Restricciones estequiométricas en las comunidades planctónicas de lagos patagónicos. Implicancias para la distribución y la conservación de Parabroteas sarsi

Autores/as

DOI:

https://doi.org/10.25260/EA.22.32.2.1.1841

Palabras clave:

estequiometría ecológica, depredación, tramas tróficas, copépodos, cladóceros

Resumen

La Región Patagónica, que incluye desde los Andes hasta la estepa, posee una red hidrográfica profusa, con lagos profundos y someros. En este trabajo analizamos las restricciones estequiométricas en redes tróficas con la presencia del copépodo depredador Parabroteas sarsi. Para ello, examinamos datos previos sobre la composición de la comunidad del zooplancton en lagos patagónicos con y sin peces (introducidos principalmente en el siglo XX) y experimentos propios de laboratorio y de campo. La estequiometría ecológica predice que los consumidores necesitan obtener relaciones elementales específicas para alcanzar máximas tasas de crecimiento. Por su parte, el marco geométrico de la nutrición propone que los consumidores pueden necesitar incluir diferentes ítems alimentarios para cumplir con sus requerimientos nutricionales. En este sentido, demostramos que el copépodo depredador no necesariamente encuentra presas que cumplan con sus requisitos estequiométricos, por lo que su crecimiento poblacional se ve limitado. Sin embargo, la combinación de diferentes presas le permite a este copépodo alcanzar sus requerimientos elementales. En presencia de peces, las redes alimentarias cambian hacia especies del zooplancton de menor tamaño y se pierden especies con menor relación carbono:nutrientes. En tal sentido, señalamos el impacto directo e indirecto de la introducción de peces en los balances estequiométricos y en la desaparición de este depredador invertebrado en las redes tróficas lacustres.

Citas

Acharya, K., M. Kyle, and J. J. Elser. 2004. Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnology and Oceanography 49:656-665. https://doi.org/10.4319/lo.2004.49.3.0656.

Adamowicz, S. J., S. Menu-Marque, P. D. Hebert, and A. Purvis. 2007. Molecular systematics and patterns of morphological evolution in the Centropagidae (Copepoda: Calanoida) of Argentina. Biological Journal of the Linnean Society 90:279-292. https://doi.org/10.1111/j.1095-8312.2007.00723.x.

Andersen, T., J. J. Elser, and D. O. Hessen. 2004. Stoichiometry and population dynamics. Ecology Letters 7:884-900. https://doi.org/10.1111/j.1461-0248.2004.00646.x.

Balseiro, E., B. Modenutti, and C. Queimaliños. 2001. Feeding of Boeckella gracilipes (Copepoda, Calanoida) on ciliates and phytoflagellates in an ultraoligotrophic Andean lake. Journal of Plankton Research 23:849-857. https://doi.org/10.1093/plankt/23.8.849.

Balseiro, E., B. Modenutti, C. Queimaliños, and M. Reissig. 2007. Daphnia distribution in Andean Patagonian lakes: Effect of low food quality and fish predation. Aquatic Ecology 41:599-609. https://doi.org/10.1007/s10452-007-9113-3.

Balseiro, E., C. Queimaliños, and B. Modenutti. 2004. Grazing impact on autotrophic picoplankton in two south andean lakes (Patagonia, Argentina) with different light:nutrient ratios. Revista Chilena de Historia Natural 77:73-85. https://doi.org/10.4067/S0716-078X2004000100007.

Balseiro, E., M. Souza, B. Modenutti, and M. Reissig. 2008. Living in transparent lakes: Low food P:C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnology and Oceanography 53:2383-2390. https://doi.org/10.4319/lo.2008.53.6.2383.

Balseiro, E., and M. Vega. 1994. Vulnerability of Daphnia middendorffiana to Parabroteas sarsi predation: The role of the tail Spine. Journal of Plankton Research 16:783-793.

Bayly, I. A. 1992. The non-marine Centropagidae. SPB Academic Publishing, The Hague.

Boersma, M., C. Becker, A. M. Malzahn, and S. Vernooij. 2009. Food chain effects of nutrient limitation in primary producers. Marine and Freshwater Research 60:983-989. https://doi.org/10.1093/plankt/16.7.783.

Boersma, M., and J. J. Elser. 2006. Too much of a good thing: On stoichiometrically balanced diets and maximal growth. Ecology 87:1325-1330. https://doi.org/10.1890/0012-9658(2006)87[1325:TMOAGT]2.0.CO;2.

Bullejos, F. J., P. Carrillo, E. Gorokhova, J. M. Medina-Sánchez, E. G. Balseiro, and M. Villar-Argaiz. 2014. Shifts in food quality for herbivorous consumer growth: multiple golden means in the life history. Ecology 95:1272-1284. https://doi.org/10.1890/13-0410.1.

Darchambeau, F., P. J. Faeovig, and D. O. Hessen. 2003. How Daphnia copes with excess carbon in its food. Oecologia 136:336-346. https://doi.org/10.1890/13-0410.1.

De los Ríos, P., and R. Rivera. 2008. On the geographic distribution of Parabroteas sarsi (Mrázek, 1901) (Copepoda, Calanoida). Anales del Instituto de la Patagonia 36:75-78. https://doi.org/10.1890/13-0410.1.

DeRobertis, A. 2002. Size-dependent visual predation risk and the timing of vertical migration: An optimization model. Limnology and Oceanography 47:925-933. https://doi.org/10.4319/lo.2002.47.4.0925.

Diaz, A., C. S. Maturana, L. Boyero, P. De Los Rios Escalante, A. M. Tonin, and F. Correa-Araneda. 2019. Spatial distribution of freshwater crustaceans in Antarctic and Subantarctic lakes. Scientific Reports 9:7928. https://doi.org/10.1038/s41598-019-44290-4.

Diéguez, M., and E. Balseiro. 1998. Colony size in Conochilus hippocrepis: Defensive adaptation to predator size. Hydrobiologia 387-388:421-425. https://doi.org/10.1023/A:1017042610913.

Elser, J. J., K. Acharya, M. Kyle, J. Cotner, W. Makino, T. Markow, T. Watts, S. Hobbie, W. Fagan, J. Schade, J. Hood, and R. W. Sterner. 2003. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters 6:936-943. https://doi.org/10.1046/j.1461-0248.2003.00518.x.

Elser, J. J., M. Kyle, J. Learned, M. L McCrackin, A. Peace, and L. Steger. 2016. Life on the stoichiometric knife-edge: effects of high and low food C:P ratio on growth, feeding, and respiration in three Daphnia. Inland Waters 6:136-146. https://doi.org/10.5268/IW-6.2.908.

Frost, P., M. A. Evans-White, Z. V. Finkel, T. C. Jensen, and V. Matzek. 2005. Are you what you eat? Physiological constraints on organismal stoichiometry in an elementally imbalanced world. Oikos 109:18-28. https://doi.org/10.1111/j.0030-1299.2005.14049.x.

García, P. E., M. C. Diéguez, M. A. Ferraro, H. E. Zagarese, and A. P. Pérez. 2010. Mycosporine-like amino acids in freshwater copepods: Potential sources and some factors that affect their bioaccumulation. Photochemistry and Photobiology 86:353-359. https://doi.org/10.1111/j.1751-1097.2009.00670.x.

Garcia, R. D., P. E. García, and M. Reissig. 2013. Sexual size dimorphism in calanoid copepods (Centropagidae) from Patagonia (Argentina). New Zealand Journal of Marine and Freshwater Research 47:504-514. https://doi.org/10.1080/00288330.2013.802699.

García, R. D., F. G. Jara, M. M. Steciow, and M. Reissig. 2018. Oomycete parasites in freshwater copepods of Patagonia: effects on survival and recruitment. Diseases in Aquatic Organisms 129:123-134. https://doi.org/10.3354/dao03240.

Hall, S. R., M. A. Leibold, D. A. Lytle, and V. H. Smith. 2004. Stoichiometry and planktonic grazer composition over gradients of light, nutrients and predation risk. Ecology 85:2291-2301. https://doi.org/10.1890/03-0471.

Hansson, L.-A., and L. J. Tranvik. 1996. Quantification of invertebrate predation and herbivory in food chains of low complexity. Oecologia 108:542-551. https://doi.org/10.1007/BF00333732.

Hansson, L.-A., and L. J. Tranvik. 2003. Food webs in sub-Antarctic lakes: a stable isotope approach. Polar Biology 26:783-788. https://doi.org/10.1007/s00300-003-0553-5.

Herstoff, E. M., C. L. Meunier, M. Boersma, and S. B. Baines. 2021. Leveraging differences in multiple prey traits allows selective copepods to meet their threshold elemental ratios. Limnology and Oceanography 66:2914-2922. https://doi.org/10.1002/lno.11800.

Hessen, D. O., P. J. Faerovig, and T. Andersen. 2002. Light, nutrients, and P : C ratios in algae: Grazer performance related to food quality and quantity. Ecology 83:1886-1898. https://doi.org/10.1890/0012-9658(2002)083[1886:LNAPCR]2.0.CO;2.

Heywood, R. 1967. Antarctic Ecosystems The freshwater lakes of Signy Island and their fauna. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 252:347-362. https://doi.org/10.1890/0012-9658(2002)083[1886:LNAPCR]2.0.CO;2.

Heywood, R. B. 1970. Ecology of the fresh-water-lakes of Signy Island, South Orkney Islands: III Biology of the copepod Pseudoboeckella silvestri Daday (Copepoda, Centropagidae). Br Antarct Surv Bull 23:1-17.

Izaguirre, I., J. Lancelotti, J. F. Saad, S. Porcel, I. O'Farrell, M. C. Marinone, I. Roesler, and M. D. C. Dieguez. 2018. Influence of fish introduction and water level decrease on lakes of the arid Patagonian plateaus with importance for biodiversity conservation. Global Ecology and Conservation 14: e00391. https://doi.org/10.1016/j.gecco.2018.e00391.

Jara, F. G., M. G. Perotti, and M. C. Diéguez. 2012. Distribution of backswimmers in shallow ponds of Patagonia and their predatory role on a common tadpole–copepod assemblage. New Zealand Journal of Marine and Freshwater Research 46:459-473. https://doi.org/10.1080/00288330.2012.707130.

Lampert, W. 1993. Phenotypic plasticity of the size at 1st reproduction in Daphnia - the importance of maternal size. Ecology 74:1455-1466. https://doi.org/10.1080/00288330.2012.707130.

Lancelotti, J., M. C. Marinone, and I. Roesler. 2017. Rainbow trout effects on zooplankton in the reproductive area of the critically endangered hooded grebe. Aquatic Conservation: Marine and Freshwater Ecosystems 27:128-136. https://doi.org/10.1002/aqc.2629.

Lancelotti, J. L., L. M. Pozzi, P. M. Yorio, M. C. Diéguez, and M. A. Pascual. 2010. Precautionary rules for exotic trout aquaculture in fishless shallow lakes of Patagonia: minimizing impacts on the threatened hooded grebe (Podiceps gallardoi). Aquatic Conservation: Marine and Freshwater Ecosystems 20:1-8. https://doi.org/10.1002/aqc.1067.

Laspoumaderes, C., B. Modenutti, J. Elser, and E. Balseiro. 2015. Does the stoichiometric carbon:phosphorus knife edge apply for predaceous copepods? Oecologia 178:557-569. https://doi.org/10.1007/s00442-014-3155-8.

Laspoumaderes, C., B. Modenutti, M. S. Souza, M. Bastidas Navarro, F. Cuassolo, and E. Balseiro. 2013. Glacier melting and stoichiometric implications for lake community structure: Zooplankton species distributions across a natural light gradient. Global Change Biology 19:316-326. https://doi.org/10.1111/gcb.12040.

Laspoumaderes, C., B. E. Modenutti, and E. G. Balseiro. 2010. Herbivory versus omnivory: linking homeostasis and elemental imbalance in copepod development. Journal of Plankton Research 32:1573-1582. https://doi.org/10.1093/plankt/fbq077.

Leroux, S. J., and L. Michel. 2010. Consumer-mediated recycling and cascading trophic interactions. Ecology 91:2162-2171. https://doi.org/10.1890/09-0133.1.

Macchi, P. J., V. E. Cussac, M. F. Alonso, and M. A. Denegri. 1999. Predation relationships between introduced salmonids and the native fish fauna in lakes and reservoirs in north Patagonia. Freshwater Biology 8:227-236. https://doi.org/10.1111/j.1600-0633.1999.tb00074.x.

Malzahn, A. M., N. Aberle, C. Clemmesen, and M. Boersma. 2007. Nutrient limitation of primary producers affects planktivorous fish condition. Limnology and Oceanography 52:2062-2071. https://doi.org/10.4319/lo.2007.52.5.2062.

Menu Marque, S. A., and M. C. Marinone. 1986. El zooplancton de seis lagos del Chubut (Argentina) y sus probables relaciones con la ictiofauna y algunos factores ambientales. Pp. 90-114 in I. Vila and E. Fagetti (eds.). Trabajos presentados al taller internacional sobre ecología y manejo de peces en lagos y embalses. Santiago de Chile, 5-10 de noviembre de 1984. FAO, Roma.

Meunier, C. L., M. Boersma, K. H. Wiltshire, and A. M. Malzahn. 2016. Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125:50-58. https://doi.org/10.1111/oik.02072.

Modenutti, B., R. Albariño, M. B. Navarro, V. D. Villanueva, M. Sol Souza, C. Trochine, C. Laspoumaderes, F. Cuassolo, G. Mariluán, L. Buria, and E. Balseiro. 2010. Structure and dynamic of food webs in Andean North Patagonian freshwater systems: Organic matter, light and nutrient relationships. Ecología Austral 20:95-114.

Modenutti, B., E. Balseiro, M. C. Dieguez, C. Queimalinos, and R. Albarino. 1998. Heterogeneity of fresh-water Patagonian ecosystems. Ecología Austral 8:155-165.

Modenutti, B., and E. G. Balseiro. 1994. Zooplankton Size Spectrum in four Lakes of the Patagonian Plateau. Limnologica 24:51-56.

Modenutti, B., C. Queimaliños, E. Balseiro, and M. Reissig. 2003. Impact of different zooplankton structures on the microbial food web of a South Andean oligotrophic lake. Acta Oecologica 24:S289-S298. https://doi.org/10.1016/S1146-609X(03)00030-4.

Modenutti, B., L. Wolinski, M. S. Souza, and E. G. Balseiro. 2018. When eating a prey is risky: Implications for predator diel vertical migration. Limnology and Oceanography 63:939-950. https://doi.org/10.1002/lno.10681.

Moe, S. J., R. S. Stelzer, M. R. Forman, W. S. Harpole, T. Daufresne, and T. Yoshida. 2005. Recent advances in ecological stoichiometry: Insights for population and community ecology. Oikos 109:29-39. https://doi.org/10.1111/j.0030-1299.2005.14056.x.

Ortubay, S., V. Cussac, M. Battini, J. Barriga, J. Aigo, M. Alonso, P. Macchi, M. Reissig, J. Yoshioka, and S. Fox. 2006. Is the decline of birds and amphibians in a steppe lake of northern Patagonia a consequence of limnological changes following fish introduction? Aquatic Conservation: Marine and Freshwater Ecosystems 16:93-105. https://doi.org/10.1002/aqc.696.

Pascual, M., P. Macchi, J. Urbanski, F. Marcos, C. Riva Rossi, M. Novara, and P. Dell'Arciprete. 2002. Evaluating potential effects of exotic freshwater fish from incomplete species presence-absence data. Biological Invasions 4:101-113. https://doi.org/10.1023/A:1020513525528.

Pizzolon, L., N. Santinelli, M. C. Marinone, and S. A. Menu-Marque. 1995. Plankton and hydrochemistry of Lake Futalaufquen (Patagonia, Argentina) during the growing season. Hydrobiologia 316:63-73. https://doi.org/10.1007/BF00019376.

Quirós, R. 1990. Factors related to variance of residuals in chlorophyll - total phosphorus regressions in lakes and reservoirs of Argentina. Hydrobiologia 200-201:343-355. https://doi.org/10.1007/BF02530352.

Quirós, R., and C. Baigún. 1985. Fish abundance related to organic matter in the Plata River Basin, South America. Trans Amer Fish Soc 114:377-387. https://doi.org/10.1007/BF02530352.

Raubenheimer, D., and S. J. Simpson. 2004. Organismal stoichiometry: quantifying non-independence among food components. Ecology 85:1203-1216. https://doi.org/10.1007/BF02530352.

Reissig, M., B. Modenutti, E. Balseiro, and C. Queimaliños. 2004. The role of the predaceous copepod Parabroteas sarsi in the pelagic food web of a large deep Andean lake. Hydrobiologia 524:67-77. https://doi.org/10.1023/B:HYDR.0000036120.33105.05.

Reissig, M., C. Trochine, C. Queimaliños, E. Balseiro, and B. Modenutti. 2006. Impact of fish introduction on planktonic food webs in lakes of the Patagonian Plateau. Biological Conservation 132:437-447. https://doi.org/10.1016/j.biocon.2006.04.036.

Schoo, K. L., N. Aberle, A. M. Malzahn, and M. Boersma. 2010. Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus? Aquatic Ecology 44:233-242. https://doi.org/10.1007/s10452-009-9265-4.

Simpson, S. J., and D. Raubenheimer. 2011. The nature of nutrition: a unifying framework. Australian Journal of Zoology 59:350. https://doi.org/10.1007/s10452-009-9265-4.

Souza, M. S., E. Balseiro, C. Laspoumaderes, and B. Modenutti. 2010. Effect of ultraviolet radiation on Acetylcholinesterase activity in freshwater copepods. Photochemistry and Photobiology 86:367-373. https://doi.org/10.1111/j.1751-1097.2009.00675.x.

Sperfeld, E., N. D. Wagner, H. M. Halvorson, M. Malishev, and D. Raubenheimer. 2017. Bridging Ecological Stoichiometry and Nutritional Geometry with homeostasis concepts and integrative models of organism nutrition. Functional Ecology 31:286-296. https://doi.org/10.1111/1365-2435.12707.

Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry. The biology of elements from molecules to the biosphere. Princeton University Press, Princeton, NJ, USA. https://doi.org/10.1515/9781400885695.

Sterner, R. W., J. J. Elser, E. J. Fee, S. J. Guildford, and T. H. Chrzanowski. 1997. The light:nutrient ratio in lakes: The balance of energy and materials affects ecosystem structure and process. The American Naturalist 150:663-684. https://doi.org/10.1086/286088.

Suzuki-Ohno, Y., M. Kawata, and J. Urabe. 2012. Optimal feeding under stoichiometric constraints: a model of compensatory feeding with functional response. Oikos 121:569-578. https://doi.org/10.1111/j.1600-0706.2011.19320.x.

Tartarotti, B., G. Baffico, P. Temporetti, and H. E. Zagarese. 2004. Mycosporine-like amino acids in planktonic organisms living under different UV exposure conditions in Patagonian lakes. Journal of Plankton Research 26:753-762. https://doi.org/10.1093/plankt/fbh073.

Tessier, A. J., and J. Welser. 1991. Cladoceran assamblage, seasonal succession and the importance of a hypolimnetic refuge. Freshwater Biology 25:85-93. https://doi.org/10.1111/j.1365-2427.1991.tb00475.x.

Trochine, C., E. Balseiro, and B. Modenutti. 2008. Zooplankton of fishless ponds of Northern Patagonia: Insights into predation effects of Mesostoma ehrenbergii. International Review of Hydrobiology 93:312-327. https://doi.org/10.1002/iroh.200711011.

Trochine, C., B. Modenutti, and E. Balseiro. 2009. Chemical signals and habitat selection by three zooplankters in Andean Patagonian ponds. Freshwater Biology 54:480-494. https://doi.org/10.1111/j.1365-2427.2008.02125.x.

Vega, M. A. P. 1995. Morphology and defensive structures in the predator-prey interaction: an experimental study of Parabroteas sarsi (Copepoda, Calanoida) with different cladoceran prey. Hydrobiologia 299:139-145. https://doi.org/10.1007/BF00017565.

Vega, M. P. 1999. Life-stage differences in the diet of Parabroteas sarsi (Daday) (Copepoda, Calanoida): A field study. Limnologica 29:186-190. https://doi.org/10.1016/S0075-9511(99)80066-8.

Vega, M. P. A. 1997. The functional response of copepodid stages to adult of Parabroteas sarsi (Copepoda, Calanoida). Internationale Revue der Gesamten Hydrobiologie 82:95-105. https://doi.org/10.1002/iroh.19970820112.

Wang, H., R. W. Sterner, and J. J. Elser. 2012. On the “strict homeostasis” assumption in ecological stoichiometry. Ecological Modelling 243:81-88. https://doi.org/10.1016/j.ecolmodel.2012.06.003.

Weller, D. L. M. 1977. Observations on the diet and development of Pseudoboeckella poppei (Calanoida, Centropagidae) from an Antarctic lake. Br Antarct Surv Bull 45:77-92.

Wolinski, L., B. Modenutti, and E. Balseiro. 2020. Melanin and antipredatory defenses in Daphnia dadayana under UVR exposure. International Review of Hydrobiology 105:106-114. https://doi.org/10.1002/iroh.201902033.

Wright, D., and J. Shapiro. 1990. refuge availability: a key to understanding the summer dissapearence of Daphnia. Freshwater Biology 24:43-62. https://doi.org/10.1111/j.1365-2427.1990.tb00306.x.

Yu, Q., Q. Chen, J. J. Elser, N. He, H. Wu, G. Zhang, J. Wu, Y. Bai, and X. Han. 2010. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecology Letters 13:1390-1399. https://doi.org/10.1111/j.1461-0248.2010.01532.x.

Stoichiometric constraints in plankton communities of Patagonian lakes. Implications for Parabroteas sarsi distribution and conservation

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2022-04-27

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Balseiro, E., Modenutti, B., Laspoumaderes, C., Schenone, L., Bastidas Navarro, M., & Martyniuk, N. (2022). Restricciones estequiométricas en las comunidades planctónicas de lagos patagónicos. Implicancias para la distribución y la conservación de Parabroteas sarsi. Ecología Austral, 32(2), 638–649. https://doi.org/10.25260/EA.22.32.2.1.1841