Acessibilidade / Reportar erro

The role of Lithodoras dorsalis (Siluriformes: Doradidae) as seed disperser in Eastern Amazon

ABSTRACT

Ichthyochory is an important process responsible for the high diversity of plant species in tropical flooded forests. Thus, this study aimed to investigate the role of a catfish species, Lithodoras dorsalis, as seed disperser in the flooded forests at the Amazon River mouth, Brazil. Analyzing the stomach contents of 371 individuals of Lithodoras dorsalis, the Germination Potential (GP%) and Germination Speed Index (GSI) of seeds that were removed intact were investigated. This allowed us to evaluate the germination performance of two important species of plants in Amazonia, Euterpe oleracea (Açaí) and Montrichardia linifera (Aninga), after passage through the digestive tract of this catfish species. Given that digestion by L. dorsalis reduced the germination viability of M. linifera and that seeds were often destroyed during consumption, we suggest that L. dorsalis may have a limited role as seed disperser of M. linifera and instead mostly act as seed predator. However, for the species E. oleracea, L. dorsalis was a potential disperser, since the performance of germination of these seeds was improved after digestion. In addition, the number of seeds consumed was directly proportional to the catfish’s body size, reinforcing the role of doradids as potential seed dispersers in tropical forests.

Keywords:
Catfish; Euterpe oleracea; Germination Performance; Montrichardia linifera; Seed dispersal

RESUMO

A ictiocoria é um importante processo responsável pela alta diversidade de espécies vegetais nas florestas tropicais alagadas. Dessa forma, este trabalho teve como objetivo investigar o papel de Lithodoras dorsalis como dispersor de sementes na Foz Amazônica, Brasil. Analisando o conteúdo estomacal de 371 espécimes de Lithodoras dorsalis, o Potencial de Germinação (PG%) e o Índice de Velocidade de Germinação (IGS) de sementes removidas intactas foram investigados. Isto permitiu-nos avaliar o desempenho germinativo de duas importantes espécies de plantas na Amazônia, Euterpe oleracea (Açaí) e Montrichardia linifera (Aninga), após passagem pelo trato digestivo desta espécie de bagre. Dado que a digestão por L. dorsalis reduziu a viabilidade de germinação de M. linifera e que as sementes foram frequentemente destruídas durante o consumo, sugerimos que L. dorsalis tem um papel limitado como dispersor de sementes de M. linifera e, em vez disso, age como predador de sementes. No entanto, para a espécie E. oleracea, L. dorsalis foi um potencial dispersor, uma vez que o desempenho germinativo das sementes foi melhorado após a digestão. Além disso, o número de sementes consumidas foi diretamente proporcional ao tamanho corporal do bagre, reforçando o papel de doradídeos como potenciais dispersores de sementes em florestas tropicais.

Palavras-chave:
Bagre; Desempenho de Germinação; Dispersão de sementes; Euterpe oleracea; Montrichardia linifera

Introduction

Seed dispersal is crucial for the maintenance of plant species, establishing patterns and limits that are critical for the population dynamics of angiosperms (Horn et al., 2011Horn MH, Correa SB, Parolin P, Pollux BJA, Anderson JT, Lucas C, Widmann P, Tjiu A, Galetti M, Goulding M. Seed dispersal by fishes in tropical and temperate fresh waters: The growing evidence. Acta Oecol. 2011; 37(6):561-77.; Beckman, Rogers, 2013Beckman NG, Rogers HS. Consequences of seed dispersal for plant recruitment in tropical forests: Interactions within the seedscape. Biotropica. 2013; 45(6):666-81.). The dispersal process has consequences for spatial distribution, gene flow, population genetics, intra and inter specific interactions and evolution (Seidler, Plotkin, 2006Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.; Wall, Beck, 2011Wall SBV, Beck MJ. A Comparison of frugivory and scatter-hoarding seed-dispersal syndromes. Bot Rev. 2011; 78(1):10-31.; Vargas, Stevenson, 2013Vargas IN, Stevenson PR. Seed and establishment limitation: Effects on plant diversity in an Amazonian rain forest. Biotropica . 2013; 45(6):737-46.). Several plant species have seeds adapted for dispersal by animals (zoochory) (Fenner, 1985Fenner M. Seed ecology. London: Chapman and Hall; 1985.; Margalef, 1991Margalef R. Ecologia. Barcelona: Omega; 1991.; Beckman, Rogers, 2013Beckman NG, Rogers HS. Consequences of seed dispersal for plant recruitment in tropical forests: Interactions within the seedscape. Biotropica. 2013; 45(6):666-81.). Generally, these plants have attractive and nutritious fruits with seeds that can survive the passage through the digestive tract of dispersers (Fenner, 1985Fenner M. Seed ecology. London: Chapman and Hall; 1985.; Margalef, 1991Margalef R. Ecologia. Barcelona: Omega; 1991.).

The animal efficiency on plant dispersal depends on the amount of dispersed seeds (number of visits to the plant and number of dispersed seeds per visit) and dispersal quality (seed treatment in the animal’s stomach and the site of deposition of the seed) (Herrera, Jordano, 1981Herrera CM, Jordano P. Prunus mahaleb and birds: the high-efficiency seed dispersal system of a temperate fruiting tree. Ecol Monogr. 1981; 51(2):203-18.; Schupp, 1993Schupp EW. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio. 1993; 107/108:15-29.; Schupp et al., 2010Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.). Seed dispersal is a mutualism and foraging by frugivores directly influences the spatial distribution of plants in the environment (Fenner, 2000Fenner M. Seeds - The Ecology of Regeneration in Plant Communities. 2nd ed. Wallingford: CABI Publishing; 2000.; Silvertown, Antonovics, 2001Silvertown J, Antonovics J. Integrating Ecology and Evolution in a Spatial Context. London: Blackwell Science Ltd; 2001.). Thus, plant seed dispersal mechanisms are probably the result of natural selection that increases the chances of spreading their seeds (Fenner, 1985Fenner M. Seed ecology. London: Chapman and Hall; 1985.; Ferreira et al., 2010Ferreira CS, Piedade MTF, Wittmann AO, Franco AC. Plant reproduction in the Central Amazonian floodplains: challenges and adaptations. AoB Plants. 2010; 2010:plq009. Available from: http://dx.doi.org/10.1093/aobpla/plq009
http://dx.doi.org/10.1093/aobpla/plq009...
).

Until a few years ago, fishes had little relevance in studies about frugivory and dispersion, being this process classically linked to birds and mammals (Correa et al., 2007Correa SB, Winemiller KO, López-Fernandez H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. BioScience. 2007; 57(9):748-56.; Correa et al., 2015bCorrea SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
http://dx.doi.org/10.1111/brv.12153...
). However, fishes were probably the first vertebrate dispersers, playing an important role on the dispersal of the first angiosperms, approximately 70 million years ago in South America (Correa et al., 2015aCorrea SB, Araujo JK, Penha JMF, Cunha CN, Stevenson PR, Anderson JT. Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biol Conserv. 2015a; 191:159-67.). In tropical ecosystems, ichthyochory contributes to the maintenance of high diversity of plant species in flooded forests and wetlands (Gottsberger, 1978Gottsberger G. Seed dispersal by fish in the inundated regions of Humaitá, Amazonia. Biotropica . 1978; 10(3):170-83.; Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Horn, 1997Horn MH. Evidence for dispersal of fig seeds by the fruit-eating characid fish Brycon guatemalensis Regan in a Costa Rican tropical rain forest. Oecologia . 1997; 109:259-64.; Pilati et al., 1999Pilati R, Andrian IF, Carneiro JWP. Desempenho germinativo de sementes de Cecropia pachystachya trec. (Cecropiaceae), recuperadas do trato digestório de Doradidae, Pterodoras granulosus (Valenciennes, 1883), da planície de inundação do Alto Paraná. Interciencia. 1999; 24:47-55.; Correa et al., 2007Correa SB, Winemiller KO, López-Fernandez H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. BioScience. 2007; 57(9):748-56.; Anderson et al., 2009Anderson JT, Saldaña-Rojas J, Flecker AS. High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia. 2009; 161(2):279-90.). Many plant species in these habitats fruit during the flood season and they are adaptated to hydrochory or ichthyochory (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Correa, Winemiller, 2014Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fuctuating resources in the Amazonian foodplain forest. Ecology. 2014; 95(1):210-24.; Correa et al., 2015bCorrea SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
http://dx.doi.org/10.1111/brv.12153...
). Thus, in such environments, understanding the relationship between the fish fauna and riparian forests can serve as a basis to understand the ecological role played by fishes (Godinho, Godinho, 2003Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUCMinas; 2003.).

There are approximately 150 species of frugivore fishes in South America, which during the flood period enter the floodplain and feed on fruits and seeds dispersing at least 566 plant species (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Junk et al., 1997Junk WJ, Soares M, Saint-Paul U. The Fish. In: Junk WJ, editor. The central Amazon Floodplain: ecology of a pulsing system. Berlin: Springer; 1997. p 385-408.; Maia, Chalco, 2002Maia LA, Chalco FP. Produção de frutos de espécies da floresta de várzea da Amazônia Central importantes na alimentação de peixes. Acta Amazon. 2002; 32(1):45-53.; Correa et al., 2015aCorrea SB, Araujo JK, Penha JMF, Cunha CN, Stevenson PR, Anderson JT. Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biol Conserv. 2015a; 191:159-67.). They represent more than 60% of all frugivorous fishes in the world (Horn et al., 2011Horn MH, Correa SB, Parolin P, Pollux BJA, Anderson JT, Lucas C, Widmann P, Tjiu A, Galetti M, Goulding M. Seed dispersal by fishes in tropical and temperate fresh waters: The growing evidence. Acta Oecol. 2011; 37(6):561-77.). These fishes have some adaptations that facilitate their activity as frugivores and seed dispersers, such molar like-teeth, long intestines and enzymes associated with carbohydrates digestion (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Drewe et al., 2004Drewe KE, Horn MH, Dickson KA, Gawlicka A. Insectivore to frugivore: ontogenetic changes in gut morphology and digestive enzyme activity in the characid fish Brycon guatemalensis from Costa Rican rain forest streams. J Fish Biol. 2004; 64(4):890-902.; Correa et al., 2007Correa SB, Winemiller KO, López-Fernandez H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. BioScience. 2007; 57(9):748-56., 2015bCorrea SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
http://dx.doi.org/10.1111/brv.12153...
). In addition to the adaptations cited above, some studies showed that ichthyochory effectiveness increases with the size of the fish, because of the high consumption of fruits, including the big ones, their extensive movement patterns and the long seed-retention time of large individuals (Galetti et al., 2008Galetti M, Donatti CI, Pizo MA, Giacomini HC. Big fish are the best: seed dispersal of Bactris glaucescens by the pacu fish (Piaractus mesopotamicus) in the Pantanal, Brazil. Biotropica . 2008; 40(3):386-89.; Anderson et al., 2011Anderson JT, Nuttle T, Saldaña-Rojas JS, Pendergast TH, Flecker AS. Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc R Soc B. 2011; 278:3329-35.; Correa et al., 2015aCorrea SB, Araujo JK, Penha JMF, Cunha CN, Stevenson PR, Anderson JT. Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biol Conserv. 2015a; 191:159-67.).

The rock-bacu Lithodoras dorsalis (Valenciennes, 1840) is one of the largest thorny catfish (Siluriformes, Doradidae), reaching at least 90 cm of standard length and 12 kg in weight (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.). This species is exploited by commercial and local fisheries in the Amazon mouth and occurs in northern South America in the Amazon estuary and neighboring coastal areas of French Guiana (Sabaj, Ferraris, 2003Sabaj MH, Ferraris CJ, Jr. Family Doradidae (Thorny Catfishes). In: Reis RE, Kullander SO, Ferraris CJ, Jr, editors. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003. p 456-69.). Lithodoras dorsalis eat fruits and seeds and possible play a role as seed disperser (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Kubitzki, Ziburski, 1994Kubitzki K, Ziburski A. Seed dispersal in flood plain forests of Amazonia. Biotropica . 1994; 26(1):30-43.; Barbosa et al., 2015Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48.). There are few studies focusing on seed dispersal by catfishes when compared to other frugivorous fish groups such as characids (Brycon spp.) and serrasalmids (Colossoma macropomum, Mylossoma duriventre and Piaractus spp.) (Horn, 1997Horn MH. Evidence for dispersal of fig seeds by the fruit-eating characid fish Brycon guatemalensis Regan in a Costa Rican tropical rain forest. Oecologia . 1997; 109:259-64.; Galetti et al., 2008Galetti M, Donatti CI, Pizo MA, Giacomini HC. Big fish are the best: seed dispersal of Bactris glaucescens by the pacu fish (Piaractus mesopotamicus) in the Pantanal, Brazil. Biotropica . 2008; 40(3):386-89.; Anderson et al., 2009Anderson JT, Saldaña-Rojas J, Flecker AS. High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia. 2009; 161(2):279-90.; Anderson et al., 2011Anderson JT, Nuttle T, Saldaña-Rojas JS, Pendergast TH, Flecker AS. Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc R Soc B. 2011; 278:3329-35.; Correa et al., 2015aCorrea SB, Araujo JK, Penha JMF, Cunha CN, Stevenson PR, Anderson JT. Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biol Conserv. 2015a; 191:159-67.). Few studies showed that seeds consumed by catfishes remain viable and/or had increased germination performance after passage through the digestive tract (Kubitzki, Ziburski, 1994Kubitzki K, Ziburski A. Seed dispersal in flood plain forests of Amazonia. Biotropica . 1994; 26(1):30-43.; Stevaux et al., 1994Stevaux MCS, Negrelle RRB, Zanette VC. Seed dispersal by the fish Pterodoras granulosus in the Paraná River basin, Brazil. J Trop Ecol. 1994; 10:621-26.; Pilati et al., 1999Pilati R, Andrian IF, Carneiro JWP. Desempenho germinativo de sementes de Cecropia pachystachya trec. (Cecropiaceae), recuperadas do trato digestório de Doradidae, Pterodoras granulosus (Valenciennes, 1883), da planície de inundação do Alto Paraná. Interciencia. 1999; 24:47-55.). The paucity of seed dispersal studies focusing on catfishes is due to the difficulty of capturing a large number of specimens to draw solid conclusions.

Due to the importance of doradids in seed dispersal and the high consumption of fruits by rock-bacu, the aim of this study was to answer the following questions: (i) What is the frequency and the proportion of fruits relative to other food items consumed by L. dorsalis? As shown for Barbosa et al. (2015Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48.), we expect L. dorsalis’ diet to consist mainly of fruits; (ii) What is the relationship between the size of individuals and fruit consumption? We expect that with increasing length there is an increase in the amount of consumed fruits, positively affecting the potential seed dispersal activity; (iii) Are the seeds consumed by rock-bacu destroyed during digestion? If L. dorsalis is a disperser, we expect that the seeds are not destroyed during digestion; (iv) What is the effect of digestion on the germination rate of intact seeds consumed by L. dorsalis? Considering the possibility that the species is a disperser, we expect an increase in germination performance of intact seeds.

Material and Methods

The role of Lithodoras dorsalis as a potential seed disperser was investigated using two abundant plant species in the Amazon estuary floodplain, listed below:

Euterpe oleracea (Mart.).Euterpe oleracea Mart. is a palm of the Arecaceae family, which can reach up to 25 m tall. Known popularly as “açaí”, it is native to the Brazilian Amazon and occurs in the states of Pará, Amazonas, Maranhão and Amapá in areas with flooded soils and floodplains (“várzea” and “igapó”) (Lorenzi et al., 1996Lorenzi H, Souza HM, Costa JTM, Cerqueira LSC, Behr N. Palmeiras do Brasil: nativas e exóticas. Nova Odessa (SP): Editora Plantarum; 1996.). The species has glabrous fruits (without hairs, trichomes or similar structures on the outer surface), globular and smooth surface, reaching up in average 2.14 g, 15.1 mm of diameter and 13.2 mm of length (Paula, 1975Paula JE. Anatomia de Euterpe oleracea Mart. (Palmae da Amazônia). Acta Amazon . 1975; 5(3):265-78.; Almeida et al., 2011Almeida EIB, Costa LC, Carneiro GG, Ribeiro WS, Barbosa JA. Análise biométrica e físico-química de frutos de açaizeiros cultivados no Brejo paraibano. Tecnol & Ciên Agropec. 2011; 5(2):1-4.). The pericarp is purple and its pulp has a high calorific value (247 kcal in 100 g of dry fruit), measuring around 1 mm (Lorenzi et al., 2006Lorenzi H, Bacher L, Lacerda M, Sartori S. Frutas brasileiras e exóticas cultivadas: de consumo in natura. Nova Odessa (SP): Instituto Plantarum de Estudos da Flora; 2006.). Due to these characteristics, the acai berry is part of the diet of Amazon human populations (Paula, 1975Paula JE. Anatomia de Euterpe oleracea Mart. (Palmae da Amazônia). Acta Amazon . 1975; 5(3):265-78.; Brondízio et al., 2003Brondízio ES, Safar CAM, Siqueira AD. The urban market of açaí fruit (Euterpe oleracea Mart.) and rural land use change: Ethnographic insights into the role of price and land tenure constraining agricultural choices in the Amazon estuary. Urban Ecosyst. 2003; 6(1/2):67-97.).

Montrichardia linifera(Arruda) Schott.Montrichardia linifera (Arruda) Schott, popularly known as “aninga”, is an amphibious herbaceous from Araceae family, reaching 4-6 m in height. This species can occur in several types of habitat, being found onshore or in water-saturated soils (Amarante et al., 2011Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.). This macrophyte is distributed in the tropics (Mayo et al., 1997Mayo SJ, Bogner J, Boyce PC. The Genera of Araceae. United Kingdom: Royal Botanic Gardens; 1997.) and has considerable importance in the formation of riverbanks and white water streams, forming extensive clonal populations by sprouting from underground and submerged stems (Amarante et al., 2011Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.). Seed length ranges from 33-51 mm (mean 39.53 mm) and width ranges from 23-33 mm (mean: 28.81 mm), weighing around 1.5 to 6.0 g (Amarante et al., 2011Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.). M. linifera serves as food for fish, reptiles and aquatic mammals, due to the high caloric value of their fruits (355.12 kcal during the rainy season and 346.4 in the dry season) (Amarante et al., 2011Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.). The aninga also has economic value for Amazon populations, since its floating stem can be used to build rafts for timber transport through rivers (Lins, Oliveira, 1994Lins ALFA, Oliveira PL. Origem, aspectos morfológicos e anatômicos das raízes embrionárias de Montrichardia linifera (Arruda) Schott (Araceae). Bol Mus Para Emílio Goeldi Ser Bot. 1994; 10(2):221-236.; Amarante et al., 2011Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.).

Study area. Fishing was conducted in the municipality of Abaetetuba, in the confluence of the Tocantins River and Pará River, in Pará State, Brazil (1°41’13,6”S; 48°52’48,8”W) (Fig. 1). The region’s hydrological regime is characteristic of tropical tidal rivers with a daily, rapid and broad flood (reaching up to 4m) which also causes a reversal in the direction of the current (Welcomme, 1979Welcomme RL. Fisheries Ecology of floodplain rivers. London: Longman Group Limited; 1979.; Barthem, Schwassmann, 1994Barthem RB, Schwassmann HO. Amazon river influence on the seasonal displacement of the salt wedge in the Tocantins river estuary, Brazil, 1983-1985. Bol Mus Para Emilio Goeldi Ser Zool. 1994; 10(1):19-130.; Hida et al., 1999Hida N, Maia JG, Hiraoka M, Shimm O, Nobuaki M. River water level changes of the Amazon Estuary: at Breves, Caxiuanã and Abaetetuba. Manaus’99 - Hydrological and Geochemical Processess in Large Scale River Basins. 1999; p.1-9.).

Fig. 1
Location of the study area near the mouth of the Amazon River in Brazil. a. Location of Brazil in South America; b. Amazon River mouth with the sampling site; c. Study area (specimens were collected within the shaded area).

The region’s vegetation is defined as tidal floodplain vegetation with ombrophilous, broadleaved species, merged with palm trees like buriti tree (Mauritia flexuosa) and açaí berry tree (E. oleracea). The fruiting period of E. oleracea is from July to November (Guimarães et al., 2004Guimarães LA, Santos TM, Rodrigues MD, Frahan BH. Produção e comercialização do açaí do município de Abaetetuba, Pará. In: Jardim MAG, Mourão L, Groissman M, editores. Açaí (Euterpe oleracea Mart.): possibilidades e limites para o desenvolvimento sustentável no estuário amazônico. Belém: Museu Paraense Emílio Goeldi; 2004. p. 159-79.), while M. flexuosa fruits from March to August (Sampaio, Carrazza, 2012Sampaio MB, Carrazza LR. Manual tecnológico de aproveitamento integral do fruto e da folha do buriti (Mauritia flexuosa). Brasília: Instituto Sociedade, População e Natureza (ISPN); 2012.) and M. linifera fructifies all year round.

The local climate is classified as Af following the Köppen-Geiger classification, corresponding to the typical conditions of tropical rainforest ecosystems (Peel et al., 2007Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci. 2007; 11(5):1633-44.). Annual precipitation is approximately 2500 mm, but during the period of our study the pluviosity was 3044 mm (mean = 253.7 ± 196.2) (Agência Nacional de Águas (ANA), 2016Agência Nacional de Águas (ANA). Hidroweb: sistema de informações hidrológicas. 2016 [Date of access - 11 October 2016]. Available from: Available from: http://hidroweb.ana.gov.br/HidroWeb
http://hidroweb.ana.gov.br/HidroWeb...
). The rainy season lasts from January to May (precipitation mean = 463.38 ± 87.42), and the dry season from June to December (precipitation mean = 103.87 ± 51.33) (Machado, 2008Machado J. O Município de Abaetetuba: Geografia Física e Dados Estatísticos. Abaetetuba: Edições Alquimia; 2008.; ANA, 2016Agência Nacional de Águas (ANA). Hidroweb: sistema de informações hidrológicas. 2016 [Date of access - 11 October 2016]. Available from: Available from: http://hidroweb.ana.gov.br/HidroWeb
http://hidroweb.ana.gov.br/HidroWeb...
). Mean temperature is 27°C, ranging from 20°C to 35°C over the course of the year. Relative humidity is high, around 85%, varying normally between 81% and 90% (Machado, 2008Machado J. O Município de Abaetetuba: Geografia Física e Dados Estatísticos. Abaetetuba: Edições Alquimia; 2008.).

Data sampling.Lithodoras dorsalis were sampled monthly over a full annual cycle, between July 2010 and June 2011. Specimens were collected in the main river channels and in the streams of Sirituba Island in Abaetetuba, Pará, Brazil (Fig. 1).

Weir fishing nets of aproximately 10 m in lenght, 3 m in height and a between-knots mesh size of 3-6 cm, were used to capture specimens. Nets were set at dusk (17:00-19:00) (Fig. 2a), depending on the tide, and removed at dawn (05:00-07:00). This period was adopted to ensure the capture of individuals moving from the smaller rivers to the main channel during the low tide (Fig. 2b). Specimens were removed from the water using seine nets (5 m x 1 m) and hand- or dip-nets (Figs 2c-d).

Fig. 2
Sampling method applied to capture Lithodoras dorsalis at the Amazon River mouth, Brazil, from July 2010 to June 2011. a. Net set at the bottom during the dusk and with low tide to allow the fish entrance in small rivers; b. Net lifted during the next morning (approximately, 12 hours after setting at the bottom), blocking the exit of fishes that came during the night; c and d. Fish sample using seine nets and hand- or dip-nets.

All captured specimens were analised in the laboratory at the Federal Institute of Pará (Instituto Federal do Pará - IFPA), where they were sacrificed with a lethal dose of anaesthetic. Then, a ventral-longitudinal incision was made from the urogenital opening to the head for the removal of the stomach, which was weighted (g) and emptied for the collection of its contents. The contents were weighed separately (g) and then sorted in a Petri dish. After the removal of the stomach, intact seeds were washed in running water and storaged in paper bags containing a substrate of vermiculite (MgFeAl)3(AlSi)4O10(OH)24H2O (Oliveira et al., 1996Oliveira EC, Piña-Rodrigues FCM, Figliolia MB. Propostas para a padronização de metodologias em análise de sementes florestais. Rev Bras Sementes. 1996; 11(1-3):1-42.).

Only E. oleracea and M. linifera reached sufficient number of seeds for analysis of germination. We analized 270 intact seeds of E. oleracea and 60 intact seeds of M. linifera. The lower number of analyzed seeds for M. linifera is because many of them were found destroyed. Only intact seeds of E. oleracea were found among digestive contents.

Following evisceration, the specimens were fixed in 10% formaldehyde, conserved in 70% alcohol, and then incorporated to the ichthyological collection of the Goeldi Museum (Museu Paraense Emílio Goeldi - MCT/MPEG), under the following catalog numbers: MPEG 19134; MPEG 19202; MPEG 19203; MPEG 19610; MPEG 19611; MPEG 21668-MPEG 21681.

Germination experiments.Euterpe oleracea seeds were planted in containers containing nutrient-rich soil to a depth of 2 cm, with germinative aperture facing up (Silva et al., 2007Silva BMS, Môro FV, Sader R, Kobori NN. Influência da posição e da profundidade de semeadura na emergência de plântulas de açaí (Euterpe oleracea Mart. - Arecaceae). Rev Bras Frutic . 2007; 29(1):187-90.; Gama et al., 2010Gama JSN, Monte DMO, Alves EU, Bruno RLA, Braga Júnior JM. Temperaturas e substratos para germinação e vigor de sementes de Euterpe oleracea Mart. Rev Ciênc Agron. 2010; 41(4):664-70.). M. linifera seeds were planted in moistened vermiculite to a depth of 1 cm, also with germinative aperture facing up.

We tested the germination of E. oleracea under three treatments: Treatment A - seeds from the stomach of specimens of L. dorsalis; Treatment B - seeds from the forest with epicarp and mesocarp removed manually and; Treatment C (Control) - seeds from the forest with epicarp and mesocarp intact (Samuels, Levey, 2005Samuels IA, Levey DJ. Effects of gut passage on seed germination: Do experiments answer the questions they ask? Funct Ecol. 2005; 19(2):365-68.). For each treatment, 90 seeds were used. To M. linifera, only two germination treatments were tested: Treatment A - seeds from L. dorsalis’ stomach; Treatment C (Control) - seeds from the forest, since these seeds have no external structures (like epicarp and mesocarp) to prevent germination. For this species, 30 seeds were used in each treatment.

In all treatments, seeds were considered germinated after the appearance of the radicle. The experiment was considered to be over when no futher germination occurred for seven consecutive days (Labouriau, 1983Labouriau LG. A germinação das sementes. Washington: OEA; 1983.; Maia et al., 2007Maia LMA, Santos LM, Parolin P. Germinação de sementes de Bothriospora corymbosa (Rubiaceae) recuperadas do trato digestório de Triportheus angulatus (sardinha) no Lago Camaleão, Amazônia Central. Acta Amazon . 2007; 37(3):321-26.; Ministério da Agricultura, Pecuária e Abastecimento, 2009Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. 2009 [Date of access - 20 October 2016]. Available from: Available from: http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/arquivos-publicacoes-insumos/2946_regras_analise_sementes.pdf/view
http://www.agricultura.gov.br/assuntos/i...
). In our study, the experiment lasted 42 days for E. oleracea and 29 for M. linifera.

Statistical analyses. The Frequency of Occurrence (FOi%) was calculated for all the fruits and seeds found in L. dorsalis’ stomachs. The aim was to define which plant species would be used in the germination test. The Frequency of Occurrence (FOi%) was calculated by the following formula (Hyslop, 1980Hyslop EJ. Stomach contents analysis - a review of methods and their application. J Fish Biol . 1980; 17(4):411-29.): FOi% = (Ni / Nsto) * 100, where: FOi% = frequency of occurrence of the item i; Ni = number of stomachs where the item i was present; Nsto = total number of stomachs analyzed.

To test the influence of the catfish’s size in the intensity of consumption of fruits and seeds, a Simple Linear Regression was used relating the weight of fruits and seeds in the stomach with the body size of the specimens collected.

The Alimentary Index (AIi%) (modified from Kawakami, Vazzoler, 1980Kawakami E, Vazzoler G. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Oceanogr. 1980. 29(2):205-07.) of fruit and seeds consumed by individuals with different body sizes was calculated. The goal was to investigate if the importance of fruit and seeds changes as the catfish’s body size increases. This index was calculated by AIi% = (FOi% * W% / ∑ FOi% * W%) * 100, where: AIi% represents the food item i alimentary index, FOi% the item i frequency of ocurrence and W% the relative weight of item i. Empty stomachs were not accounted for the analysis.

The Germination Potential (GP%) for E. oleracea and M. linifera was calculated to assess the effect of digestion in seeds consumed by L. dorsalis (viability or not). The calculation was based on the formula proposed by Labouriau, Valadares (1976Labouriau LG, Valadares MB. On the germination of seeds of Calotropis procera. An Acad Bras Cien. 1976; 48:174-86.): GP% = (GS / SA) * 100, where: GS is the number of germinated seeds and SA is the total number of seeds in the sample. The comparison of germination potential between treatments was performed using the chi-square (χ2) test with 5% significance. Before the test, we checked chi-square assumptions and in cases that they did not fulfill, we did a description of the Germination Potential.

The Germination Speed Index (GSI) was performed to test the effect of the passage through the digestive tract of catfishes on the seeds’ germination rate. This index was determined by registering the germination frequencies at intervals of 24 hours and it was calculated by the formula adapted from Maguire (1962Maguire JD. Speed of germination - Aid in selection and evaluation for seedling emergence and vigor. Crop Sci. 1962; 2(2):176-77.): GSI = Σ (Gi%/ Ni), where: GSI is the sum of the ratio between the percentage of germinated seeds at time i (Gi%) within given time i (Ni).

Results

During the 12 months of the study period, 371 specimens of L. dorsalis were captured, of which 268 (74.93%) presented some plant species (fruits or seeds) in their stomachs. Fruits and seeds (intact and masticated) of seven different plant species were recorded and E. oleracea, M. flexuosa and M. linifera were the most common (Tab. 1).

Tab. 1
Frequency of Occurrence (FOi%) of fruits and seeds (intact and masticated) recorded in the diet of Lithodoras dorsalis at the Amazon River mouth, Brazil, from July 2010 to June 2011. Marked species (*) indicate that intact seeds were sampled.

Linear regression analysis showed that L. dorsalis have a potencial role in seed dispersal. There was a positive relationship between L. dorsalis’ body size and the total amount of fruits and seeds consumed by the specimens (R2 = 0.35; p < 0.001) (Fig. 3).

Fig. 3
Relationship between body size (cm) and the general consumption of fruits and seeds (g) by Lithodoras dorsalis at the Amazon River mouth, Brazil, from July 2010 to June 2011.

Euterpe oleracea, pulp and seeds (mainly intact), seems to be more important in the diet of L. dorsalis’ for individuals with intermediate size between 13.6 and 24.7 cm (Tab. 2). M. flexuosa, mainly pulp remains, was more important for smaller catfishes (<13.6 cm SL). M. linifera, pulp and seeds (mainly mastigated), was more consumed by large individuals (> 24.7 cm SL).

Tab. 2
Alimentary Index (AIi%) of the main plant species consumed by Lithodoras dorsalis in each length class at the Amazon River mouth, Brazil, from July 2010 to June 2011.

Only Euterpe oleracea fulfilled all assumptions of chi-square. For this species, the effect of digestion by L. dorsalis was similar between Treatment A (seeds from the stomach of specimens of L. dorsalis) and Treatment B (manual removal of epicarp and mesocarp) (χ2 = 1.966; df = 1; p = 0.160). However, none of the seeds that had not passed through the digestive tract and which epicarp and mesocarp were still attached to the seed (treatment C) germinated (Tab. 3).

Tab. 3
Germination Potential (GP%) of Euterpe oleracea’s and Montrichardia linifera’s intact seeds sampled at the Amazon River mouth, Brazil, from July 2010 to June 2011. Treatment A - seeds from the stomach of specimens of Lithodoras dorsalis; Treatment B - seeds from the forest with epicarp and mesocarp removed manually; Treatment C (Control) - seeds from the forest with epicarp and mesocarp intact.

For Montrichardia linifera, the Germination Potential of seeds from forest plants was numerically diferent from that of seeds taken from the stomachs of L. dorsalis.

The seeds of E. oleracea from L. dorsalis’ stomachs (Treatment A) germinated on the 15th day (± 0.577), two days before seeds from the forest, with epicarp and mesocarp removed manually (Treatment B), which germinated on the 17th day (± 0.707).

The Euperpe oleracea’s Germination Speed Index was higher for seeds from the stomach of L. dorsalis, which amounted to 50% of germination on the 21th day and 100% of germination on the 30th day. However, for Treatment B, only 10% of the seeds germinated until day 21 (Fig. 4).

Fig. 4
Germination Speed Index (GSI) of Euterpe oleracea’s intact seeds from Lithodoras dorsalis’ stomachs (Treatment A); from the forest, with epicarp and mesocarp removed manually (Treatment B); and originating from the forest with epicarp and mesocarp intact (Treatment C) at the Amazon River mouth, Brazil, from July 2010 to June 2011.

The patterns of Germination Speed Index for M. linifera were similar to those of E. oleracea. The seeds removed from the fish’s stomachs (Treatment A) germinated one day before seeds from Treatment C. Although only 33.3% of M. linifera’s seeds in Treatment A germinated, all of these germinated by 19th day while 78% of seeds from Treatment C germinated in 22 days (Fig. 5).

Fig. 5
Germination Speed Index (GSI) of Montrichardia linifera’s intact seeds from Lithodoras dorsalis’ stomachs (Treatment A); and from the forest (Treatment C - Control) at the Amazon River mouth, Brazil, from July 2010 to June 2011.

Discussion

Lithodoras dorsalis, as well as other species of the Doradidae family, is essentially frugivorous (Ringuelet et al., 1967Ringuelet RA, Arámburu RH, Arámburu AA. Los Peces Argentos de Agua Dulce. La Plata: Comisión de Investigaciones Científicas de la provincia de Buenos Aires; 1967.; Stevaux et al., 1994Stevaux MCS, Negrelle RRB, Zanette VC. Seed dispersal by the fish Pterodoras granulosus in the Paraná River basin, Brazil. J Trop Ecol. 1994; 10:621-26.; Santos et al., 2004Santos GM, Mérona B, Juras AA, Jégu M. Peixes do baixo rio Tocantins: 20 anos depois da Usina Hidrelétrica Tucuruí. Brasília: ELETRONORTE; 2004.; Santos et al., 2006Santos GM, Ferreira EJG, Zuanon JAS. Peixes comerciais de Manaus. Manaus: Próvarzea; 2006.; Barbosa et al., 2015Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48.). In the Amazon mouth, E. oleracea, M. linifera and M. flexuosa were the most consumed fruit species and contributed the highest proportional weight to L. dorsalis diet. The presence of intact seeds of three plant species in fish digestive tract can be a positive indicator that this animal is a potential disperser (Gottsberger, 1978Gottsberger G. Seed dispersal by fish in the inundated regions of Humaitá, Amazonia. Biotropica . 1978; 10(3):170-83.). In general, consumption by frugivores could increase germination success via scarification (Stevaux et al., 1994Stevaux MCS, Negrelle RRB, Zanette VC. Seed dispersal by the fish Pterodoras granulosus in the Paraná River basin, Brazil. J Trop Ecol. 1994; 10:621-26.; Pilati et al., 1999Pilati R, Andrian IF, Carneiro JWP. Desempenho germinativo de sementes de Cecropia pachystachya trec. (Cecropiaceae), recuperadas do trato digestório de Doradidae, Pterodoras granulosus (Valenciennes, 1883), da planície de inundação do Alto Paraná. Interciencia. 1999; 24:47-55.). In Neotropical regions, some studies have shown that the passage of seeds through the digestive tract of fish increased germination success between 33% and 100% (Pollux, 2011Pollux BJA. The experimental study of seed dispersal by fish (ichthyochory). Freshw Biol. 2011; 56:197-212.).

Besides increasing germination performance, disperser’s body zise, regardless of the species, can also influence the seed dispersal effectiveness (Schupp et al., 2010Schupp EW, Jordano P, Gómez JM. Seed dispersal effectiveness revisited: A conceptual review. New Phytol. 2010; 188(2):333-53.; Wotton, Kelly, 2012Wotton DM, Kelly D. Do larger frugivores move seeds further?: Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. J Biogeogr [serial on internet]. 2012; 39(11):1973-83. Available from: http://dx.doi.org/10.1111/jbi.12000
http://dx.doi.org/10.1111/jbi.12000...
; Correa et al., 2015bCorrea SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
http://dx.doi.org/10.1111/brv.12153...
; Li et al., 2016Li N, Li X, An S, Lu C. Impact of multiple bird partners on the seed dispersal effectiveness of China’s relic trees. Sci Rep [serial on internet]. 2016; 6:17489. Available from: http://dx.doi.org/10.1038/srep17489
http://dx.doi.org/10.1038/srep17489...
). Individuals of different sizes can generally differ in their diets due to morphological limitations during periods of development (Abelha et al., 2001Abelha MCF, Agostinho AA, Goulart E. Plasticidade trófica em peixes de água doce. Acta Sci. 2001; 23(2):425-34.; Dala Corte et al., 2016Dala Corte RB, Silva ER, Fialho CB. Diet-morphology relationship in the stream-dwelling characid Deuterodon stigmaturus (Gomes, 1947) (Characiformes: Characidae) is partially conditioned by ontogenetic development. Neotrop Ichthyol . 2016; 14(2):e150178. Available from: http://dx.doi.org/10.1590/1982-0224-20150178
http://dx.doi.org/10.1590/1982-0224-2015...
). In our study, there was a dominance of young specimens (8 to 33cm) because the Amazon River mouth is known as a nursery or growth area for L. dorsalis, a migatory fish that reproduce in upstream areas of Amazonas River (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.). Despite the presence of only young specimens, the results obtained from the study of L. dorsalis’ feeding corroborated the cited above: the bigger the individuals, the bigger the possibility of obtaining fruits and seeds (Barbosa et al., 2015Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48.).

As the body size increases, specimens can expand their foraging ability, using a wider spectrum of resources (Abelha et al., 2001Abelha MCF, Agostinho AA, Goulart E. Plasticidade trófica em peixes de água doce. Acta Sci. 2001; 23(2):425-34.), including larger fruits and seeds like aninga M. linifera. In our study, smaller fishes fed mainly on pieces of fruits (mainly the pulp) such as buriti M. flexuosa. With an increased body size, catfishes started to consume other fruits such as açaí E. oleracea and aninga M. linifera, and also increased the abundance and diversity of items consumed per individual, e.g. crustaceans (see Barbosa et al., 2015Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48. to access the complete diet of L. dorsalis). This higher fruits and seeds intake is evidence that L. dorsalis can be a disperser species, since one of the factors that influence the efficiency of a disperser is the number of seeds consumed per visit to the plant (Schupp, 1993Schupp EW. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio. 1993; 107/108:15-29.; Schupp et al., 2010Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.).

Ichthiochory allows new seedlings to develop distant from the source plant, enhancing the distribution of these species throughout the floodplain (Steavaux et al., 1994Stevaux MCS, Negrelle RRB, Zanette VC. Seed dispersal by the fish Pterodoras granulosus in the Paraná River basin, Brazil. J Trop Ecol. 1994; 10:621-26.). A single seed can be consumed by many species of fish, increasing the probability of the plant species of reaching new areas and connect plant populations in fragmented landscapes (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.; Schupp, 1993Schupp EW. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio. 1993; 107/108:15-29.; Nathan, Muller-Landau, 2000Nathan R, Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol. 2000; 15(7):278-85.; Levey et al., 2005Levey DJ, Bolker BM, Tewksbury JJ, Sargent S, Haddad NM. Effects of landscape corridors on seed dispersal by birds. Science. 2005; 309(5731):146-48.; Piedade et al., 2006Piedade MTF, Parolin P, Junk WJ. Phenology, fruit production and seed dispersal of Astrocaryum jauari (Arecaceae) in Amazonian black water floodplains. Rev Biol Trop. 2006; 54(4):1171-78.; Seidler, Plotkin 2006Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.; Schupp et al., 2010Schupp EW, Jordano P, Gómez JM. Seed dispersal effectiveness revisited: A conceptual review. New Phytol. 2010; 188(2):333-53.). The Amazon mouth is full of islands (Goulding et al., 2003Goulding M, Barthem RB, Ferreira EJG. The Smithsonian Atlas of the Amazon. Washington: Smithsonian Institution; 2003.; Machado, 2008Machado J. O Município de Abaetetuba: Geografia Física e Dados Estatísticos. Abaetetuba: Edições Alquimia; 2008.) and seeds of plant species consumed by L. dorsalis can possibly reach several new sites that would not be attained without the aid of this potential disperser.

Even if many fishes consume a single plant species, dispersal mechanisms can cause interdependence as the result of natural selection, which selects traits that increase the survival chances of the seeds (Fenner, 1985Fenner M. Seed ecology. London: Chapman and Hall; 1985.). This may be the case of L. dorsalis and E. oleracea since, even though it feeds on several plant species, the rock-bacu led to an improvement in germination performance of seeds of açaí. Due to this possible interdependence relationship, seed dispersal is an important process for dispersers and plants, where both sides are favored: the disperser, for having a high-energy food source, e.g. açaí with 247 kcal in 100 g of dry fruit (Lorenzi et al., 2006Lorenzi H, Bacher L, Lacerda M, Sartori S. Frutas brasileiras e exóticas cultivadas: de consumo in natura. Nova Odessa (SP): Instituto Plantarum de Estudos da Flora; 2006.), and the plant, for having the opportunity to perpetuate its species and colonize new environments (Beckman, Rogers, 2013Beckman NG, Rogers HS. Consequences of seed dispersal for plant recruitment in tropical forests: Interactions within the seedscape. Biotropica. 2013; 45(6):666-81.; Correa et al., 2015bCorrea SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
http://dx.doi.org/10.1111/brv.12153...
). The dispersion sets the initial spatial distribution of plants, determines the group of interacting species and contributes to the community structure and the maintenance of species diversity (Seidler, Plotkin, 2006Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.; Anderson et al., 2009Anderson JT, Saldaña-Rojas J, Flecker AS. High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia. 2009; 161(2):279-90.).

Lithodoras dorsalis speeded germination but reduced germination success for M. linifera. This means that, despite the increased germination performance, a very low number of progeny plants were generated (Schupp, 1993Schupp EW. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio. 1993; 107/108:15-29.) and thus, this catfish cannot be considered a disperser of this specific plant species. The opposite occurred for açaí E. oleracea seeds, where the digestive process accelerated germination, resulting on a high germination percentage. The natural removal of the epicarp and the mesocarp of this plant by L. dorsalis may have enable the breaking of seed dormancy and its subsequent germination, generating several offsprings (around 85%) (Nascimento, Silva, 2005Nascimento WMO, Silva WR. Comportamento fisiológico de sementes de açaí (Euterpe oleracea Mart.) submetidas à desidratação. Rev Bras Frutic . 2005; 27(3):349-51.; Empresa Brasileira de Pesquisa Agropecuária (Embrapa), 2006Empresa Brasileira de Pesquisa Agropecuária (Embrapa). Sistema de Produção do Açaí. 2006 [Date of access - 15 June 2014] Available from: Available from: http://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/Acai/SistemaProducaoAcai_2ed/index.htm
http://sistemasdeproducao.cnptia.embrapa...
; Martins et al., 2009Martins CC, Nakagawa J, Bovi MLA. Avaliação da qualidade fisiológica de sementes de Açaí. Rev Bras Frutic. 2009; 31(1):231-35.; Gama et al., 2010Gama JSN, Monte DMO, Alves EU, Bruno RLA, Braga Júnior JM. Temperaturas e substratos para germinação e vigor de sementes de Euterpe oleracea Mart. Rev Ciênc Agron. 2010; 41(4):664-70.).

In view of the potential role as a seed disperser for L. dorsalis, we concluded that the species has a diet composed mainly of fruits. The species is a potential disperser of açaí E. oleracea, widening the germination performance of the seeds that passed through the animal’s digestive tract, when compared to seeds taken from parent trees. Also, with an increasing in body size, the seeds consumed by the rock-bacu also increase, favoring its possible role as a disperser. Finally, there is the importance of riparian forests to fish populations and vice versa due to its interdependence relationship, where each one plays a key role: as food source and as seed disperser.

Acknowledgments

We thank the Brazilian Higher Education Training Program (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES) for the scholarship (TAPB), the Brazilian National Research Council (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq) for the research fellowship provided to LFAM (process no. 301343/2012-8) and the Federal Institute of Pará - Abaetetuba Campus (Instituto Federal do Pará - IFPA-Abaetetuba) for the logistic support. We also thank the researches and professors M.Sc. Marta Coutinho (IFPA), Dr. José Birindeli (Museu de Zoologia da Universidade de São Paulo; MZUSP), and Dr. Alba Lins (MPEG) for helping on the identification of the stomach contents of Lithodoras dorsalis, Dr. Ana Cristina Mendes de Oliveira for reviewing part of the text and Mr. Ilso, Jaime and Giovani for the field assistance.

References

  • Abelha MCF, Agostinho AA, Goulart E. Plasticidade trófica em peixes de água doce. Acta Sci. 2001; 23(2):425-34.
  • Almeida EIB, Costa LC, Carneiro GG, Ribeiro WS, Barbosa JA. Análise biométrica e físico-química de frutos de açaizeiros cultivados no Brejo paraibano. Tecnol & Ciên Agropec. 2011; 5(2):1-4.
  • Amarante CB, Solano FAR, Lins ALFA, Müller AH, Müller RCS. Caracterização física, química e nutricional dos frutos da aninga. Planta Daninha. 2011; 29(2):295-303.
  • Agência Nacional de Águas (ANA). Hidroweb: sistema de informações hidrológicas. 2016 [Date of access - 11 October 2016]. Available from: Available from: http://hidroweb.ana.gov.br/HidroWeb
    » http://hidroweb.ana.gov.br/HidroWeb
  • Anderson JT, Saldaña-Rojas J, Flecker AS. High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia. 2009; 161(2):279-90.
  • Anderson JT, Nuttle T, Saldaña-Rojas JS, Pendergast TH, Flecker AS. Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc R Soc B. 2011; 278:3329-35.
  • Barbosa TAP, Barthem RB, Montag LFA. Feeding ecology of immature Lithodoras dorsalis (Valenciennes, 1840) (Siluriformes: Doradidae) in a tidal environment, estuary of the rio Amazonas. Neotrop Ichthyol. 2015; 13(2):341-48.
  • Barthem RB, Schwassmann HO. Amazon river influence on the seasonal displacement of the salt wedge in the Tocantins river estuary, Brazil, 1983-1985. Bol Mus Para Emilio Goeldi Ser Zool. 1994; 10(1):19-130.
  • Beckman NG, Rogers HS. Consequences of seed dispersal for plant recruitment in tropical forests: Interactions within the seedscape. Biotropica. 2013; 45(6):666-81.
  • Brondízio ES, Safar CAM, Siqueira AD. The urban market of açaí fruit (Euterpe oleracea Mart.) and rural land use change: Ethnographic insights into the role of price and land tenure constraining agricultural choices in the Amazon estuary. Urban Ecosyst. 2003; 6(1/2):67-97.
  • Correa SB, Araujo JK, Penha JMF, Cunha CN, Stevenson PR, Anderson JT. Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biol Conserv. 2015a; 191:159-67.
  • Correa SB, Pereira RC, Fleming T, Goulding M, Anderson JT. Neotropical fsh-fruit interactions: eco-evolutionary dynamics and conservation. Biol Rev [serial on internet]. 2015b; Available from: http://dx.doi.org/10.1111/brv.12153
    » http://dx.doi.org/10.1111/brv.12153
  • Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fuctuating resources in the Amazonian foodplain forest. Ecology. 2014; 95(1):210-24.
  • Correa SB, Winemiller KO, López-Fernandez H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. BioScience. 2007; 57(9):748-56.
  • Dala Corte RB, Silva ER, Fialho CB. Diet-morphology relationship in the stream-dwelling characid Deuterodon stigmaturus (Gomes, 1947) (Characiformes: Characidae) is partially conditioned by ontogenetic development. Neotrop Ichthyol . 2016; 14(2):e150178. Available from: http://dx.doi.org/10.1590/1982-0224-20150178
    » http://dx.doi.org/10.1590/1982-0224-20150178
  • Drewe KE, Horn MH, Dickson KA, Gawlicka A. Insectivore to frugivore: ontogenetic changes in gut morphology and digestive enzyme activity in the characid fish Brycon guatemalensis from Costa Rican rain forest streams. J Fish Biol. 2004; 64(4):890-902.
  • Empresa Brasileira de Pesquisa Agropecuária (Embrapa). Sistema de Produção do Açaí. 2006 [Date of access - 15 June 2014] Available from: Available from: http://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/Acai/SistemaProducaoAcai_2ed/index.htm
    » http://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/Acai/SistemaProducaoAcai_2ed/index.htm
  • Fenner M. Seed ecology. London: Chapman and Hall; 1985.
  • Fenner M. Seeds - The Ecology of Regeneration in Plant Communities. 2nd ed. Wallingford: CABI Publishing; 2000.
  • Ferreira CS, Piedade MTF, Wittmann AO, Franco AC. Plant reproduction in the Central Amazonian floodplains: challenges and adaptations. AoB Plants. 2010; 2010:plq009. Available from: http://dx.doi.org/10.1093/aobpla/plq009
    » http://dx.doi.org/10.1093/aobpla/plq009
  • Galetti M, Donatti CI, Pizo MA, Giacomini HC. Big fish are the best: seed dispersal of Bactris glaucescens by the pacu fish (Piaractus mesopotamicus) in the Pantanal, Brazil. Biotropica . 2008; 40(3):386-89.
  • Gama JSN, Monte DMO, Alves EU, Bruno RLA, Braga Júnior JM. Temperaturas e substratos para germinação e vigor de sementes de Euterpe oleracea Mart. Rev Ciênc Agron. 2010; 41(4):664-70.
  • Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUCMinas; 2003.
  • Gottsberger G. Seed dispersal by fish in the inundated regions of Humaitá, Amazonia. Biotropica . 1978; 10(3):170-83.
  • Goulding M. The fishes and the forest: explorations in Amazonian natural history. London: University of California Press; 1980.
  • Goulding M, Barthem RB, Ferreira EJG. The Smithsonian Atlas of the Amazon. Washington: Smithsonian Institution; 2003.
  • Guimarães LA, Santos TM, Rodrigues MD, Frahan BH. Produção e comercialização do açaí do município de Abaetetuba, Pará. In: Jardim MAG, Mourão L, Groissman M, editores. Açaí (Euterpe oleracea Mart.): possibilidades e limites para o desenvolvimento sustentável no estuário amazônico. Belém: Museu Paraense Emílio Goeldi; 2004. p. 159-79.
  • Herrera CM, Jordano P. Prunus mahaleb and birds: the high-efficiency seed dispersal system of a temperate fruiting tree. Ecol Monogr. 1981; 51(2):203-18.
  • Hida N, Maia JG, Hiraoka M, Shimm O, Nobuaki M. River water level changes of the Amazon Estuary: at Breves, Caxiuanã and Abaetetuba. Manaus’99 - Hydrological and Geochemical Processess in Large Scale River Basins. 1999; p.1-9.
  • Horn MH. Evidence for dispersal of fig seeds by the fruit-eating characid fish Brycon guatemalensis Regan in a Costa Rican tropical rain forest. Oecologia . 1997; 109:259-64.
  • Horn MH, Correa SB, Parolin P, Pollux BJA, Anderson JT, Lucas C, Widmann P, Tjiu A, Galetti M, Goulding M. Seed dispersal by fishes in tropical and temperate fresh waters: The growing evidence. Acta Oecol. 2011; 37(6):561-77.
  • Hyslop EJ. Stomach contents analysis - a review of methods and their application. J Fish Biol . 1980; 17(4):411-29.
  • Junk WJ, Soares M, Saint-Paul U. The Fish. In: Junk WJ, editor. The central Amazon Floodplain: ecology of a pulsing system. Berlin: Springer; 1997. p 385-408.
  • Kawakami E, Vazzoler G. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Oceanogr. 1980. 29(2):205-07.
  • Kubitzki K, Ziburski A. Seed dispersal in flood plain forests of Amazonia. Biotropica . 1994; 26(1):30-43.
  • Labouriau LG. A germinação das sementes. Washington: OEA; 1983.
  • Labouriau LG, Valadares MB. On the germination of seeds of Calotropis procera An Acad Bras Cien. 1976; 48:174-86.
  • Levey DJ, Bolker BM, Tewksbury JJ, Sargent S, Haddad NM. Effects of landscape corridors on seed dispersal by birds. Science. 2005; 309(5731):146-48.
  • Li N, Li X, An S, Lu C. Impact of multiple bird partners on the seed dispersal effectiveness of China’s relic trees. Sci Rep [serial on internet]. 2016; 6:17489. Available from: http://dx.doi.org/10.1038/srep17489
    » http://dx.doi.org/10.1038/srep17489
  • Lins ALFA, Oliveira PL. Origem, aspectos morfológicos e anatômicos das raízes embrionárias de Montrichardia linifera (Arruda) Schott (Araceae). Bol Mus Para Emílio Goeldi Ser Bot. 1994; 10(2):221-236.
  • Lorenzi H, Souza HM, Costa JTM, Cerqueira LSC, Behr N. Palmeiras do Brasil: nativas e exóticas. Nova Odessa (SP): Editora Plantarum; 1996.
  • Lorenzi H, Bacher L, Lacerda M, Sartori S. Frutas brasileiras e exóticas cultivadas: de consumo in natura. Nova Odessa (SP): Instituto Plantarum de Estudos da Flora; 2006.
  • Machado J. O Município de Abaetetuba: Geografia Física e Dados Estatísticos. Abaetetuba: Edições Alquimia; 2008.
  • Maguire JD. Speed of germination - Aid in selection and evaluation for seedling emergence and vigor. Crop Sci. 1962; 2(2):176-77.
  • Maia LA, Chalco FP. Produção de frutos de espécies da floresta de várzea da Amazônia Central importantes na alimentação de peixes. Acta Amazon. 2002; 32(1):45-53.
  • Maia LMA, Santos LM, Parolin P. Germinação de sementes de Bothriospora corymbosa (Rubiaceae) recuperadas do trato digestório de Triportheus angulatus (sardinha) no Lago Camaleão, Amazônia Central. Acta Amazon . 2007; 37(3):321-26.
  • Margalef R. Ecologia. Barcelona: Omega; 1991.
  • Martins CC, Nakagawa J, Bovi MLA. Avaliação da qualidade fisiológica de sementes de Açaí. Rev Bras Frutic. 2009; 31(1):231-35.
  • Mayo SJ, Bogner J, Boyce PC. The Genera of Araceae. United Kingdom: Royal Botanic Gardens; 1997.
  • Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. 2009 [Date of access - 20 October 2016]. Available from: Available from: http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/arquivos-publicacoes-insumos/2946_regras_analise_sementes.pdf/view
    » http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/arquivos-publicacoes-insumos/2946_regras_analise_sementes.pdf/view
  • Nascimento WMO, Silva WR. Comportamento fisiológico de sementes de açaí (Euterpe oleracea Mart.) submetidas à desidratação. Rev Bras Frutic . 2005; 27(3):349-51.
  • Nathan R, Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol. 2000; 15(7):278-85.
  • Oliveira EC, Piña-Rodrigues FCM, Figliolia MB. Propostas para a padronização de metodologias em análise de sementes florestais. Rev Bras Sementes. 1996; 11(1-3):1-42.
  • Paula JE. Anatomia de Euterpe oleracea Mart. (Palmae da Amazônia). Acta Amazon . 1975; 5(3):265-78.
  • Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci. 2007; 11(5):1633-44.
  • Piedade MTF, Parolin P, Junk WJ. Phenology, fruit production and seed dispersal of Astrocaryum jauari (Arecaceae) in Amazonian black water floodplains. Rev Biol Trop. 2006; 54(4):1171-78.
  • Pilati R, Andrian IF, Carneiro JWP. Desempenho germinativo de sementes de Cecropia pachystachya trec. (Cecropiaceae), recuperadas do trato digestório de Doradidae, Pterodoras granulosus (Valenciennes, 1883), da planície de inundação do Alto Paraná. Interciencia. 1999; 24:47-55.
  • Pollux BJA. The experimental study of seed dispersal by fish (ichthyochory). Freshw Biol. 2011; 56:197-212.
  • Ringuelet RA, Arámburu RH, Arámburu AA. Los Peces Argentos de Agua Dulce. La Plata: Comisión de Investigaciones Científicas de la provincia de Buenos Aires; 1967.
  • Sabaj MH, Ferraris CJ, Jr. Family Doradidae (Thorny Catfishes). In: Reis RE, Kullander SO, Ferraris CJ, Jr, editors. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003. p 456-69.
  • Sampaio MB, Carrazza LR. Manual tecnológico de aproveitamento integral do fruto e da folha do buriti (Mauritia flexuosa). Brasília: Instituto Sociedade, População e Natureza (ISPN); 2012.
  • Samuels IA, Levey DJ. Effects of gut passage on seed germination: Do experiments answer the questions they ask? Funct Ecol. 2005; 19(2):365-68.
  • Santos GM, Ferreira EJG, Zuanon JAS. Peixes comerciais de Manaus. Manaus: Próvarzea; 2006.
  • Santos GM, Mérona B, Juras AA, Jégu M. Peixes do baixo rio Tocantins: 20 anos depois da Usina Hidrelétrica Tucuruí. Brasília: ELETRONORTE; 2004.
  • Schupp EW. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio. 1993; 107/108:15-29.
  • Schupp EW, Jordano P, Gómez JM. Seed dispersal effectiveness revisited: A conceptual review. New Phytol. 2010; 188(2):333-53.
  • Seidler TG, Plotkin JB. Seed dispersal and spatial pattern in tropical trees. PLoS Biol. 2006; 4(11):e344.
  • Silva BMS, Môro FV, Sader R, Kobori NN. Influência da posição e da profundidade de semeadura na emergência de plântulas de açaí (Euterpe oleracea Mart. - Arecaceae). Rev Bras Frutic . 2007; 29(1):187-90.
  • Silvertown J, Antonovics J. Integrating Ecology and Evolution in a Spatial Context. London: Blackwell Science Ltd; 2001.
  • Stevaux MCS, Negrelle RRB, Zanette VC. Seed dispersal by the fish Pterodoras granulosus in the Paraná River basin, Brazil. J Trop Ecol. 1994; 10:621-26.
  • Vargas IN, Stevenson PR. Seed and establishment limitation: Effects on plant diversity in an Amazonian rain forest. Biotropica . 2013; 45(6):737-46.
  • Wall SBV, Beck MJ. A Comparison of frugivory and scatter-hoarding seed-dispersal syndromes. Bot Rev. 2011; 78(1):10-31.
  • Welcomme RL. Fisheries Ecology of floodplain rivers. London: Longman Group Limited; 1979.
  • Wotton DM, Kelly D. Do larger frugivores move seeds further?: Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. J Biogeogr [serial on internet]. 2012; 39(11):1973-83. Available from: http://dx.doi.org/10.1111/jbi.12000
    » http://dx.doi.org/10.1111/jbi.12000

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    10 May 2016
  • Accepted
    03 Apr 2017
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br