Energetic and health effects of protein overconsumption constrain dietary adaptation in an apex predator
1.Fuller, A. et al. Physiological mechanisms in coping with climate change. Phys. Biochem. Zool. 83, 713–720. https://doi.org/10.1086/652242 (2010).Article
Google Scholar
2.Raubenheimer, D., Simpson, S. J. & Tait, A. H. Match and mismatch: Conservation physiology, nutritional ecology and the timescales of biological adaptation. Philos. Trans. R. Soc. B 367, 1628–1646. https://doi.org/10.1098/rstb.2012.0007 (2012).CAS
Article
Google Scholar
3.Tracy, C. R. et al. The importance of physiological ecology in conservation biology. Integr. Comp. Biol. 46, 1191–1205. https://doi.org/10.1093/icb/icl054 (2006).Article
PubMed
Google Scholar
4.Parker, K. L., Barboza, P. S. & Gillingham, M. P. Nutrition integrates environmental responses of ungulates. Funct. Ecol. 23, 57–69. https://doi.org/10.1111/j.1365-2435.2009.01528.x (2009).Article
Google Scholar
5.Morris, J. G. Idiosyncratic nutrient requirements of cats appear to be diet-induced evolutionary adaptations. Nutr. Res. Rev. 15, 153–168. https://doi.org/10.1079/NRR200238 (2002).CAS
Article
PubMed
Google Scholar
6.Hofmann, R. R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia 78, 443–457. https://doi.org/10.1007/BF00378733 (1989).ADS
CAS
Article
PubMed
Google Scholar
7.Rode, K. D., Chapman, C. A., McDowell, L. R. & Stickler, C. Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus Ascanius). Biotropica 38, 625–634. https://doi.org/10.1111/j.1744-7429.2006.00183.x (2006).Article
Google Scholar
8.Birnie-Gauvin, K., Peiman, K. S., Raubenheimer, D. & Cooke, S. J. Nutritional physiology and ecology of wildlife in a changing world. Cons Phys. 5, cox030. https://doi.org/10.1093/conphys/cox030 (2017).CAS
Article
Google Scholar
9.Rode, K. D. & Robbins, C. T. Why bears consume mixed diets during fruit abundance. Can. J. Zool. 78, 1640–1645. https://doi.org/10.1139/z00-082 (2000).Article
Google Scholar
10.Robbins, C. T. et al. Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos 116, 1675–1683. https://doi.org/10.1111/j.0030-1299.2007.16140.x (2007).Article
Google Scholar
11.Erlenbach, J. A., Rode, K. D., Raubenheimer, D. & Robbins, C. T. Macronutrient optimization and energy maximization determine diets of brown bears. J. Mamm. 95, 160–168. https://doi.org/10.1644/13-MAMM-A-161 (2014).Article
Google Scholar
12.Nie, Y. et al. Giant pandas are macronutritional carnivores. Curr. Biol. 29, 1677–1682. https://doi.org/10.1016/j.cub.2019.03.067 (2019).CAS
Article
PubMed
Google Scholar
13.Sponheimer, M., Clauss, M. & Codron, D. Dietary evolution: The panda paradox. Curr. Biol. 29, R417–R419. https://doi.org/10.1016/j.cub.2019.04.045 (2019).CAS
Article
PubMed
Google Scholar
14.Stirling, I. & McEwan, E. H. The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can. J. Zool. 53, 1021–1027. https://doi.org/10.1139/z75-117 (1975).CAS
Article
PubMed
Google Scholar
15.Liu, S. P. et al. Population genomics reveal recent speciation and rapid evolutionary adaptation in Polar Bears. Cell 157, 785–794. https://doi.org/10.1016/j.cell.2014.03.054 (2014).CAS
Article
PubMed
PubMed Central
Google Scholar
16.Kohl, K. D., Coogan, S. C. P. & Raubenheimer, D. Do wild carnivores forage for prey or for nutrient? Evidence for nutrient-specific foraging in vertebrate predators. BioEssays 37, 701–709. https://doi.org/10.1002/bies.201400171 (2015).Article
PubMed
Google Scholar
17.Machovsky-Capuska, G. E. & Raubenheimer, D. The nutritional ecology of marine apex predators. Ann. Rev. Mar. Sci. 12, 361–387. https://doi.org/10.1146/annurev-marine-010318-095411 (2020).Article
PubMed
Google Scholar
18.Hewson-Hughes, A. K., Colyer, A., Simpson, S. J. & Raubenheimer, D. Balancing macronutrient intake in a mammalian carnivore: Disentangling the influences of flavor and nutrition. R. Soc. Open 3, 160081. https://doi.org/10.1098/rsos.160081 (2016).ADS
CAS
Article
Google Scholar
19.McKinney, M. A., Atwood, T. C., Iverson, S. J. & Peacock, E. Temporal complexity of southern Beaufort Sea polar bear diets during a period of increasing land use. Ecosphere 8, e01633. https://doi.org/10.1002/ecs2.1633 (2017).Article
Google Scholar
20.Rode, K. D. et al. Spring fasting behavior in a marine apex predator provides an index of ecosystem productivity. Glob. Change Biol. 24, 410–423. https://doi.org/10.1111/gcb.13933 (2018).ADS
Article
Google Scholar
21.Rode, K. D. et al. Variation in the response of an arctic top predator experiencing habitat loss: Feeding and reproductive ecology of two polar bear populations. Glob. Change Biol. 20, 76–88. https://doi.org/10.1111/gcb.12339 (2014).ADS
Article
Google Scholar
22.Rode, K. D. et al. Seal body condition and atmospheric circulation patterns in the Chukchi Sea influence polar bear body condition, recruitment, and feeding ecology. Glob. Change Biol. https://doi.org/10.1111/gcb.15572 (2021).Article
Google Scholar
23.Yurkowski, D. J., Hussey, N. E., Semeniuk, C., Ferguson, S. H. & Fisk, A. T. Effects of fat extraction and the utility of fat normalization models on δ13C and δ15N values in Arctic marine mammal tissues. Pol. Biol. 38, 131–143. https://doi.org/10.1007/s00300-014-1571-1 (2014).Article
Google Scholar
24.Hilderbrand, G. V., Jenkins, S. G., Schwartz, C. C., Hanley, T. A. & Robbins, C. T. Effect of seasonal differences in dietary meat intake on changes in body mass and composition in wild and captive brown bears. Can. J. Zool. 77, 1623–1630. https://doi.org/10.1139/z99-133 (1999).Article
Google Scholar
25.McCullough, D. R. & Ullrey, D. E. Proximate mineral and gross energy composition of white-tailed deer. J. Wildl. Manag. 47, 430–441. https://doi.org/10.2307/3808516 (1983).Article
Google Scholar
26.Pritchard, G. T. & Robbins, C. T. Digestive and metabolic efficiencies of grizzly and black bears. Can. J. Zool. 68, 1645–1651. https://doi.org/10.1139/z90-244 (1990).Article
Google Scholar
27.LaDouceur, E. E. B., Garner, M. M., Davis, B. & Tseng, F. A retrospective study of end-stage renal disease in captive polar bears (Ursus maritimus). J. Zoo Wildl. Med. 45, 69–77. https://doi.org/10.1638/2013-0071R.1 (2014).Article
PubMed
Google Scholar
28.Derocher, A. E. & Stirling, I. Aspects of survival in juvenile polar bears. Can. J. Zool. 74, 1246–1252. https://doi.org/10.1139/z96-138 (1996).Article
Google Scholar
29.Hedberg, G. E. et al. Milk composition in free-ranging polar bears (Ursus maritimus) as a model for captive rearing milk formula. Zoo Biol. 30, 550–565. https://doi.org/10.1002/zoo.20375 (2011).CAS
Article
PubMed
Google Scholar
30.Jensen, K. et al. Nutrient-specific compensatory feeding in a mammalian carnivore, the mink, Neovison vison. Br. J. Nutr. 112, 1226–1233. https://doi.org/10.1017/S0007114514001664 (2014).CAS
Article
PubMed
Google Scholar
31.Rosen, D. A. S. & Trites, A. W. Examining the potential for nutritional stress in young Stellar sea lions: Physiological effects of prey composition. J. Comp. Phys. B 175, 265–273. https://doi.org/10.1007/s00360-005-0481-5 (2005).CAS
Article
Google Scholar
32.Kirsch, P. E., Iverson, S. J. & Bowen, W. D. Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Phys. Biochem. Zool. 73, 45–59. https://doi.org/10.1086/316723 (2000).CAS
Article
Google Scholar
33.Zhao, L., Schell, D. M. & Castellini, M. A. Dietary macronutrients influence 13C and 15N signatures of pinnipeds: Captive feeding studies with harbor seals (Phoca vitulina). Physiol. Part A Mol. Integr. Phys. 143, 469–478. https://doi.org/10.1016/j.cbpa.2005.12.032 (2006).CAS
Article
Google Scholar
34.Diaz Gomez, M., Rosen, D. A. S. & Trites, A. W. Net energy gained by northern fur seals (Callorhinus ursinus) is impacted more by diet quality than diet diversity. Can. J. Zool. 94, 12–135. https://doi.org/10.1139/cjz-2015-0143 (2016).CAS
Article
Google Scholar
35.Le Bellego, L., van Milgen, J. & Noblet, J. Effect of high temperature and low-protein diets on performance of growing pigs. J. Anim. Sci. 79, 1259–1271. https://doi.org/10.2527/2001.7951259x (2002).Article
Google Scholar
36.Anton, S. D. et al. Effects of popular diets without specific calorie targets on weight loss outcomes: Systematic review of findings from clinical trials. Nutrients 9, 822. https://doi.org/10.3390/nu9080822 (2017).Article
PubMed Central
Google Scholar
37.Bininda-Emonds, O. R. P., Gittleman, J. L. & Purvis, A. Building large trees by combining phylogenetic information: A complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74, 143–175. https://doi.org/10.1017/S0006323199005307 (1999).CAS
Article
PubMed
Google Scholar
38.Plantinga, E. A., Bosch, G. & Hendriks, W. H. Estimation of the dietary nutrient profile of free-roaming feral cats: Possible implications for nutrition of domestic cats. Br. J. Nutr. 106, S35–S48. https://doi.org/10.1017/S0007114511002285 (2011).CAS
Article
PubMed
Google Scholar
39.Hewson-Hughes, A. K. et al. Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris. Behav. Ecol. 24, 293–304. https://doi.org/10.1093/beheco/ars168 (2013).Article
PubMed
Google Scholar
40.Trites, A. W. & Donnelly, C. P. The decline of Steller sea lions Eumetopias jubatus in Alaska: A review of the nutritional stress hypothesis. Mamm. Rev. 33, 3–28. https://doi.org/10.1046/j.1365-2907.2003.00009.x (2003).Article
Google Scholar
41.Hauser, D. D. W., Allen, C. S., Rich, H. B. Jr. & Quinn, T. P. Resident harbor seals (Phoca vitulina) in Iliamna Lake, Alaska: Summer diet and partial consumption of adult sockeye salmon (Oncorhynchus nerka). Aquat. Mamm. 34, 303–309. https://doi.org/10.1578/AM.34.3.2008.303 (2008).Article
Google Scholar
42.Jia, Y. et al. Long-term high intake of whole proteins results in renal damage in pigs. J. Nutr. 140, 1646–1652. https://doi.org/10.3945/jn.110.123034 (2010).CAS
Article
PubMed
Google Scholar
43.Wakefield, A. P., House, J. D., Ogborn, M. R., Weiler, H. A. & Aukema, H. M. A diet of 35% of energy from protein leads to kidney damage in female Sprague–Dawley rats. Br. J. Nutr. 106, 656–663. https://doi.org/10.1017/S0007114511000730 (2011).CAS
Article
PubMed
Google Scholar
44.Ko, G.-J., Rhee, C. M., Kalantar-Zadeh, K. & Joshi, S. The effects of high-protein diets on kidney health and longevity. J. Am. Soc. Nephrol. 31, 1667–1679. https://doi.org/10.1681/ASN.2020010028 (2020).CAS
Article
PubMed
Google Scholar
45.Bӧswald, L. F., Kienzle, E. & Dobenecker, B. Observation about phosphorus and protein supply in cats and dogs prior to the diagnosis of chronic kidney disease. J. Phys. Anim. Nutr. 102, 31–36. https://doi.org/10.1111/jpn.12886 (2017).CAS
Article
Google Scholar
46.Ioannou, G. N., Morrow, O. B., Connole, M. L. & Lee, S. P. Association between dietary nutrient composition and the incidence of cirrhosis or liver cancer in the united states population. Hepatology 50, 175–184. https://doi.org/10.1002/hep.22941 (2009).CAS
Article
PubMed
Google Scholar
47.Tryland, M. et al. Plasma biochemical values from apparently healthy free-ranging polar bears from Svalbard. J. Wildl. Dis. 38, 566–575. https://doi.org/10.7589/0090-3558-38.3.566 (2002).CAS
Article
PubMed
Google Scholar
48.Thiemann, G. W., Iverson, S. J. & Stirling, I. Polar bear diets and Arctic marine food webs: Insights from fatty acid analysis. Ecol. Monogr. 78, 591–613. https://doi.org/10.1890/07-1050.1 (2008).Article
Google Scholar
49.Ryg, M., Smith, T. G. & Oritsland, N. A. Seasonal changes in body mass and body composition of ringed seals (Phoca hispida) on Svalbard. Can. J. Zool. 68, 470–475. https://doi.org/10.1139/z90-069 (1990).Article
Google Scholar
50.Ferguson, S. H. et al. Demographic, ecological, and physiological responses of ringed seals to an abrupt decline in sea ice availability. Peer J. 5, e2957. https://doi.org/10.7717/peerj.2957 (2017).Article
PubMed
PubMed Central
Google Scholar
51.Atwood, T. C. et al. Rapid environmental change drives increased land use by an Arctic marine predator. PLoS One 11, 30155932. https://doi.org/10.1371/journal.pone.0155932 (2016).ADS
CAS
Article
Google Scholar
52.Molnar, P. K. et al. Fasting season length sets temporal limits for global polar bear persistence. Nat. Clim. Change 10, 732–738. https://doi.org/10.1038/s41558-020-0818-9 (2020).ADS
Article
Google Scholar
53.Rode, K. D., Robbins, C. T., Nelson, L. & Amstrup, S. C. Can polar bears use terrestrial foods to offset lost ice-based hunting opportunities?. Front. Ecol. Environ. 13, 138–145. https://doi.org/10.1890/140202 (2015).Article
Google Scholar
54.McArt, S. H. et al. Summer nitrogen availability as a bottom-up constraint on moose in south-central Alaska. Ecology 90, 1400–1411. https://doi.org/10.1890/08-1435.1 (2009).Article
PubMed
Google Scholar
55.Lahtinen, M., Clinnick, D., Mannermaa, K., Salonen, J. S. & Viranta, S. Excess protein enabled dog domestication during severe Ice Age winters. Sci. Rep. 11, 7. https://doi.org/10.1038/s41598-020-78214-4 (2021).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
56.Regehr, E. V., Hostetter, N. J., Wilson, R. R. & Rode, K. D. Integrated population modeling provides the first empirical estimates of vital rates and abundance for polar bears in the Chukchi Sea. Sci. Rep. 8, 16780. https://doi.org/10.1038/s41598-018-34824-7 (2018).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
57.Crawford, J. A., Quakenbush, L. T. & Citta, J. J. A comparison of ringed seal and bearded seal diet, condition, and productivity between historical (1975–19480 and recent (2003–2012) periods in the Alaskan Bering and Chukchi Seas. Progr. Oceanogr. 136, 133–150. https://doi.org/10.1016/j.pocean.2015.05.011 (2015).ADS
Article
Google Scholar
58.Germain, L. R., McCarthy, M. D., Koch, P. L. & Harvey, J. T. Stable carbon and nitrogen isotopes in multiple tissues of wild and captive harbor seals (Phoca vitulina) off the California coast. Mar. Mamm. Sci. 28, 542–560. https://doi.org/10.1111/j.1748-7692.2011.00516.x (2011).CAS
Article
Google Scholar
59.Erlenbach, J. A. Nutritional and landscape ecology of brown bears (Ursus arctos). PhD dissertation. Washington State University, Pullman, WA, USA (2020).60.Laidre, K. L., Stirling, I., Estes, J. A., Kochnev, A. & Roberts, J. Historical and potential future importance of large whales as food for polar bears. Front. Ecol. Environ. 16, 515–524. https://doi.org/10.1002/fee.1963 (2018).Article
Google Scholar
61.Newsome, S. D., Koch, P. L., Etnier, M. A. & Aurioles-Gamboa, D. Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Mar. Mamm. Sci. 22, 556–572. https://doi.org/10.1111/j.1748-7692.2006.00043.x (2006).Article
Google Scholar
62.Stock, B. C. et al. Analyzing mixing systems using a new generation of Bayesian tracker mixing models. Peer J. 6, e5096. https://doi.org/10.7717/peerj.5096 (2018).Article
PubMed
PubMed Central
Google Scholar
63.Rode, K. D. et al. Isotopic incorporation and the effects of fasting and dietary fat content on isotopic discrimination in large carnivorous mammals. Phys. Biochem. Zool. 89, 182–197. https://doi.org/10.1086/686490 (2016).CAS
Article
Google Scholar
64.Merrill, A. L. & Watt, B. K. Energy Value of Foods: Basis and Derivation, Revised. Agriculture Handbook 74 (United States Department of Agriculture, 1973).65.Dyck, M. G. & Morin, P. In vivo digestibility trials of a captive polar bear (Ursus maritimus) feeding on harp seal (Pagophilus growenlandicus) and Arctic charr (Salvelinus alpinus). Pak. J. Zool. 43, 759–767 (2011).CAS
Google Scholar More