Keywords
trophic position
trophic guilds
carbon sources
food chain
isótopos estables
posición trófica
gremios tróficos
fuentes de carbono
cadena trófica
How to Cite
Abstract
Amazonian fish assemblages are typically high in species diversity and trophic complexity. Stable isotopes are valuable tools to describe the trophic structure of such assemblages, providing useful information for conservation and ecological management. This study aimed at estimating the relative contribution of the different basal carbon sources to the diet of primary consumer fishes (herbivores and detritivores), and determining the trophic position (TP) of the dominant fishes from each trophic guild (herbivores, detritivores, invertivores and piscivores). For this purpose we analyzed stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in potential food sources, and muscle tissue of fishes in five oxbow lakes located in the floodplain of River Ichilo, Bolivia. Terrestrial plants and C3 aquatic macrophytes were the major carbon source contributing to the diet of herbivorous fishes, whereas particulate organic matter (POM) contributed more to the diet of detritivore fishes. In general, C4 aquatic macrophytes contributed little to the diet of herbivores and detritivores. However, we found a relatively high contribution of C4 macrophytes (28 %) to the diet of the herbivores Mylossoma duriventre and Schizodon fasciatus. We found a good agreement between our estimated TP values and the trophic group assigned based on diet composition from literature. The herbivore M. duriventre was at the bottom of the food web, being the baseline organism (TP = 2). The remaining primary consumers (herbivores and algivore/detritivores) exhibited relatively high TP values (2.3 - 2.9), probably due to their opportunistic feeding behavior. Omnivore/invertivore species studied displayed TP values near the 3.0 value expected for secondary consumers. Piscivore fishes were at the top TP, with TP values varying from 3.3 (Serrasalmus spilopleura and Serrasalmus rhombeus) to 3.8 (Pseudoplatystoma fasciatum). The fact that detritivore fishes, the most abundant food source for piscivores, occupy relatively high TPs determines that food chains in these particular Amazonian floodplains are longer than previously thought.References
Abrantes, K. G., Barnett, A., & Bouillon, S. (2014). Stable isotope-based community metrics as a tool to identify patterns in food web structure in east African estuaries. Functional Ecology, 28, 270-282. doi: 10.1111/1365-2435.12155
Araujo-Lima, C. A. R. M., Forsberg, B. R., Victoria, R. L., & Martinelli, L. (1986). Energy sources for detritivorous fishes in the Amazon. Science, 234, 1256-1258.
Ayala, G., Zambrana, K., & Maldonado, M. (2000). Estructura trófica de la ictiocenosis en lagunas de la llanura inundable de los ríos Ichilo y Chapare. Revista Boliviana de Ecología y Conservación Ambiental, 7, 25-35.
Azevedo-Silva, C. E., Almeida, R., Carvalho, D. P., Ometto, J. P. H. B., de Camargo, P. B., Dorneles, P. R., … Torres, J. P. M. (2016). Mercury biomagnification and the trophic structure of the ichthyofauna from a remote lake in the Brazilian Amazon. Environmental Research, 151, 286-296. doi: 10.1016/j.envres.2016.07.035
Benedito-Cecilio, E., Araujo-Lima, C. A. R. M., Forsberg, B. R., Bittencourt, M. M., & Martinelli, L. C. (2000). Carbon sources of Amazonian fisheries. Fisheries Management and Ecology, 7, 305-315. doi: 10.1046/j.1365-2400.2000.007004305.x
Busst G. M. A., & Britton J. R. (2017). Comparative trophic impacts of two globally invasive cyprinid fishes reveal species-specific invasion consequences for a threatened native fish. Freshwater Biology, 62:1587-1595. doi: 10.1111/fwb.12970
Carscallen, W. M. A., Vandenberg, K., Lawson, J. M., Martinez, N. D., & Romanuk, T. N. (2012). Estimating trophic position in marine and estuarine food webs. Ecosphere, 3, 1-20. doi: 10.1890/ES11-00224.1
Carvajal, F., & Maldonado M. (2005). Influencia de la conexión río-laguna sobre la ictiocenosis lacustre en la várzea del río Ichilo (Cochabamba - Bolivia). Revista Boliviana de Ecología y Conservación Ambiental, 17, 33-48.
Carvalho, D. R., Castro, D., Callisto, M., Moreira, M. Z., & Pompeu, P. S. (2015), Isotopic variation in five species of stream fishes under the influence of different land uses. Journal of Fish Biology, 87, 559-578. doi:10.1111/jfb.12734
Coat, S., Monti, D., Bouchon, C., & Lepoint, G. (2009). Trophic relationships in a tropical stream food web assessed by stable isotope analysis. Freshwater Biology, 54, 1028-1041. doi: 10.1111/j.1365-2427.2008.02149.x
Cucherousset, J., Bouletreau, S., Martino, A., Roussel, J. M., & Santoul, F. (2012). Using stable isotope analyses to determine the ecological effects of non-native fishes. Fisheries Management and Ecology, 19, 111-119. doi:10.1111/j.1365-2400.2011.00824.x
De Carvalho, D. R., de Castro, D. M. P., Callisto, M., Moreira, M. Z., Pompeu, P. S. (2017). The trophic structure of fish communities from streams in the Brazilian Cerrado under different land uses: an approach using stable isotopes. Hydrobiologia, 795, 199-217. doi: 10.1007/s10750-017-3130-6
Deines, P., Grey, J., Richnow, H. H., & Eller, G. (2007). Linking larval chironomids to methane: Seasonal variation of the microbial methane cycle and chironomid δ13C. Aquatic Microbial Ecology, 46, 273-282. doi: 10.3354/ame046273
De Mérona, B., & Rankin-de-Mérona, J. (2004). Food resource partitioning in a fish community of central Amazon floodplain. Neotropical Ichthyology, 2(2), 75-84.
Dos Santos, G.M. (1990). Pesca e Ecologia dos peixes de Rondônia. Manaus, AM, Brasil: Fundação Universidade do Amazonas.
Forsberg, B. R., Martinelli, L. A., Victoria, R. L., & Bonassi, J. A. (1993). Autotrophic carbon sources for fish of the Central Amazon. Ecology, 74(3), 643-652.
Freitas, C. E. C., Siqueira-Souza, F. K., Guimarães, A. R., Santos, F. A., & Santos, I. L. A. (2010). Interconnectedness during high water maintains similarity in fish assemblages of island floodplain lakes in the Amazonian Basin. Zoologia, 27(6), 931-938. doi: 10.1590/S1984-46702010000600014
Fry, B. (2006). Stable isotope ecology. New York: Springer.
Goulding, E. G., Carvalho, M., & Ferreira, L. (1988). Río Negro: Rich life in poor water. The Hague: SPB Academic Publishing.
Gu, B., Schelske, C. L., & Hoyer, M. V. (1997). Intrapopulation feeding diversity in Blue Tilapia: Evidence from stable-isotope analyses. Ecology, 78(7), 2263-2266.
Hamilton, S. K., Lewis Jr., W. M., & Sippel, S. J. (1992). Energy-sources for aquatic animals in the Orinoco River floodplain: evidence from stable isotopes. Oecologia, 89, 324-330.
Herwig, B. R., Soluk, D. A., Dettmers, J. M., & Wahl, D. H. (2004). Trophic structure and energy flow in backwater lakes of two large floodplain rivers assessed using stable isotopes. Canadian Journal of Fisheries and Aquatic Sciences, 61(1), 12-22. doi: 10.1139/f03-139
Jackson, A. T., Adite, A., Roach, K. A., & Winemiller, K. O. (2013). Primary production, food web structure, and fish yields in constructed and natural wetlands in the floodplain of an African river. Canadian Journal of Fisheries and Aquatic Sciences, 70, 543-553. doi: 10.1139/cjfas-2012-0403
Jepsen, D. B., & Winemiller, K. O. (2002). Structure of tropical river food webs revealed by stable isotope ratios. Oikos, 96(1), 46-55. doi: 10.1034/j.1600-0706.2002.960105.x
Jones, R. I., & Grey, J. (2004). Stable isotope analysis of chironomid larvae from some Finnish forest lakes indicates dietary contribution from biogenic methane. Boreal Environment Research, 9(1), 17-23.
Junk, W. J., Bayley, P. B., & Sparks, R. E. (1989). The flood pulse concept in river-floodplain systems. Canadian Special Publication of Fisheries and Aquatic Sciences, 106, 110-127.
Junk, W. J., & Piedade, M. T. F. (1993). Herbaceous plants of the Amazon floodplain near Manaus: Species diversity and adaptations to the flood pulse. Amazoniana, 12(3/4), 467-484.
Layman, C. A., Winemiller, K. O., Arrington, D. A., & Jepsen, D. B. (2005). Body size and trophic position in a diverse tropical food web. Ecology, 86(9), 2530-2535. doi: 10.1890/04-1098
Leite, R. G., Araújo-Lima, C. A. R. M., Victoria, R. L., & Martinelli, L. A. (2002). Stable isotope analysis of energy sources for larvae of eight fish species from the Amazon floodplain. Ecology of Freshwater Fish, 11, 56-63.
Lewis Jr., W. L., Hamilton, S. K., Rodriguez, M. A., Saunders III, J. F., & Lasi, M. A. (2001). Foodweb analysis of the Orinoco floodplain based on production estimates and stable isotope data. Journal of the North American Benthological Society, 20, 241-254.
Lopes, C. A., Benedito, E., & Martinelli, L. A. (2009). Trophic position of bottom-feeding fish in the Upper Paraná River floodplain. Brazilian Journal of Biology, 69(2), 573-581.
Maldonado, M., Goitia, E., & Rejas, D. (2005). El río Ichilo: un sistema río-llanura de inundación en el alto Amazonas (Bolivia). Revista Boliviana de Ecología y Conservación Ambiental, 17, 69-88.
Manetta, G. I., Benedito-Cecilio, E., & Martinelli, M. (2003). Carbon sources and trophic position of the main species of fishes of Baía River, Paraná River floodplain, Brazil. Brazilian Journal of Biology, 63(2), 283-290. doi: 10.1590/S1519-69842003000200013
Marshall, B. G., Forsberg, B. R., & Peleja, R. (2016). Evidence of mercury biomagnification in the food chain of the cardinal tetra Paracheirodon axelrodi (Osteichthyes : Characidae ) in the Rio Negro, central Amazon , Brazil. Journal of Fish Biology, 89, 220-240. doi: 10.1111/jfb.12952
Matsubayashi, J., Morimoto, J. O., Tayasu, I., Mano, T., Nakajima, M., Takahashi, O., Kobayashi, K., & Nakamura, F. (2015). Major decline in marine and terrestrial animal consumption by brown bears (Ursus arctos). Science Reports, 5, 1-8. doi: 10.1038/srep09203
McCallum, E.S., Marentette, J.R., Schiller, C., Jindal, S. Empringham, K., Marsh-Rollo, S., … Balshine, S. (2017). Diet and foraging of Round Goby (Neogobius malastomus) in a contaminated harbor. Aquatic Ecosystem Health & Management, 20, 252-264. doi: 14634988.2016.1254468.
McCutchan Jr, J. H., Lewis Jr, W. M., Kendall, C., & McGrath, C. C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos, 102, 378-390.
McMeans, B. C., Rooney, N., Arts, M. T., & Fisk, A. T. (2013). Food web structure of a coastal Arctic marine ecosystem and implications for stability. Marine Ecology Progress Series, 482, 17-28. doi: 10.3354/meps10278
Michener, R. H., & Kaufman, L. (2007). Stable isotope ratios as tracers in marine food webs: An update. In M. Michener, & K. Lajtha (Eds.), Stable isotopes ecology and environmental science (2nd ed., pp. 238-282). Oxford: Wiley-Blackwell.
Minagawa, M., & Wada, E. (1984). Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta, 48(5), 1135-1140. doi: 10.1016/0016-7037(84)90204-7
Molina, C. I., Gibon, F., Oberdorff, T., Dominguez, E., Pinto, J., Marín, R., & Roulet, M. (2011). Macroinvertebrate food web structure in a floodplain lake of the Bolivian Amazon. Hydrobiologia, 663, 135-153. doi: 10.1007/s10750-010-0565-4
Mortillaro, J. M., Pouilly, M., Wach, M., Freitas, C. E. C., Abril, G., & Meziane, T. (2015). Trophic opportunism of central Amazon floodplain fish. Freshwater Biology, 60(8), 1659-1670. doi: 10.1111/fwb.12598
Parnell, A. C, Inger, R., Bearhop, S., & Jackson A.L. (2010). Source partitioning using stable isotopes: Coping with too much variation. PLoS ONE, 5(3), e9672. doi: 10.1371/journal.pone.000967
Pauly, D., & Watson, R. (2005). Background and interpretation of the “Marine Trophic Index” as a measure of biodiversity. Philosophical Transactions of the Royal Society: Biological Sciences, 360, 415-423.
Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83(3), 703-718. doi: 10.2307/3071875
Pouilly, M., Rejas, D., Pérez, T., Duprey, J. L., Molina, C. I., Hubas, C., & Guimarães, J. R. D. (2013). Trophic Structure and Mercury Biomagnification in Tropical Fish Assemblages, Iténez River, Bolivia. PLoS ONE, 8. doi: 10.1371/journal.pone.0065054
Pouilly, M., Yunoki, T., Rosales, C., & Torres, L. (2004). Trophic structure of fish assemblages from Mamoré River floodplain lakes (Bolivia). Ecology of Freshwater Fish, 13, 245-257. doi: 10.1111/j.1600-0633.2004.00055.x/full
Rejas, D. (2004). Trophic relations and nutrient recycling in a tropical floodplain lake (Doctoral dissertation). Katholieke Universiteit Leuven, Belgium.
Rejas, D., & Maldonado, M. (2000). Variaciones espacio-temporales de la composición de la comunidad de peces de una laguna de la várzea del río Ichilo (Cochabamba, Bolivia). Revista Boliviana de Ecología y Conservación, 7, 37-46.
Rejas, D., Muylaert, K., & De Meester, L. (2005). Nutrient limitation of bacteria and sources of nutrients supporting nutrient-limited bacterial growth in an Amazonian floodplain lake. Aquatic Microbial Ecology, 39, 57-67.
Rejas, D., Villarpando, P., & Carvajal, F. (2005). Variaciones estacionales en la dieta de Moenkhausia dichroura Kner (Pisces, Characidae) en una laguna de la várzea del río ichilo (Cochabamba - Bolivia). Revista Boliviana de Ecología y Conservación, 17, 49-54.
Rosing, M. N., Ben-David, M., & Barry, R. P. (1998). Analysis of Stable Isotope Data: A K Nearest-neighbors randomization test. Journal of Wildlife Management, 62(1), 380-388.
Sanseverino, A. M., Bastviken, D., Sundh, I., Pickova, J., & Enrich-Prast, A. (2012). Methane carbon supports aquatic food webs to the fish level. PLoS ONE, 7(8). doi: 10.1371/journal.pone.0042723
Sarmiento, J., Bigorne, R., Carvajal-Vallejos F. M., Maldonado, M., Leciak, E., & Oberdorff, T. (2014). Peces de Bolivia/Bolivian fishes. Bolivia: IRD - BioFresh (UE) / Plural Editores.
Sioli, H. (1984). The Amazon: Limnology and landscape ecology of a mighty tropical river and its basin. Netherlands: Dr. Junk Publishers, Dordrecht.
Siqueira-Souza, F. K., & Freitas, C. E. C. (2004). Fish diversity of floodplain lakes on the lower stretch of the Solimões river. Brazilian Journal of Biology, 64(3A), 501-510. doi: 10.1590/S1519-69842004000300013
Thébault, E., & Loreau, M. (2003). Food-web constraints on biodiversity-ecosystem functioning relationships. Proceedings of the National Academy of Sciences of the United States of America, 100(25), 14949-14954.
Vander-Zanden, M. J., Cabana, G., & Rasmussen, J. B. (1997). Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences, 1158, 1142-1158. doi: 10.1139/cjfas-54-5-1142
Vander-Zanden, M. J., & Rasmussen, J. B. (1999). Primary consumer δ13C and δ 15N and the trophic position of aquatic consumers. Ecology, 80(4), 1395-1404.
Wantzen, K. M., de Arruda-Machado, F., Voss, M., Boriss, H., & Junk, W. J. (2002). Seasonal isotopic shifts in fish of the Pantanal wetland, Brazil. Aquatic Sciences, 64(3), 239-251. doi: 10.1007/PL00013196
Warfe, D. M., Jardine, T. D., Pettit, N. E., Hamilton, S. K., Pusey, B. J., Bunn, S. E., … Douglas, M. M. (2013). Productivity, disturbance and ecosystem size have no influence on food chain length in seasonally connected rivers. PLoS ONE, 8(6). doi: 10.1371/journal.pone.0066240
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