartamento de Ciências Biológicas, Centro de Ciências Agrárias, Universidade Federal da Paraíba – UFPB, Campus II, Rod. PB-079, s/n, Cidade Universitária, CEP 58397-000, Areia, PB, Brazil *e-mail: [email protected] Received: July 31, 2012 – Accepted: January 15, 2013 – Distributed: February 28, 2014 (With 2 figures) Abstract Studies of the dispersal modes of plants aid our understanding of the dynamics of resource and its availability for dispersal agents. The present work sought to characterize the fruiting patterns of the native Caatinga (dryland) cactus Cereus jamacaru, identify its principal dispersers, and evaluate the effects of seed passage through digestive tract of dispersers on its germination. Cereus jamacaru present an annual fruiting pattern and fruiting peaks occurred during June/2009 and February/2010. A total of 135 visits by nine species of resident Caatinga bird species were recorded. The most frequent visiting bird species were Paroaria dominicana and Euphonia chlorotica. Length of bird visits varied from 15 seconds to 4 minutes and seeds removed by birds travelled 10.6 ± 11.2 m until dispersers make the first landing perch, in some cases more than 40 meters away. Germination tests show birds had a high quantity of viable seeds of C. jamacaru in its feces. Seeds that passed through the digestive tract of birds showed a similar germinability of the seeds of the control group. However, the seeds dispersed by birds showed lowest mean germination time related to the control group seeds. This study highlights the potential role of birds as seed dispersers of C. jamacaru, swallowing the whole seeds and defecating intact seeds, accelerating the germination process and transporting seeds away from the mother plant. Keywords: frugivores, seed germination tests, phenology, ornithochory. Frugivoria e dispersão de sementes por aves em Cereus jamacaru DC. ssp. jamacaru (Cactaceae) na Caatinga, uma floresta seca no Nordeste do Brasil Resumo Estudos do modo de dispersão das espécies vegetais permitem o entendimento da dinâmica dos recursos e sua disponibilidade para os dispersores. O objetivo deste trabalho foi caracterizar o padrão de frutificação de Cereus jamacaru, uma espécie nativa da Caatinga, identificar os seus principais dispersores e avaliar o efeito da passagem das sementes pelo trato digestivo destes animais sobre sua germinação. Cereus jamacaru apresentou um padrão de frutificação anual, com pico de frutificação nos meses de Junho/2009 e Fevereiro/2010. No total foram registradas 135 visitas de nove espécies de aves frugívoras da Caatinga, sendo os dispersores mais frequentes Paroaria dominicana e Euphonia chlorotica. O tempo de duração das visitas foi curto, variando de 15 segundos a 4 minutos, e a distância média dos voos pós-alimentação foi 10,6 ± 11,2 m da planta-mãe, podendo também alcançar distâncias superiores a 40 metros. Os resultados dos testes de germinação mostraram que as aves apresentam uma alta quantidade de sementes viáveis de C. jamacaru em suas fezes. As sementes que passaram pelo trato digestivo das aves mostraram germinabilidade semelhante aquelas do grupo controle. No entanto, as sementes dispersadas pelas aves apresentaram um menor tempo médio necessário para germinação. Esse estudo destaca o papel das aves como potenciais dispersores de C. jamacaru, eliminando sementes intactas, acelerando o processo de germinação e carregando as sementes para longe da planta mãe. Palavras-chave: frugívoros, germinação, fenologia, ornitocoria. 32 Braz. J. Biol., 2014, vol. 74, no. 1, p. 32-40 Frugivory and seed dispersal of Cereus jamacaru 1. Introduction phenology, secondary dispersal and seed germination (Quirino, 2006; Andrade et al., 2006; Leal et al., 2007; Seed dispersal is an important stage in the reproductive Meiado et al., 2010). C. jamacaru demonstrates annual cycle of most plants (Wenny and Levey, 1998). Seed flowering and fruiting related to seasonal rainfall, with a dispersal by frugivorous animals constitutes a symbiotic zoochorous dispersal syndrome (Quirino, 2006; Leal et process in which plant diaspores are dispersed usually al., 2007). Although fruits have zoochorous characteristics, in exchange for nutritional rewards in the form of fleshy which animal species are responsible for this species seed pericarps (Van der Pijl, 1982; Coates-Estrada and Estrada, dispersal remains to be verified. What is the effect of 1988). This type of plant-animal mutualism represents a seeds passage through the digestive tract of dispersers? much more complex relationship than a simple exchange of The present study was designed to answer these questions advantages and is influenced by many factors Howe( and and characterize the fruiting pattern of Cereus jamacaru. Smallwood, 1982), including environmental conditions, Also, we aimed to identify the principal fruit consumers fruiting phenology, and the efficiency of the dispersal agent. and examine their potential as seed dispersers. Dispersal success depends directly on the feeding behavior of the frugivore, fruit processing, and post- 2. Material and Methods feeding movements (Jordano and Schupp, 2000). Seed disperser birds have many distinct characteristics that 2.1. Study area influence their dispersal efficiency, including variations in their behavioral patterns and seed retention times, their The present study was undertaken at a private natural digestive processes, and mode which seeds are subsequently reserve (PNR) at Fazenda Almas (7° 28’ 15” S and 36° 52’ deposited in the environment; all of these factors will 51” W), which has an area of 3.505 hectares and is located influence the reproductive success of plants Herrera( and largely in the municipality of São José dos Cordeiros, with Jordano, 1981; Moermond and Denslow, 1985). a small section in the municipality of Sumé, in Paraiba Studies on frugivory have been carried out in a variety state (PB), Brazil. The reserve is localized in the Cariri Paraibano region, region with the lowest rainfall levels of environments, most of these being humid forests. in the Caatinga zone of PB. Climate of the region is However, the arid and semiarid ecosystems of the world characterized by extreme conditions such as high radiation, have received little attention (Jordano, 1992). Semiarid low relative humidity and cloudiness, and high average ecosystems in the Neotropics have a great variety of columnar annual temperature, varying from 26 to 33 °C (Prado, cacti that produce a large biomass of fleshy fruits that 2003). Annual average precipitation levels are less than produce a large biomass of fleshy fruits with a high sugar 600 mm and quite irregular; regional climate is classified content and water (Sosa, 1991). In the northeast semiarid as ‘warm semiarid’ (Bsh) with summer rains, according to of Brazil, Cactaceae represents a widely distributed family the Köppen system (Köppen, 1948). The PNR is dominated in Caatinga (Taylor and Zappi, 2004), being one of the top by both dense and open arboreal habitats of Caatinga four species-rich plant families in the ecosystem (Rodal vegetation, with other specific open habitats such as rock and Sampaio, 2002). Many species of Cactaceae show outcrops (“lajedos”) with their distinctive floras, and small reproductive activities not directly dependent on rainfall sandy areas (“campestres”) scattered among the arboreal patterns (Petit, 2001), offering resources to pollinators formations (Barbosa et al., 2007). and dispersers independent of the precipitation – being considered key-species that can sustain the frugivorous 2.2. Study species vertebrate community during periods of extreme scarcity Cereus jamacaru DC. ssp. jamacaru (Cactaceae) is a of other food resources (Terborgh, 1986). widely distributed species, both in natural and anthropic Fruits of Cactaceae are generally fleshy with a great areas (Anderson, 2001). This species is a columnar number of seeds embedded in a structure that is denominated cactus locally known as ‘mandacaru’ that belongs to the funicular pulp (Taylor and Zappi, 2004). These fruits tribe Cereeae which comprises approximately 35 species constitute an important resource for different groups of (Anderson, 2001), used as forage, as an ornamental plant, animals, such as birds, insects, reptiles, and mammals, and in popular medicine (Andrade et al., 2006). Cereus that can manipulate and/or ingest seeds and transport them jamacaru plants are treelike plants with distinct trunks of without damages, therefore contributing to its germination up to 60 cm in diameter and many erect branches, forming in sites distant from the mother plant (Silva, 1988; León dense crowns with up to 10 m height. The flowers are de la Luz and Domínguez, 1991; Silvius, 1995; Soriano solitary, nocturnal and white; its pollination syndromes et al., 1999; Ruiz et al., 2000; Godinez-Alvarez et al., apparently involve sphingophily