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