Keywords
bioenergetic modelling
waterbirds
wetlands
guanotrofia
bioenergética
aves acuáticas
humedales
How to Cite
Abstract
Introduction: The colonies of wading birds reach thousands of highly grouped nests, which have a marked influence on the characteristics of the soil or the water that surrounds them due to a hyperfertilization effect. This causes the harmful accumulation of nitrogen compounds altering the chemistry of the substrate and causing defoliation and death of vegetation. The impact of these colonies on the mangroves in Cuba has not been evaluated, due to the logistical difficulties involved and the complexity of their processes. Objective: Mathematical modeling is a useful tool in these situations, so in this work the estimation of the quantities of biomass, energy and nutrients mobilized in a colony of herons was carried out, through a bioenergetic model of system dynamics. Methods: We used 29 primary variables, 3 bioenergetic equations and the postnatal growth equation of this species, implemented in the STELLA 9.1.3 program. From the interaction of these variables, the energy required by the reproduction cycle, the biomass consumed and the nutrients deposited in the colony were obtained. A sensitivity analysis and an uncertainty analysis were carried out to explore the variables that have the most influence on the results. The model was validated by the consistency in the units, the test of extreme values and the comparison with values recorded in the literature. Finally, disturbances scenarios that can affect a real colony were simulated. Results: According to the model, each nestling require 10 219.2 kcal to growth. The colony must totally invest 6.71x106 kcal, which represents consumption close to 2.2 tons of dams. Due to this consumption, the nutrients deposited in the colony by the excreta were 49 kg of nitrogen, 7 kg of phosphorus and 56 kg of calcium. According to the sensitivity analysis, the variables that produce the strongest changes in the result are the number of adults in the colony and the average clutch size. The uncertainty analysis showed little influence of the variables selected on the response variables. The most harmful simulated disturbances for the colony were the affectations to the recruitment and the increase of the mortality of the nestlings.
References
Allaway, W. G., & Ashford, A. E. (1984). Nutrient input by seabirds to the forest on a coral island of the Great Barrier Reef. Marine Ecology Progress Series, 19, 297-298.
Alongi, D. M. (2008). Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine, Coastal and Shelf Science, 76, 1-13.
Antúnez, O., & Denis, D. (2013). Aspectos de la reproducción de la Marbella (Anhinga anhinga) en Cuba. Revista Cubana de Ciencias Biológicas, 2(2), 73-76.
Arendt, W. J. (1988). Range expansion of the Cattle Egret (Bubulcus ibis) in the Greater Caribbean Basin. Colonial Waterbirds, 11, 252-262.
Arendt, W. J. & Arendt, A. I. (1988): Aspects of the breeding biology of the Cattle Egret (Bubulcus ibis) in Monserrat, West Indies, and its impact on nest vegetation. Colonial Waterbirds, 11(1), 72-84.
Baisre, J. A. (2006). Assessment of nitrogen flows into the Cuban landscape. Biogeochemistry, 79, 91-108
Bateman, D. L. (1970). Movement-behavior in three species of colonial nesting wading birds: a radio-telemetric study (Doctoral dissertation). Auburn University, Alabama, USA.
Baxter, G. S., & Fairweather, P. G. (1994). Nitrogen and phosphorus in wetlands with and without egrets. Australian Journal of Ecology, 19, 409-416.
Bedard, J., Therriault, J. C., & Berube, J. (1980). Assessment of the importance of nutrient recycling by seabirds in the St. Lawrence Estuary. Canadian Journal of Fisheries and Aquatic Sciences, 37, 583-588.
Bildstein, K. L. (1997). Wading-bird science: A guide for the Twenty-first century. Colonial Waterbirds, 20(1), 138-142.
Bildstein, K. L., Blood, E., & Fredtirick, P. C. (1992). The relative importance of biotic and abiotic vectors in nutrient processing in South Carolina, U.S.A., estuarine ecosystem. Estuaries, 15, 147-157.
Bildstein, K. L., Post, W., Johnston, J., & Frederick, P. (1990). Freshwater wetlands, rainfall, and the breeding ecology of White Ibises in coastal South Carolina. The Wilson Bulletin, 102, 84-98.
Blanco, P., & Sánchez, B. (2006). Importancia de los manglares cubanos para la ornitofauna. En L. Menéndez & J. M. Guzmán (Eds.), Ecosistema de manglar en el Archipiélago Cubano: Estudios y experiencias enfocados a su gestión (pp. 142-152). Cuba: Editorial Academia.
Blanco, P., Peris, S., & Sánchez, B. (2000). Las aves Limícolas (Charadriiformes) nidificantes de Cuba: Su distribución y reproducción. Alicante, España: Centro Iberoamericano de la Biodiversidad.
Browder, J. A. (1973). Studies on the feeding ecology and morphological variation of the Cattle Egret Bubulcus ibis (Linnaeus) (Aves: Ardeidae) (Master dissertation). University Miami, Coral Gables, Florida, USA.
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., & West, G. B. (2004). Toward a metabolic theory of ecology. Ecology, 85(7), 1771-1789.
Brzorad, J. N., Maccarone, A. D., & Conley, K. J. (2004). Foraging energetics of Great Egrets and Snowy Egrets. Journal of Field Ornithology, 75(3), 266-280.
Burger, J. (1978). Competition between Cattle Egrets and native North American herons, egrets and ibises. Condor, 80, 15-23.
Burger, J. (1979). Resource partitioning nest site selection in mixed species colonies of herons, egrets and ibises. American Midland Naturalist, 101, 191-210.
Burger, J. (1982). An overview of proximate factors affecting reproductive success in colonial birds: concluding remarks and summary of panel discussion. Colonial Waterbirds, 5, 58-65.
Burns, E. C., & Chapin, J. B. (1969). Arthropods in the diet of the Cattle Egret, Bubulcus ibis, in southern Louisiana. Journal of Economic Entomology, 62, 736-738.
Cairns, D. K., Chapdewne, G., & Montevechi, W. A. (1991). Prey exploitation by seabirds in the Gulf of St. Lawrence. In J. C. Theniault (Ed.), The Gulf of St. Lawrence: small ocean or big estuary? (pp. 277-291). Ottawa, Canada: Canadian Special Publication of Fisheries and Aquatic Sciences.
Carey, C. (1996). Avian energetics and nutritional ecology. London, UK: Chapman y Hall.
Carey, C., Rahn, H., & Parisi, P. (1980). Calories, water, lipid and yolk in avian eggs. Condor, 82, 335-343.
Chipps, S. R. & Wahl, D. H. (2008). Bioenergetics Modeling in the 21st Century: Reviewing New Insights and Revisiting Old Constraints. Transactions of the American Fisheries Society, 137, 298-313
Clevelandn, C. C., Townsend, A. R., Schimel, D. S., Fisher, H., Howarth, R. W., Hedin, L. O., … Mason, M. F. (1999). Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochemical Cycles, 13, 623-645.
Cloern, J., Krantz, T., & Duffy, J. E. (2007). Eutrophication. In J. Cloern (Ed.), Encyclopedia of Earth. Washington DC, USA: Environmental Information Coalition, National Council for Science and the Environment. Retrieved from http://www.eoearth.org/article/Eutrophication
Crosby, G. T. (1972). Spread of the Cattle Egret in the Western Hemisphere. Bird-Banding, 43, 205-212.
Cuesta-Santos, O., Ortiz-Bulto, P. L., & González, M. L. (1998). Deposition and atmospheric nitrogen concentrations trends in Cuba. Water, Air, Soil Pollution, 106, 163-169.
Denis, D. (2001). Dinámica metapoblacional en las colonias de garzas (Aves: Ardeidae) de la ciénaga de Biramas, Cuba. Journal of Caribbean Ornithology, 16(1), 35-44.
Denis, D. (2006). Aves en los manglares: la complejidad de su reproducción. Capítulo IV. En L. Mugica (Ed.), Aves acuáticas en los humedales de Cuba (pp. 66-93). La Habana, Cuba: Editorial Científico-Técnica.
Denis, D. (2011). Patrones de crecimiento postnatal en ocho especies de garzas (Aves: Ardeidae). Revista de Biología Tropical, 59(2), 771-787.
Denis, D. (2015). Modelación matemática del consumo de energía y biomasa durante el crecimiento postnatal en garzas (Aves: Ardeidae). Poeyana, 501, 49-56.
Denis, D. (2016). Diferencias morfométricas entre pichones hermanos en siete especies de garzas (Aves: Ardeidae) en la ciénaga de Birama, Cuba. Revista Cubana de Ciencias Biológicas, 4(3), 67-75.
Denis, D., & Rodríguez-Ochoa, A. (2017). Modelación matemática del consumo de presas y el flujo de energía asociado a la reproducción de Rostrhamus sociabilis (Aves: Falconiformes). Animal Biodiversity and Conservation, 40(2), 221-245.
Denis, D., & Alonso, M. (2011). Cronología de la cría de las aves acuáticas y su relación con factores climáticos en la ciénaga de Birama, Cuba. Mesoamericana, 14(1), 35-43.
Denis, D., & Rodríguez, P. (2006). La reproducción de las aves acuáticas coloniales en los manglares de Cuba. En L. Menéndez (Ed.), Ecosistema de manglar en el Archipiélago Cubano: Estudios y experiencias enfocados a su gestión. La Habana, Cuba: Editorial Academia.
Denis, D., Rodríguez, A., Rodríguez, P., & Jiménez, A. (2003). Reproducción de la Garza Ganadera (Bubulcus ibis) en la Ciénaga de Biramas, Cuba. Journal of Caribbean Ornithology, 16(1), 45-54.
Denis, D., Rodríguez, P., Rodríguez, A., Jiménez, A., & Ponce de León, J. L. (2002). Segregación espacio-temporal en varias colonias de garzas (Aves: Ardeidae) en la ciénaga de Birama, Cuba. En J. J. Neiff (Ed.), Humedales de Iberoamérica (pp. 204-210). CYTED- Programa Iberoamericano de Ciencia y Tecnología para el Desarrollo- Subprograma XVIII, Red Iberoamericana de Humedales.
Denis, D., Rodríguez, P., Rodríguez, A., & Torrella, L. (2006). Evaluación del efecto del disturbio de los investigadores sobre la reproducción en tres especies de garzas coloniales (Aves: Ardeidae). Biología, 20(1-2), 70-72.
Denis, D., Olavarrieta, U., & Andraca, L. (2008). Actualización de la constante de Hoyt para el cálculo del volumen de los huevos en garzas cubanas (Aves: Ciconiiformes). Biología, 22(1-2), 75-77.
Denis, D., Mugica, L., Acosta, M., & Torrella, L. (1999). Nuevos reportes sobre la época reproductiva de aves acuáticas coloniales en Cuba. El Pitirre, 12(1), 7-9.
Drent, R. H. & Daan, S. (1980). The prudent parent: energetic adjustments in avian breeding. Ardea, 68, 225-252.
Dusi, J. L., Dusi, R. T., Bateman, D. L., McDonald, C. A., Stuart, J. J., & Dismukes, J. F. (1971). Ecological impacts of wading birds on the aquatic environment. Alabama, USA: AU Water Resources Center.
Dusi, J. L., & Dusi, R. T. (1970). Nesting success and mortality of nestlings in a Cattle Egret colony. Wilson Bulletin, 82, 458-460.
Ellis, H. I., & Gabrielsen, G. W. (2002). Energetics of Free-Ranging Seabirds. In E. A. Schreiber & J. Burger (Eds.), Biology of marine birds (pp. 359-408). Florida, USA: CRC Press.
Emlen, J. M. (1966). The role of time and energy in food preference. The American Naturalist, 100(916), 611-617.
Emlen, J. M. (1968). Optimal choice in animals. The American Naturalist, 102(926), 385-389.
Fasola, M., Rosa, P., & Canova, L. (1993). The diets of squacco herons, little egrets, night, purple and grey herons in their Italian breeding ranges. Revue d'Ecologie (La Terre et la Vie), 48, 35-47.
Fogarty, M. J., & Hetrick, W. M. (1973). Summer foods of Cattle Egrets in north central Florida. Auk, 90, 268-280.
Forbes, L. S. (1989). Coloniality in herons: Lack’s predation hypothesis reconsidered. Colonial Waterbirds, 12, 24-29.
Fortes, H., & Denis, D. (2013). Reproducción del Gavilán Caracolero Rostrhamus sociabilis (Aves: Falconiformes) en dos humedales de Cuba. Journal of Caribean Ornithology, 26, 1-7.
Frederick, P. C., & Powell, G. V. N. (1994). Nutrient transport by wading birds in the Everglades. In S. Davis, & J. C. Ogden (Eds.), Everglades: the ecosystem and its restoration (pp. 571-584). Florida, USA: St. Lucie Press.
Golovkin, A. N., & Garkavaya, G. P. (1975). Fertilization of waters off the Murrnansk coast by bird excreta near various types of colonies. Russian Journal of Marine Biology, 15, 345-351.
Hanebrink, E. L. (1971). Food, feeding behavior and extension of range by the Cattle Egret. The Migrant - The Tennessee Ornithological Society, 42, 49-53.
Hansell, M. (2000). Bird nests and construction behaviour. Cambridge, UK: Cambridge University Press.
Horton, T. (1999, April). Great Blues are Going Great Guns. Smithsonian Magazine, 130-140. Retrieved from https://www.smithsonianmag.com/science-nature/great-blues-are-going-great-guns-67331912
Hoyt, D. (1979). Practical methods of estimating volume and fresh weight of bird eggs. Auk, 103, 613-617.
Jenni, D. A. (1973). Regional variation in the food of nestling Cattle Egrets. Auk, 90, 821-826.
Jiménez, A., & Denis, D. (2009). Nestling diet of five species of herons and egrets in Birama´s swamp, Cuba. Journal of Caribbean Ornithology, 22, 26-31
Jiménez, A., García-Lau, I., González, A., Mugica, L., & Acosta, M. (2014). Valores de masa corporal de 183 especies de aves cubanas. Revista Cubana de Ciencias Biológicas, 3(1), 22-42.
Jonas, R. B., & Tuttle, J. H. (1990). Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Applied and Environmental Microbiology, 56(3), 747-757.
Jordan, T. E., & Weller, D. E. (1996). Human contributions to terrestrial nitrogen flux. BioScience, 46(9), 655-664.
Kahl, M. P. (1962). Bioenergetics of growth in nestling Wood Storks. Condor, 64, 169-183.
Kendeigh, S. C., Dol'nik, V. R., & Govrilov, V. M. (1977). Avian energetics. In J. Pinowski & S. C. Kendeigh (Eds.), Granivorous birds in ecosystems (pp. 129-205). Massachusetts, USA: Cambridge University Press.
King, J. R. (1974). Seasonal allocation of time and energy resources in birds. In R. A. Jr. Paynter (Ed.), Avian energetics (pp. 4-85). Massachusetts, USA: Nuttal Ornithological Club.
Klein, M. L. (1993). Waterbird behavioral responses to human disturbances. Wildlife Society Bulletin, 21, 31-39.
Kushlan, J. A. (1977). Growth energetics of White Ibises. Condor, 79, 31-36.
Kushlan, J. A., Voorhees, S. A., Loftus, W. F., & Frohring, P. C. (1986). Length, mass and caloric relationships of everglades animals. Florida Scientist, 49(2), 65-79.
Lack, D. (1968). Ecological adaptation for breeding in birds. London, UK: Chapman and Hall.
Madenjlwc, C. P., & Gabrey, S. W. (1995). Waterbird predation on fish in western lake Erie: a bioenergetics model application. The Condor, 97, 141-153.
Mainwaring, M. C., & Hartley, I. R. (2013). The energetic costs of nest building in birds. Avian Biology Research, 6(1), 12-17.
Martin, N. L., Cabrera, L., Ordunas, L., Vila, M., & Iglesias, B. (1967). The Cattle Egret-the bird of major importance for the agricultural economy of the country. Academia de Ciencias de Cuba. Museo “Felipe Poey,” Havana. Trabajos de Divulgación, 42, 1-4.
Master, T. L., Frankel, M., & Russell, M. (1993). Benefits of foraging in mixed-species wader aggregations in a southern New Jersey saltmarsh. Colonial Waterbirds, 16(2), 149-157.
McKechnie, A. E., & Wolf, B. O. (2004). The allometry of avian basal metabolic rate: good predictions need good data. Physiological and Biochemical Zoology, 77(3), 502-521.
Menéndez, L., & Guzmán, J. M. (2006). Ecosistema de manglar en el Archipiélago Cubano: Estudios y experiencias enfocados a su gestión. La Habana, Cuba: Edit. Academia.
Menéndez, L., González, A. V., Guzmán, J. M., Rodríguez, L. F., Capote, R. P., Gómez, R., … Jiménez, Y. (2000). Informe de proyecto de investigación: Bases ecológicas para la restauración de manglares en áreas seleccionadas del archipiélago cubano y su relación con los cambios globales. Informe final de proyecto. Programa Nacional de Cambios Globales y Evolución del Medio Ambiente Cubano. IES. CITMA.
Mock, D. W., Lamey, T. C., & Ploger, B. J. (1987). Proximate and ultimate roles of food amount in regulating egret sibling aggression. Ecology, 68(6), 1760-1772.
Mooij, W. M., Bennetts, R. E., Kitchens, W. M., & DeAngelis, D. L. (2002). Exploring the effect of drought extent and interval on the Florida snail kite: interplay between spatial and temporal scales. Ecological Modeling, 149, 25-39.
Morales, G., & Pacheco, J. (1986). Effects of diking of a Venezuelan savanna on avian habitat, on species diversity, energy flow, and mineral flow through wading birds. Colonial Waterbirds, 9(2), 236-242.
Mullers, R. H. E., Navarro, R. A., Daan, S., Tinbergen, J. M., & Meijer, H. A. J. (2009). Energetic costs of foraging in breeding Cape gannets Morus capensis. Marine Ecology Progress Series, 393, 161-171.
Nagy, K. A. (1987). Field metabolic rate and food requirement scaling in mammals and birds. Ecological Monographs, 57, 111-128.
Nemeth, E., Bossew, P., & Plutzar, C. (2005). A distance-dependent estimation of foraging ranges of neighbouring bird colonies. Ecological Modelling, 182(1), 67-73
Onuf, C. P., Teal, J. M., & Valiela, T. (1977). Interaction of nutrients, plant growth and herbivory in a mangrove ecosystem. Ecology, 58, 514-526.
Orians, G. H. (1961). The ecology of blackbird (Agelaius) social systems. Ecological Monographs, 31(3), 285-312.
Orians, G. H. (1969). On the evolution of mating systems in birds and mammals. The American Naturalist, 103(934), 589-603.
Powell, G. V. N., Fourqurean, J., Kenworthy, V. J., & Zieman, J. C. (1991). Bird colonies cause seagrass enrichment in a subtropical estuary: Observational and experimental evidence. Estuarine, Coastal and Shelf Science, 32, 567-579.
Powell, G. V. N., & Powell, A. H. (1986). Reproduction by Great White Herons Ardea herodias in Florida Bay as an Indicator of Habitat Quality. Biological Conservation, 36, 101-113.
Ranglack, G. S., Argus, R. A., & Marion, K. R. (1991). Physical and temporal factors influencing breeding success of Cattle Egrets (Bubulcus ibis) in a West Alabama Colony. Colonial Waterbirds, 14, 140-149.
Recher, H. F., & Recher, J. A. (1969). Comparative foraging efficiency of adult and immature Little Blue Herons (Florida caerulea). Animal Behavior, 17, 320-322.
Ricklefs, R. E. (1983). Avian postnatal development. In D. S. Farner, J. R. King, & K. C. Parkes (Eds), Avian biology (pp. 1-83). New York, USA: Academic Press.
Ricklefs, R. E., & Hussell, D. T. (1984). Changes in adult mass associated with the nesting cycle in the European Starling. Ornis Scandinavica, 15, 155-161.
Rodgers, J. A. (1987). Breeding chronology and reproductive success of Cattle Egrets and Little Blue Herons on the west coast of Florida, USA. Colonial Waterbirds, 10, 38-44.
Rodgers, J. A. (1979). Breeding behavior and ecology of Little Blue Herons and communicatory trends in the Ardeidae (Ph.D. dissertation). Univ. of South Florida, Tampa.
Shanholtzer, G. F (1972). Range expansion dynamics of the Cattle Egret (Doctor dissertation). University Georgia, Athens, USA.
Siegfried, W. R. (1972). Breeding success and reproductive output of the Cattle Egret. Ostrich, 43, 43-55.
Siegfried, W. R. (1969). Energy metabolism of the Cattle Egret. African Zoology, 4, 265-273.
Siegfried, W. R. (1973). Food requirements and growth of Cattle Egrets in South Africa. Living Bird, 11, 193-206.
Smil, V. (1999). Nitrogen in crop production: an account of global flows. Global Biochemical Cycles, 13, 647-662.
Smith, W. J. (1958). Cattle Egret (Bubulcus ibis) nesting in Cuba. Auk, 75(1), 89.
Stanley, T. R. (2002). How many kilojoules does a Black-billed Magpie nest cost? Journal of Field Ornithology, 73(3), 292-297.
Stinner, D. H. (1983). Colonial wading birds and nutrient cycling in the Okefenokee Swamp ecosystem (Doctor dissertation). University Georgia, Athens, USA.
Telfair, R. C. (1983). The Cattle Egret: A Texas focus and world view. Texas, USA: The Kleberg Studies in Natural Resources.
Telfair, R. C. (1993). Cattle Egret (Bubulcus ibis) population trends and dynamics in Texas (1954-1990). Austin, Texas, USA: Nongame and Urban Program, Fish & Wildlife Division, Texas Parks & Wildlife Department.
Ward, P., & Zahavi, A. (1973). The importance of certain assemblages of birds as "information centres" for finding food. Ibis, 115, 517-534.
Werschkul, D. F. (1977). Changes in a southeastern heronry. Oriole, 42, 5-10.
Weseloh, D. V., & Casselman, J. M. (1992). Fish consumption by double-crested cormorants on Lake Ontario. Burlington, Canada: Canadian Wildlife Service.
Wiese, J. H. (1978). Heron nest-site selection and its ecological effects. In A. Sprunt, J. C. Ogden, & S. Winckler (Eds.), Wading birds (pp. 27-34). New York, USA: National Audubon.
Williams, J. B. (1996). Energetics of avian incubation (Cap. 11). In C. Carey (Ed.), Avian energetics and nutritional ecology (pp. 375-416). London, UK: Chapman & Hall.
Wolff, W. F. (1994). An individual-oriented model of a wading bird nesting colony. Ecological Modelling, 72(1-2), 75-114.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2019 Dennis Denis, Emerio Alejandro Curbelo, Yarelys Ferrer-Sánchez