Prey amino acid composition affects rates of protein synthesis and N wastage of a freshwater carnivore
Georgia K. Dwyer A B E , Rick J. Stoffels C D , Ewen Silvester B and Gavin N. Rees
C
+ Author Affiliations
- Author Affiliations
A Centre for Regional and Rural Futures, Deakin University, Locked Bag 20000, Geelong, Vic. 3220, Australia.
B Department of Ecology, Environment and Evolution, La Trobe University, PO Box 821, Wodonga, Vic. 3690, Australia.
C CSIRO Land and Water, PO Box 821, Wodonga, Vic. 3690, Australia.
D National Institute of Water and Atmospheric Research, PO Box 8602, Riccarton, Christchurch, 8440, New Zealand.
E Corresponding author. Email: g.dwyer@deakin.edu.au
Marine and Freshwater Research 71(2) 229-237 https://doi.org/10.1071/MF18410
Submitted: 17 August 2018 Accepted: 29 July 2019 Published: 23 October 2019
Abstract
Humans modify prey communities and hence alter the availability of nutrients to wild carnivores. Such changes in amino acid ‘landscapes’ are likely to affect the growth of individuals, and potentially the success of populations. This study aimed to determine whether amino acid composition of animal prey alone affects protein synthesis efficiency and N wastage of a freshwater carnivore. River blackfish (Gadopsis marmoratus) were fed two diets differing only in amino acid composition: the first diet was formulated to match the composition of the fish themselves, representing a balanced ‘ideal protein’, whereas the second diet was produced to match the composition of a prey item, namely the shrimp Macrobrachium australiense. By measuring the postprandial increase in metabolic rate (specific dynamic action) and ammonia excretion, it was found that the amino acid composition of the fish diet was associated with an increase in protein synthesis, whereas the shrimp diet doubled the amount of dietary amino acids directed to pathways of catabolic energy production and N wastage. This study adds to the stoichiometric ecology literature by showing that changes in the amino acid composition of food webs could affect carnivore growth and nutrient cycling.
Additional keywords: diet, digestive energetics, energetic cost, metabolic rate, nutrient cycling, postprandial metabolism, specific dynamic action.
References
Alegbeleye, W. O., Obasa, S. O., Olude, O. O., Otubu, K., and Jimoh, W. (2012). Preliminary evaluation of the nutritive value of the variegated grasshopper (Zonocerus variegatus L.) for African catfish Clarias gariepinus (Burchell. 1822) fingerlings. Aquaculture Research 43, 412–420.| Preliminary evaluation of the nutritive value of the variegated grasshopper (Zonocerus variegatus L.) for African catfish Clarias gariepinus (Burchell. 1822) fingerlings.Crossref | GoogleScholarGoogle Scholar |
Allen-Ankins, S., and Stoffels, R. J. (2017). Contrasting fundamental and realized niches: two fishes with similar thermal performance curves occupy different thermal habitats. Freshwater Science 36, 635–652.
| Contrasting fundamental and realized niches: two fishes with similar thermal performance curves occupy different thermal habitats.Crossref | GoogleScholarGoogle Scholar |
Andrade, D. V., De Toledo, L. F., Abe, A. S., and Wang, T. (2004). Ventilatory compensation of the alkaline tide during digestion in the snake Boa constrictor. The Journal of Experimental Biology 207, 1379–1385.
| Ventilatory compensation of the alkaline tide during digestion in the snake Boa constrictor.Crossref | GoogleScholarGoogle Scholar | 15010489PubMed |
Barroso, F. G., de Haro, C., Sánchez-Muros, M.-J., Venegas, E., Martínez-Sánchez, A., and Pérez-Bañón, C. (2014). The potential of various insect species for use as food for fish. Aquaculture 422–423, 193–201.
| The potential of various insect species for use as food for fish.Crossref | GoogleScholarGoogle Scholar |
Borsook, H., and Dubnoff, J. (1943). The metabolism of proteins and amino acids. Annual Review of Biochemistry 12, 183–204.
| The metabolism of proteins and amino acids.Crossref | GoogleScholarGoogle Scholar |
Brown, C. R., and Cameron, J. N. (1991). The induction of specific dynamic action in channel catfish by infusion of essential amino acids. Physiological Zoology 64, 276–297.
| The induction of specific dynamic action in channel catfish by infusion of essential amino acids.Crossref | GoogleScholarGoogle Scholar |
Brucet, S., Boix, D., López-Flores, R., Badosa, A., and Quintana, X. D. (2005). Ontogenic changes of amino acid composition in planktonic crustacean species. Marine Biology 148, 131–139.
| Ontogenic changes of amino acid composition in planktonic crustacean species.Crossref | GoogleScholarGoogle Scholar |
Chabot, D. (2009). Comparison of a commercial and three experimental diets for their effects on the SDA characteristics of Atlantic cod, Gadus morhua. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 153, S140.
| Comparison of a commercial and three experimental diets for their effects on the SDA characteristics of Atlantic cod, Gadus morhua.Crossref | GoogleScholarGoogle Scholar |
Chabot, D., Koenker, R., and Farrell, A. (2016). The measurement of specific dynamic action in fishes. Journal of Fish Biology 88, 152–172.
| The measurement of specific dynamic action in fishes.Crossref | GoogleScholarGoogle Scholar | 26768974PubMed |
Coulson, R. A., and Hernandez, T. (1979). Increase in metabolic rate of the alligator fed proteins or amino acids. The Journal of Nutrition 109, 538–550.
| Increase in metabolic rate of the alligator fed proteins or amino acids.Crossref | GoogleScholarGoogle Scholar | 430258PubMed |
Dwyer, G. K., Stoffels, R. J., and Pridmore, P. A. (2014). Morphology, metabolism and behaviour: responses of three fishes with different lifestyles to acute hypoxia. Freshwater Biology 59, 819–831.
| Morphology, metabolism and behaviour: responses of three fishes with different lifestyles to acute hypoxia.Crossref | GoogleScholarGoogle Scholar |
Dwyer, G. K., Stoffels, R. J., Rees, G. N., Shackleton, M., and Silvester, E. (2018). A predicted change in the amino acid landscapes available to freshwater carnivores. Freshwater Science 37, 108–120.
| A predicted change in the amino acid landscapes available to freshwater carnivores.Crossref | GoogleScholarGoogle Scholar |
El-Sayed, A. F. (1998). Total replacement of fish meal with animal protein sources in Nile tilapia, Oreochromis niloticus (L.), feeds. Aquaculture Research 29, 275–280.
| Total replacement of fish meal with animal protein sources in Nile tilapia, Oreochromis niloticus (L.), feeds.Crossref | GoogleScholarGoogle Scholar |
Finke, M. D. (2013). Complete nutrient content of four species of feeder insects. Zoo Biology 32, 27–36.
| Complete nutrient content of four species of feeder insects.Crossref | GoogleScholarGoogle Scholar | 22689347PubMed |
Fountoulakis, M., and Lahm, H.-W. (1998). Hydrolysis and amino acid composition analysis of proteins. Journal of Chromatography – A 826, 109–134.
| Hydrolysis and amino acid composition analysis of proteins.Crossref | GoogleScholarGoogle Scholar | 9917165PubMed |
Furuya, W. M., Graciano, T. S., Vidal, L. V. O., Xavier, T. O., Gongora, L. D., Righetti, J. S., and Furuya, V. R. B. (2012). Digestible lysine requirement of Nile tilapia fingerlings fed arginine–tolysine-balanced diets. Revista Brasileira de Zootecnia 41, 485–490.
| Digestible lysine requirement of Nile tilapia fingerlings fed arginine–tolysine-balanced diets.Crossref | GoogleScholarGoogle Scholar |
Gietzen, D. W., and Aja, S. M. (2012). The brain’s response to an essential amino acid-deficient diet and the circuitous route to a better meal. Molecular Neurobiology 46, 332–348.
| The brain’s response to an essential amino acid-deficient diet and the circuitous route to a better meal.Crossref | GoogleScholarGoogle Scholar | 22674217PubMed |
Gómez-Requeni, P., Mingarro, M., Calduch-Giner, J., Médale, F., Martin, S., Houlihan, D., Kaushik, S., and Pérez-Sánchez, J. (2004). Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232, 493–510.
| Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata).Crossref | GoogleScholarGoogle Scholar |
Grandison, R. C., Piper, M. D., and Partridge, L. (2009). Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061–1064.
| Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila.Crossref | GoogleScholarGoogle Scholar | 19956092PubMed |
Green, J., and Hardy, R. (2008). The effects of dietary protein: energy ratio and amino acid pattern on nitrogen utilization and excretion of rainbow trout Oncorhynchus mykiss (Walbaum). Journal of Fish Biology 73, 663–682.
| The effects of dietary protein: energy ratio and amino acid pattern on nitrogen utilization and excretion of rainbow trout Oncorhynchus mykiss (Walbaum).Crossref | GoogleScholarGoogle Scholar |
Helland, S., Terjesen, B. F., and Berg, L. (2003). Free amino acid and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana. Aquaculture 215, 213–228.
| Free amino acid and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana.Crossref | GoogleScholarGoogle Scholar |
Holt, G. J. (2011). ‘Larval Fish Nutrition.’ (Wiley: Chichester, UK)
Jabir, M. A. R., Jabir, S. A. R., and Vikineswary, S. (2012). Nutritive potential and utilization of super worm (Zophobas morio) meal in the diet of Nile tilapia (Oreochromis niloticus) juvenile. African Journal of Biotechnology 11, 6592–6598.
Jobling, M. (1985). Growth. In ‘Fish Energetics: New Perspectives’. (Eds P. Tytler and P. Calow.) pp. 213–230. (Croom Helm: London, UK.)
Kaushik, S. J., and Seiliez, I. (2010). Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquaculture Research 41, 322–332.
| Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs.Crossref | GoogleScholarGoogle Scholar |
Koehnle, T. J., Russell, M. C., and Gietzen, D. W. (2003). Rats rapidly reject diets deficient in essential amino acids. The Journal of Nutrition 133, 2331–2335.
| Rats rapidly reject diets deficient in essential amino acids.Crossref | GoogleScholarGoogle Scholar | 12840202PubMed |
Kolmakova, A. A., Gladyshev, M. I., Kalachova, G. S., Kravchuk, E. S., Ivanova, E. A., and Sushchik, N. N. (2013). Amino acid composition of epilithic biofilm and benthic animals in a large Siberian river. Freshwater Biology 58, 2180–2195.
| Amino acid composition of epilithic biofilm and benthic animals in a large Siberian river.Crossref | GoogleScholarGoogle Scholar |
Li, P., Mai, K., Trushenski, J., and Wu, G. (2009). New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37, 43–53.
| New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds.Crossref | GoogleScholarGoogle Scholar | 18751871PubMed |
Lintermans, M. (2007). ‘Fishes of the Murray–Darling Basin.’ (Murray–Darling Basin Commission: Canberra, ACT, Australia.)
Lyndon, A., Houlihan, D., and Hall, S. (1992). The effect of short-term fasting and a single meal on protein synthesis and oxygen consumption in cod, Gadus morhua. Journal of Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 162, 209–215.
| The effect of short-term fasting and a single meal on protein synthesis and oxygen consumption in cod, Gadus morhua.Crossref | GoogleScholarGoogle Scholar | 1377211PubMed |
McCue, M., Bennett, A., and Hicks, J. (2005). The effect of meal composition on specific dynamic action in Burmese pythons (Python molurus). Physiological and Biochemical Zoology 78, 182–192.
| The effect of meal composition on specific dynamic action in Burmese pythons (Python molurus).Crossref | GoogleScholarGoogle Scholar | 15778938PubMed |
McIntyre, P. B., and Flecker, A. S. (2010). Ecological stoichiometry as an integrative framework in stream fish ecology. In ‘Community Ecology of Stream Fishes: Concepts, Approaches, and Techniques. American Fisheries Society Symposium 73’, 19–20 August 2008, Ottawa, ON, Canada. (Eds K. B. Gido and D. A. Jackson.) pp. 539–558. (American Fisheries Society: Bethesda, MD, USA.)
Moody, E. K., Corman, J. R., Elser, J. J., and Sabo, J. L. (2015). Diet composition affects the rate and N : P ratio of fish excretion. Freshwater Biology 60, 456–465.
| Diet composition affects the rate and N : P ratio of fish excretion.Crossref | GoogleScholarGoogle Scholar |
Morosinotto, C., Villers, A., Varjonen, R., and Korpimäki, E. (2017). Food supplementation and predation risk in harsh climate: interactive effects on abundance and body condition of tit species. Oikos 126, 863–873.
| Food supplementation and predation risk in harsh climate: interactive effects on abundance and body condition of tit species.Crossref | GoogleScholarGoogle Scholar |
Murphy, M. E., and Pearcy, S. D. (1993). Dietary amino acid complementation as a foraging strategy for wild birds. Physiology & Behavior 53, 689–698.
| Dietary amino acid complementation as a foraging strategy for wild birds.Crossref | GoogleScholarGoogle Scholar |
Nakagaki, B., Sunde, M., and DeFoliart, G. (1987). Protein quality of the house cricket, Acheta domesticus, when fed to broiler chicks. Poultry Science 66, 1367–1371.
| Protein quality of the house cricket, Acheta domesticus, when fed to broiler chicks.Crossref | GoogleScholarGoogle Scholar |
Onifade, A., Oduguwa, O., Fanimo, A., Abu, A., Olutunde, T., Arije, A., and Babatunde, G. (2001). Effects of supplemental methionine and lysine on the nutritional value of housefly larvae meal (Musca domestica) fed to rats. Bioresource Technology 78, 191–194.
| Effects of supplemental methionine and lysine on the nutritional value of housefly larvae meal (Musca domestica) fed to rats.Crossref | GoogleScholarGoogle Scholar | 11333040PubMed |
Österblom, H., Olsson, O., Blenckner, T., and Furness, R. W. (2008). Junk-food in marine ecosystems. Oikos 117, 967–977.
| Junk-food in marine ecosystems.Crossref | GoogleScholarGoogle Scholar |
Pörtner, H. O., and Knust, R. (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97.
| Climate change affects marine fishes through the oxygen limitation of thermal tolerance.Crossref | GoogleScholarGoogle Scholar | 17204649PubMed |
Rolland, M., Larsen, B. K., Holm, J., Dalsgaard, J., and Skov, P. V. (2015). Effect of plant proteins and crystalline amino acid supplementation on postprandial plasma amino acid profiles and metabolic response in rainbow trout (Oncorhynchus mykiss). Aquaculture International 23, 1071–1087.
| Effect of plant proteins and crystalline amino acid supplementation on postprandial plasma amino acid profiles and metabolic response in rainbow trout (Oncorhynchus mykiss).Crossref | GoogleScholarGoogle Scholar |
Sandblom, E., Gräns, A., Axelsson, M., and Seth, H. (2014). Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20141490.
| Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future.Crossref | GoogleScholarGoogle Scholar |
Saravanan, S., Geurden, I., Figueiredo-Silva, A. C., Nusantoro, S., Kaushik, S., Verreth, J., and Schrama, J. W. (2013). Oxygen consumption constrains food intake in fish fed diets varying in essential amino acid composition. PLoS One 8, e72757.
| Oxygen consumption constrains food intake in fish fed diets varying in essential amino acid composition.Crossref | GoogleScholarGoogle Scholar | 23991148PubMed |
Stoffels, R. J. (2015). Physiological trade-offs along a fast-slow lifestyle continuum in fishes: what do they tell us about resistance and resilience to hypoxia? PLoS One 10, e0130303.
| Physiological trade-offs along a fast-slow lifestyle continuum in fishes: what do they tell us about resistance and resilience to hypoxia?Crossref | GoogleScholarGoogle Scholar | 26070078PubMed |
Tacon, A. G. (1995). Feed ingredients for carnivorous fish species: alternatives to fishmeal and other fishery resources. In ‘Sustainable Fish Farming’. (Eds H. Reinertsen and H. Haaland.) pp. 89–114. (A.A. Balkema: Rotterdam, Netherlands.)
Thor, P., Cervetto, G., Besiktepe, S., Ribera-Maycas, E., Tang, K. W., and Dam, H. G. (2002). Influence of two different green algal diets on specific dynamic action and incorporation of carbon into biochemical fractions in the copepod Acartia tonsa. Journal of Plankton Research 24, 293–300.
| Influence of two different green algal diets on specific dynamic action and incorporation of carbon into biochemical fractions in the copepod Acartia tonsa.Crossref | GoogleScholarGoogle Scholar |
Trites, A. W., Miller, A. J., Maschner, H. D., Alexander, M. A., Bograd, S. J., Calder, J. A., Capotondi, A., Coyle, K. O., Lorenzo, E. D., and Finney, B. P. (2007). Bottom-up forcing and the decline of Steller sea lions (Eumetopias jubatus) in Alaska: assessing the ocean climate hypothesis. Fisheries Oceanography 16, 46–67.
| Bottom-up forcing and the decline of Steller sea lions (Eumetopias jubatus) in Alaska: assessing the ocean climate hypothesis.Crossref | GoogleScholarGoogle Scholar |
Vahl, O. (1984). The relationship between specific dynamic action (SDA) and growth in the common starfish, Asterias rubens L. Oecologia 61, 122–125.
| The relationship between specific dynamic action (SDA) and growth in the common starfish, Asterias rubens L.Crossref | GoogleScholarGoogle Scholar | 28311394PubMed |
Vanni, M. J. (2002). Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33, 341–370.
| Nutrient cycling by animals in freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar |
Wood, C. M., de Souza Netto, J. G., Wilson, J. M., Duarte, R. M., and Val, A. L. (2017). Nitrogen metabolism in tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia. Journal of Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 187, 135–151.
| Nitrogen metabolism in tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia.Crossref | GoogleScholarGoogle Scholar | 27530913PubMed |
Wu, G., Bazer, F. W., Dai, Z., Li, D., Wang, J., and Wu, Z. (2014). Amino acid nutrition in animals: protein synthesis and beyond. Annual Review of Animal Biosciences 2, 387–417.
| Amino acid nutrition in animals: protein synthesis and beyond.Crossref | GoogleScholarGoogle Scholar | 25384149PubMed |
