4.4 Implications of resource partitioning among demographic groups
Resource partitioning among demographic groups has important implications for the ecology, evolution, and conservation of a species. Dietary specialization can influence a suite of ecological interactions including the intensity of inter- and intraspecific competition, microhabitat use, and the risk of predation or parasitism. In particular, different mortality risks among demographic groups specializing on different prey taxa could markedly impact the size and demographic structure of a population (Durell, 2000, 2003). For example, certain prey may supply greater nutrition, while others have a lower risk of predation or parasitism. This risk-benefit trade-off could lead to differences in body condition or mortality risk among demographic groups of western sandpipers; however, the implications of dietary specialization are difficult to assess because the physiological processes used to assimilate nutrition from biofilm and differences in predation risk for birds consuming biofilm compared to invertebrates are uncertain. Future studies aimed at understanding the effects of biofilm consumption on body condition and the risk-benefit trade-offs of different diets are warranted.
From an evolutionary perspective, differences in body condition or mortality risk resulting from dietary specialization can impact an individual’s fitness (Bolnick et al., 2003; Durell, 2000). In addition, intraspecific niche variation could subject demographic groups to different selection pressures and facilitate adaptive speciation (Bolnick et al., 2003). However, despite the resource partitioning that we observed in western sandpipers, sympatric speciation appears unlikely in this species because diet composition only differs seasonally, and theoretical models of competitive speciation have demonstrated that niche variation between individuals needs to be relatively large to drive speciation (Dieckmann & Doebeli, 1999).
Resource managers must understand the ecological and evolutionary consequences of resource partitioning among demographic groups to make informed conservation decisions. If a demographic group specializes in foraging within a particular habitat or on particular prey, the loss of that habitat or prey could have a disproportionately negative affect on the demographic group. Although the importance of conserving invertebrate prey for migratory shorebirds has been well-recognized, conservation strategies that target regions of high biofilm production are lacking. For western sandpipers, conservation of biofilm at migratory stopovers as far south as SF Bay appears necessary to support the nutritional demands of all demographic groups.
CONCLUSION
During the non-breeding season, shorebirds rely on adequate prey at wintering and migratory stopover areas to maintain their body condition and prepare for breeding. With high metabolic rates and long migration distances, they must forage on nutrient-dense prey to meet their daily energy requirements. Increased competition for prey during migration, a period of extremely high energy expenditure, could result in age- and sex-related dietary specialization. Our results provide the first evidence that age- and sex-related dietary specialization in western sandpipers facilitates seasonal resource partitioning that would reduce competition during spring at the onset of the breeding migration. Seasonal dietary specialization in western sandpipers is associated with differences in bill length and body mass. Differences among age classes in social status and acquired foraging skills may also play a role. Understanding resource partitioning throughout the annual cycle and among different demographic groups is critical because dietary specialization has important implications for the ecology, evolution, and conservation of a species.
ACKNOWLEDGMENTS
We thank A. Schultz, S. Moskal, M. Iglecia, V. Bui, L. A. Curry, C. Kroeger, C. Yi, A. Loveland, Y. W. Chan, E. Flynn, D. Drolette and T. Mathews for assistance with data collection. We thank C. Strong and J. Albertson at Don Edwards National Wildlife Refuge for site access and logistical support, and USGS Science Coordinator, Michael Chotkowski, for supporting manuscript preparation. Sarah Peterson and three anonymous reviewers provided helpful feedback. This research was supported by the USGS Priority Ecosystems Science Program, The USGS Ecosystems Mission Area, the USGS Western Ecological Research Center, and Grants-in-Aid for Scientific Research (KAKENHI) grant 18H04156 from the Japan Society for the Promotion of Science. Samples were approved by the USGS Western Ecological Research Center Animal Care and Use Committee and collected under USGS Banding Permit 22911 and CDFW Permit SC-004857. Mention of trade names is for descriptive purposes only and does not imply endorsement by the U.S. government.
AUTHORS’ CONTRIBUTIONS
L. A. Hall led the data analysis and manuscript preparation. S. E. W. De La Cruz, I. Woo., and J. Y. Takekawa designed the project, oversaw data collection, and assisted with data analysis, and writing. T. Kuwae assisted with project design, with sample collection, preparation, and analysis, and with writing.
DATA AVAILABILITY
Data from this research are archived at: https://doi.org/XXXXXXXX
REFERENCES
Alves, J. A., Gunnarsson, T. G., Potts, P. M., Sutherland, W. J., & Gill, J. A. (2013). Sex-biases in distribution and resource use at different spatial scales in a migratory shorebird. Ecology and Evolution , 3 (4), 1079–1090. doi: 10.1002/ece3.503
Beninger, P. G., Elner, R. W., Morançais, M., & Decottignies, P. (2011). Downward trophic shift during breeding migration in the shorebird Calidris mauri (western sandpiper). Marine Ecology Progress Series , 428 , 259–269. doi: 10.3354/meps09050
Bishop, M. A., Warnock, N., & Takekawa, J. Y. (2004). Differential spring migration by male and female western sandpipers at interior and coastal stopover sites. Ardea , 92 (2), 185–196.
Bishop, M. A., Warnock, N., & Takekawa, J. Y. (2006). Spring migration patterns in western sandpipers Calidris mauri. In G. C. Boere, C. A. Gailbraith, & D. A. Stroud (Eds.), Waterbirds Around the World: A Global Overview of the Conservation, Management and Resarch of the World’s Waterbird Flyways (pp. 545–550). Edinburgh: The Stationery Office.
Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D., & Forister, M. L. (2003). The ecology of individuals: incidence and implications of individual specialization. American Naturalist , 161 (1), 1–28. doi: 10.1086/343878
Buenrostra, A. A., Warnock, N., & De la Cueva, H. (1999). Wintering western sandpipers Calidris mauri at Estero de Punta Banda, Baja California, México. Bulletin-Wader Study Group , 88 , 59–63.
Burger, J. (1980). Age differences in foraging black-necked stilts in Texas. The Auk , 97 (3), 633–636.
Butler, R. W., Delgado, F. S., De La Cueva, H., Pulido, V., & Sandercock, B. K. (1996). Migration routes of the western sandpiper.The Wilson Bulletin , 108 (4), 662–672.
Butler, R. W., Kaiser, G. W., & Smith, G. E. J. (1987). Migration chronology, length of stay, sex ratio, and weight of western sandpipers, (Calidris mauri ) on the South Coast of British Columbia.Journal of Field Ornithology , 58 (2), 103–111.
Catry, T., Alves, J. A., Gill, J. A., Gunnarsson, T. G., & Granadeiro, J. P. (2012). Sex promotes spatial and dietary segregation in a migratory shorebird during the non-breeding season. PLoS ONE ,7 (3). doi: 10.1371/journal.pone.0033811
Dalerum, F., & Angerbjörn, A. (2005). Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes.Oecologia , 144 (4), 647–658. doi: 10.1007/s00442-005-0118-0
Dieckmann, U., & Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature , 400 (6742), 354–357. doi: 10.1038/22521
Durell, S. E. A. Le V. Dit (2000). Individual feeding specialisation in shorebirds: population consequences and conservation implications.Biological Reviews , 75 (4), 503–518. doi: 10.1111/j.1469-185X.2000.tb00053.x
Durell, S. E. A. Le V. Dit (2003). The implications for conservation of age-and sex-related feeding specializations in shorebirds. Wader Study Group Bulletin , (100), 35–39. Retrieved from http://sora.unm.edu/sites/default/files/journals/iwsgb/v100/p00035-p00039.pdf
Egeler, O., & Williams, T. D. (2000). Seasonal, age, and sex-related variation in fatty-acid composition of depot fat in relation to migration in western sandpipers. The Auk , 117 (1), 110. doi: 10.1642/0004-8038(2000)117[0110:saasrv]2.0.co;2
Elner, R. W., Beninger, P. G., Jackson, D. L., & Potter, T. M. (2005). Evidence of a new feeding mode in western sandpiper (Calidris mauri ) and dunlin (Calidris alpina ) based on bill and tongue morphology and ultrastructure. Marine Biology , 146 (6), 1223–1234. doi: 10.1007/s00227-004-1521-5
Evans Ogden, L. J., Hobson, K. A., & Lank, D. B. (2004). Blood isotopic (δ 13 C and δ 15 N) turnover and diet-tissue fractionation factors in captive dunlin (Calidris alpina pacifica ). The Auk ,121 (1), 170–177. doi: 10.2307/4090066
Fasola, M., Canova, L., & Biddau, L. (1996). Foraging habits of Crab Plovers Dromas ardeola overwintering on the Kenya Coast.Waterbirds , 19 (2), 207–213. doi: 10.2307/1521857
Fernández, G., & Lank, D. B. (2006). Sex, age, and body size distributions of western sandpipers during the nonbreeding season with respect to local habitat. The Condor , 108 (3), 547–557. doi: 10.1650/0010-5422(2006)108[547:saabsd]2.0.co;2
Fernández, G., & Lank, D. B. (2008). Foraging behaviour of non-breeding Western Sandpipers Calidris mauri as a function of sex, habitat and flocking. Ibis , 150 (3), 518–526. doi: 10.1111/j.1474-919X.2008.00812.x
Florin, S. T., Felicetti, L. A., & Robbins, C. T. (2011). The biological basis for understanding and predicting dietary-induced variation in nitrogen and sulphur isotope ratio discrimination.Functional Ecology , 25 (3), 519–526. doi: 10.1111/j.1365-2435.2010.01799.x
Franks, S. E., Fernández, G., Hodkinson, D. J., Kyser, T. K., & Lank, D. B. (2013). The long and the short of it: no dietary specialisation between male and female western sandpipers despite strong bill size dimorphism. PloS One , 8 (11), e79835. doi: 10.1371/journal.pone.0079835
Franks, S. E., Lank, D. B., & Wilson, Jr., W. H. (2020). Western sandpiper (Calidris mauri ). In Birds of the World (A. F. Poole, editor) (version 1.). Retrieved from https://doi.org/10.2173/bow.wessan.01
Goss-Custard, J. D., & Durell, S. E. A. Le V. Dit (1987). Age-related effects in oystercatchers, Haematopus ostralegus , feeding on mussels, Mytilus edulis . I. Foraging efficiency and interference.The Journal of Animal Ecology , 56 (2), 521. doi: 10.2307/5065
Groves, S. (1978). Age-related differences in ruddy turnstone foraging and aggressive behavior. The Auk , 95 (1), 95–103.
Guarini, J. M., Blanchard, G. F., Bacher, C., Gros, P., Riera, P., Richard, P., … Sauriau, P. (1998). Dynamics of spatial patterns of microphytobenthic biomass: inferences from a geostatistical analysis of two comprehensive surveys in Marennes-Oleron Bay (France).Marine Ecology Progress Series , 166 , 131–141. doi: 10.3354/meps166131
Guglielmo, C. G., & Williams, T. D. (2003). Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the western sandpiper (Calidris mauri ). Physiological and Biochemical Zoology , 76 (1), 84–98. doi: 10.1086/367942
Hopkins, J. B., & Ferguson, J. M. (2012). Estimating the diets of animals using stable isotopes and a comprehensive Bayesian mixing model.PLoS ONE , 7 (1). doi: 10.1371/journal.pone.0028478
Iverson, G. C., Warnock, S. E., Butler, R. W., Bishop, M. A., & Warnock, N. (1996). Spring migration of western sandpipers along the Pacific Coast of North America: a telemetry study. The Condor ,98 (1), 10–21. doi: 10.2307/1369502
Jardine, C. B., Bond, A. L., Davidson, P. J. A., Butler, R. W., & Kuwae, T. (2015). Biofilm consumption and variable diet composition of western sandpipers (Calidris mauri ) during migratory stopover.PLoS ONE , 10 (4), 1–14. doi: 10.1371/journal.pone.0124164
Jehl, J. R., & Murray, B. G. (1986). The evolution of normal and reverse sexual size dimorphism in shorebirds and other birds. In R. F. Johnston (Ed.), Current Ornithology (Vol. 3, pp. 1–86). New York: Plenum Press.
Jiménez, A., Elner, R. W., Favaro, C., Rickards, K., & Ydenberg, R. C. (2015). Intertidal biofilm distribution underpins differential tide-following behavior of two sandpiper species (Calidris mauriand Calidris alpina ) during northward migration. Estuarine, Coastal and Shelf Science , 155 , 8–16. doi: 10.1016/j.ecss.2014.12.038
Kuwae, T., Beninger, P. G., Decottignies, P., Mathot, K. J., Lund, D. R., & Elner, R. W. (2008). Biofilm grazing in a higher vertebrate: the western sandpiper, Calidris mauri . Ecology , 89 (3), 599–606.
Kuwae, T., Miyoshi, E., Hosokawa, S., Ichimi, K., Hosoya, J., Amano, T., … Elner, R. W. (2012). Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm.Ecology Letters , 15 (4), 347–356. doi: 10.1111/j.1461-0248.2012.01744.x
Lindström, Å., & Klaassen, M. (2003). High basal metabolic rates of shorebirds while in the Arctic: a circumpolar view. The Condor ,105 (3), 420–427. doi: 10.1650/7222
Lourenço, P. M., Granadeiro, J. P., Guilherme, J. L., & Catry, T. (2015). Turnover rates of stable isotopes in avian blood and toenails: Implications for dietary and migration studies. Journal of Experimental Marine Biology and Ecology , 472 , 89–96. doi: 10.1016/j.jembe.2015.07.006
Lovvorn, J. R., De La Cruz, S. E. W., Takekawa, J. Y., Shaskey, L. E., & Richman, S. E. (2013). Niche overlap, threshold food densities, and limits to prey depletion for a diving duck assemblage in an estuarine bay. Marine Ecology Progress Series , 476 , 251–268. doi: 10.3354/meps10104
Maillet, D., & Weber, J. M. (2006). Performance-enhancing role of dietary fatty acids in a long-distance migrant shorebird: the semipalmated sandpiper. Journal of Experimental Biology ,209 (14), 2686–2695. doi: 10.1242/jeb.02299
Maillet, D., & Weber, J. M. (2007). Relationship between n-3 PUFA content and energy metabolism in the flight muscles of a migrating shorebird: evidence for natural doping. Journal of Experimental Biology , 210 (3), 413–420. doi: 10.1242/jeb.02660
Mathot, K. J., & Elner, R. W. (2004). Evidence for sexual partitioning of foraging mode in western sandpipers (Calidris mauri ) during migration. Canadian Journal of Zoology , 82 , 1035–1042. doi: 10.1139/Z04-080
Mathot, K. J., Lund, D. R., & Elner, R. W. (2010). Sediment in stomach contents of western sandpipers and dunlin provide evidence of biofilm feeding. Waterbirds , 33 (3), 300–306.
Mathot, K. J., Smith, B. D., & Elner, R. W. (2007). Latitudinal clines in food distribution correlate with differential migration in the western sandpiper. Ecology , 88 (3), 781–791. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/17503605
McCutchan, J. H., Lewis, 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. doi: 10.1111/j.0030-1299.2005.erratum_1.x
Morrison, M. L. (1981). The structure of western warbler assemblages: analysis of foraging behavior and habitat selection in Oregon. The Auk , 98 , 578–588.
Myers, J. P., Morrison, R. I. G., Antas, P. Z., Harrington, B. A., Lovejoy, Thomas, E., Sallaberry, M., … Tarak, A. (1987). Conservation strategy for migratory species. American Scientist ,75 (1), 18–26.
Nebel, S. (2005). Latitudinal clines in bill length and sex ratio in a migratory shorebird: A case of resource partitioning? Acta Oecologica , 28 (1), 33–38. doi: 10.1016/j.actao.2005.02.002
Nebel, S., Jackson, D. L., & Elner, R. W. (2005). Functional association of bill morphology and foraging behaviour in calidrid sandpipers. Animal Biology , 55 (3), 235–243. doi: 10.1163/1570756054472818
Nebel, S., Lank, D. B., O’Hara, P. D., Fernández, G., Haase, B., Delgado, F., … Warnock, S. E. (2002). Western sandpipers (Calidris mauri ) during the nonbreeding season: spatial segregation on a hemispheric scale. The Auk , 119 (4), 922–928.
O’Hara, P. D., Fernández, G., Becerril, F., De La Cueva, H., & Lank, D. B. (2005). Life history varies with migratory distance in western sandpipers Calidris mauri . Journal of Avian Biology ,36 (3), 191–202. doi: 10.1111/j.0908-8857.2005.03368.x
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., … Wagner, H. (2019). vegan: community ecology package. R package v. 2.5-5 . Retrieved from https://cran.r-project.org/package=vegan
Page, G. W., & Fearis, B. (1971). Sexing western sandpipers by bill length. Bird-Banding , 42 , 297–298.
Page, G. W., Stenzel, L. E., & Kjelmyr, J. E. (1999). Overview of shorebird abundance and distribution in wetlands of the Pacific coast of the contiguous United States. The Condor , 101 (3), 461–471.
Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J., & Montaña, C. G. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia , 152 (1), 179–189. doi: 10.1007/s00442-006-0630-x
Puttick, G. M. (1978). The diet of the curlew sandpiper at Langebaan Lagoon, South Africa. Ostrich , 49 (4), 158–167.
Pyle, P. (2008). Identification guide to North American birds: part II Anatidae to Alcidae. Point Reyes Station, California, USA: Slate Creek Press.
Quinn, J. T., Hamilton, D. J., & Hebert, C. E. (2017). Fatty acid composition and concentration of alternative food of semipalmated sandpipers (Calidris pusilla ) in the upper bay of fundy, Canada.Canadian Journal of Zoology , 95 (8), 565–573. doi: 10.1139/cjz-2016-0246
R Core Team. (2019). R: A language and environment for statistical computing. Retrieved from https://www.r-project.org/.
Recher, H. F. (1966). Some aspects of the ecology of migrant shorebirds.Ecology , 47 (3), 393–406.
Robbins, C. T., Felicetti, L. A., & Florin, S. T. (2010). The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation. Oecologia , 162 (3), 571–579. doi: 10.1007/s00442-009-1485-8
Rowan, A. (2012). Effects of restoration on the small shorebird carrying capacity of a south bay mud flat . San Francisco State University.
Schnurr, P. J., Drever, M. C., Elner, R. W., Harper, J., & Arts, M. T. (2020). Peak abundance of fatty acids from intertidal biofilm in relation to the breeding migration of shorebirds. Frontiers in Marine Science , 7 (February), 1–17. doi: 10.3389/fmars.2020.00063
Schnurr, P. J., Drever, M. C., Kling, H. J., Elner, R. W., & Arts, M. T. (2019). Seasonal changes in fatty acid composition of estuarine intertidal biofilm: implications for western sandpiper migration.Estuarine, Coastal and Shelf Science , 224 , 94–107. doi: 10.1016/j.ecss.2019.04.047
Senner, S. E., Norton, D. W., & West, G. C. (1989). Feeding ecology of western sandpipers, Calidris mauri , and dunlins, C. alpina , during spring migration at Hartney, Bay, Alaska. Canadian Field-Naturalist , 103 (3), 372–379.
Stal, L. J. (2003). Microphytobenthos, their extracellular polymeric substances, and the morphogenesis of intertidal sediments.Geomicrobiology Journal , 20 (5), 463–478. doi: 10.1080/713851126
Stein, R. W., Fernández, G., De La Cueva, H., & Elner, R. W. (2008). Disproportionate bill length dimorphism and niche differentiation in wintering western sandpipers (Calidris mauri ). Canadian Journal of Zoology , 86 (7), 601–609. doi: 10.1139/Z08-033
Stein, R. W., Place, A. R., Lacourse, T., Guglielmo, C. G., & Williams, T. D. (2005). Digestive organ sizes and enzyme activities of refueling western sandpipers (Calidris mauri ): contrasting effects of season and age. Physiological and Biochemical Zoology ,78 (3), 434–446. doi: 10.1086/430038
Sutherland, T. F., Shepherd, P. C. F., & Elner, R. W. (2000). Predation on meiofaunal and macrofaunal invertebrates by western sandpipers (Calidris mauri ): evidence for dual foraging modes. Marine Biology , 137 (5–6), 983–993. doi: 10.1007/s002270000406
Svanbäck, R., & Bolnick, D. I. (2005). Intraspecific competition affects the strength of individual specialization: An optimal diet theory method. Evolutionary Ecology Research , 7 (7), 993–1012.
Székely, T., Freckleton, R. P., & Reynolds, J. D. (2004). Sexual selection explains Rensch’s rule of size dimorphism in shorebirds.Proceedings of the National Academy of Sciences of the United States of America , 101 (33), 12224–12227. doi: 10.1073/pnas.0404503101
Székely, T., Reynolds, J. D., & Figuerola, J. (2000). Sexual size dimorphism in shorebirds, gulls, and alcids: The influence of sexual and natural selection. Evolution , 54 (4), 1404–1413. doi: 10.1111/j.0014-3820.2000.tb00572.x
Underwood, G. J. C., & Paterson, D. M. (2003). The importance of extracellular carbohydrate production by marine epipelic diatoms.Advances in Botanical Research , 40 , 183–240.
Vanderklift, M. A., & Ponsard, S. (2003). Sources of variation in consumer-diet delta 15N enrichment: a meta-analysis. Oecologia ,136 (2), 169–182. doi: 10.1007/s00442-003-1270-z
Warnock, S. E., & Takekawa, J. Y. (1995). Habitat preferences of wintering shorebirds in a temporally changing environment: western sandpipers in the San Francisco Bay estuary. The Auk ,112 (4), 920–930. Retrieved from http://www.jstor.org/stable/4089023
Warnock, S. E., & Takekawa, J. Y. (1996). Wintering site fidelity and movement patterns of Western Sandpipers Calidris mauri in the San Francisco Bay estuary. Ibis , 138 , 160–167. Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.1474-919X.1996.tb04323.x/abstract
Weihs, C., Ligges, U., Luebke, K., & Raabe, N. (2005). klaR analyzing German business cycles. In D. Baier, R. Decker, & L. Schmidt-Thieme (Eds.), Data analysis and decision support (pp. 335–343). Berlin: Springer Verlag.
Williams, T. D., Warnock, N., Takekawa, J. Y., & Bishop, M. A. (2007). Flyway-scale variation in plasma triglyceride levels as an index of refueling rate in spring-migrating western sandpipers (Calidris mauri ). The Auk , 124 (3), 886–897. doi: 10.1642/0004-8038(2007)124[886:FVIPTL]2.0.CO;2