Nitrogen Xuxes from Treefrogs to Tank Epiphytic Bromeliads: an Isotopic and Physiological Approach
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Oecologia (2010) 162:941–949 DOI 10.1007/s00442-009-1533-4 PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Nitrogen Xuxes from treefrogs to tank epiphytic bromeliads: an isotopic and physiological approach Gustavo Q. Romero · Fausto Nomura · Ana Z. Gonçalves · Natacha Y. N. Dias · Helenice Mercier · Elenice de C. Conforto · Denise de C. Rossa-Feres Received: 7 March 2009 / Accepted: 30 November 2009 / Published online: 19 December 2009 © Springer-Verlag 2009 Abstract Diverse invertebrate and vertebrate species live with frogs had higher stable N isotopic composition (15N) in association with plants of the large Neotropical family values than those without frogs. Similar results were Bromeliaceae. Although previous studies have assumed obtained from a controlled greenhouse experiment. Linear that debris of associated organisms improves plant nutri- mixing models showed that frog feces and dead termites tion, so far little evidence supports this assumption. In this used to simulate insects that eventually fall inside the bro- study we used isotopic (15N) and physiological methods to meliad tank contributed, respectively, 27.7% (§0.07 SE) investigate if the treefrog Scinax hayii, which uses the tank and 49.6% (§0.50 SE) of the total N of V. bituminosa. Net epiphytic bromeliad Vriesea bituminosa as a diurnal shelter, photosynthetic rate was higher in plants that received feces contributes to host plant nutrition. In the Weld, bromeliads and termites than in controls; however, this eVect was only detected in the rainy, but not in the dry season. These results demonstrate for the Wrst time that vertebrates con- tribute to bromeliad nutrition, and that this beneWt is sea- Communicated by Zoe Cardon. sonally restricted. Since amphibian–bromeliad associations G. Q. Romero (&) · E. C. Conforto · D. C. Rossa-Feres occur in diverse habitats in South and Central America, this Departamento de Zoologia e Botânica, IBILCE, mechanism for deriving nutrients may be important in Universidade Estadual Paulista (UNESP), bromeliad systems throughout the Neotropics. Rua Cristóvão Colombo, 2265, São José do Rio Preto 15054-000, SP, Brazil e-mail: [email protected] Keywords Bromeliad-frog interactions · Digestive mutualism · Nutrient provisioning · F. Nomura Tillandsioideae · Scinax hayii Departamento de Ecologia, ICB, Universidade Federal de Goiás (UFG), CP 131, Goiânia 7401-970, GO, Brazil Introduction A. Z. Gonçalves Pós-Graduação em Ecologia, Instituto de Biologia, Nutrient Xuxes across ecological compartments can exert Universidade Estadual de Campinas (UNICAMP), CP 6109, Campinas 13083-970, SP, Brazil profound direct and indirect eVects on the recipient system (Purtauf and Scheu 2005). Although transfer of nutrients N. Y. N. Dias from primary producers to higher trophic levels is well Pós-Graduação em Biologia Animal, established, inverse nutrient Xux, i.e., from animals to Universidade Estadual Paulista (UNESP), Rua Cristóvão Colombo 2265, plants, is a much less recognized process (e.g., Anderson São José do Rio Preto 15054-000, SP, Brazil and Polis 1999). Nutrient Xuxes from animals to plants can occur at multiple scales. For example, on a broad scale, sea H. Mercier bird guano improves the net primary productivity of plants Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Matão, on oceanic islands (Anderson and Polis 1999; Wait et al. 277, São Paulo 05508-900, SP, Brazil 2005), and resource pulses of cicadas (Magicicada spp.) in 123 942 Oecologia (2010) 162:941–949 17-year cycles improve growth and reproduction in temperate plants as diurnal shelters, diVerent degrees of specialization forest plants (Yang 2004). On a smaller scale, several can be noted. For instance, Aparasphenodon brunoi has a studies have reported nutrient Xuxes from ants to myrme- hyperossiWed helmet-like cranium that protects the species cophilous plants (Rico-Gray et al. 1989; Treseder et al. against predators in the bromeliad’s tanks (Teixeira et al. 1995; Sagers et al. 2000; Fischer et al. 2003; Solano and 2002), while Scinax hayii, also common in bromeliads, has Dejean 2004), from mutualistic Pameridea bugs (Miridae) no evident morphological modiWcations (Carvalho-e-Silva to the carnivorous host plant Roridula (Anderson and et al. 2000; F. Nomura, personal observation). Midgley 2002, 2003), and from the jumping spider Psecas In southeastern Brazil, the treefrog Scinax hayii chapoda to its Bromeliaceae host plant, Bromelia balansae (Hylidae) commonly uses the tank epiphytic bromeliad (Romero et al. 2006, 2008). Although diverse invertebrates Vriesea bituminosa (Tillandsioideae) as a diurnal shelter, and vertebrates live associated with plants of the large Neo- thus comprising a suitable system in which to test N Xuxes tropical family Bromeliaceae, little is known about whether and reciprocal beneWts in frog-bromeliad systems. In addi- and how these animals contribute to their host plants’ per- tion, insects that fall into bromeliad tanks might also con- formance. tribute to bromeliad nutrition. In this study we conducted Many species in the family Bromeliaceae typically live Weld observations and surveys, and performed a controlled in low-nutrient environments (rock outcrops, sandy soils, greenhouse experiment during two seasons (dry and wet) to tree canopies), but have their leaves organized in rosettes, address the following questions: an arrangement that forms a tank or phytotelmata, which 1. Does S. hayii contribute to V. bituminosa nutrition allows them to intercept and retain debris and water through its debris (feces)? (Benzing 2000). Minerals and water accumulated in the 2. Does the bromeliad absorb N derived from insects that rosette can be absorbed through specialized trichomes die inside its tanks? (Sakai and Sanford 1980; Benzing et al. 1985). Whereas 3. How much of the bromeliad’s N is derived from tree- plants of the subfamilies Pitcairnioideae and Bromelioi- frog feces and from dead insects? deae seem to be unable to absorb large organic mole- 4. How does N uptake from treefrogs and dead insects cules through their trichomes, plants of the subfamily inXuence the physiology of the bromeliad (e.g., gas Tillandsioideae (e.g., Vriesea) can take up complex exchanges, protein and chlorophyll concentrations)? organic compounds, such as amino acids (Endres and 5. Do these responses vary in diVerent seasons? Mercier 2003; Cambuí and Mercier 2006). Therefore, bromeliads of this subfamily could derive nutrients from predator feces and arthropod carcasses in their tanks Materials and methods (Romero et al. 2006). Many anuran species from South and Central America Study system use bromeliads during their life cycles, although the degree of specialization in the use of this microhabitat varies among Vriesea bituminosa (Tillandsioideae) is a tank epiphytic species (Peixoto 1995; Richardson 1999; Carvalho-e-Silva bromeliad that commonly inhabits trees in Brazilian rain- et al. 2000; Schineider and Teixeira 2001; Teixeira et al. forests, but can also occur in inselberg and cerrado vegeta- 2002; Haddad and Prado 2005). For example, some species tion (Romero 2006; Versieux and Wendt 2007; G. Q. are specialized, spending their entire life cycle in associa- Romero, personal observation). Its rosettes are large and tion with bromeliads, reproducing and feeding among the colorful, and accumulate large amounts of rainwater (range plant axils, and producing tadpoles with morphological and for four small bromeliads: 240–260 ml). Because of these behavioral adaptations [e.g., Syncope antenori (Krungel traits, it is preferred by landscape designers for use in pri- and Richter 1995); Phyllodytes luteolus (Giaretta 1996)]. vate gardens, and is frequently extracted from the wild for Other species use bromeliads during the reproductive this type of commercial use; thus it is an endangered spe- period, as calling or oviposition sites or as microhabitats for cies (Versieux and Wendt 2007). This plant’s rosette can tadpole development [e.g., Physalaemus spiniger (Haddad shelter several animal groups, including spiders, ants and and Pombal 1998); Aplastodiscus sibilatus (Cruz et al. frogs (Romero 2006; G. Q. Romero, personal observation; 2003); Dendrobates pumilio (Young 1979)]. At the other F. Nomura, unpublished data). extreme, some anurans use bromeliads only as diurnal shel- The treefrog Scinax hayii (Hylidae) frequently uses ters [e.g., Eleutherodactylus johnstonei (Ovaska 1991); V. bituminosa as a diurnal shelter. This is a common, Aparasphenodon brunoi (Teixeira et al. 2002); Dendropsophus medium-sized frog (about 43 mm total length) belonging to nahdereri and Scinax perereca (Conte and Rossa-Feres the Scinax ruber clade (Faivovich et al. 2005), which is 2006); and Scinax hayii (F. Nomura, personal observa- endemic to the Atlantic rainforest and occurs from Espírito tion)]. Even in those anuran species that only use bromeliad 123 Oecologia (2010) 162:941–949 943 Santo to Santa Catarina states, southeastern Brazil. This the frogs ate prior to capture, the Wrst feces produced were species lives in primary and secondary lowland and mon- discarded, and the remaining feces were randomly applied tane forests, along forest edges, in secondary vegetation, in the experimental bromeliads (treatment 1 below). Ter- and even inside houses. Usually it occurs on low vegetation mites were also collected, dried, weighed and stored to be near streams and ponds (Carvalho-e-Silva and Carvalho- used in the experiment. The experiment had three treat- e-Silva