Abstract
Human-induced rapid environmental change (HIREC) has altered landscape processes and negatively impacted many species globally. Some of the most dramatic changes have been in wetlands where flows have been disrupted, and new wetlands have been created to retain runoff. In response to disrupted natural wetland conditions, Wood Stork (Mycteria americana) populations in South Florida have significantly declined over the past several decades. Despite the well-documented sensitivity of Wood Storks to natural wetland conditions, Wood Storks are often observed foraging in roadside created wetlands; however, the availability of prey in created wetlands is currently unknown. We sampled natural and created wetlands to determine aquatic fauna available for foraging Wood Storks. To determine prey use, we collected food boluses from Wood Storks in both natural wetland and urban landscapes. Historical studies found nonnative fish were absent in Wood Stork diet prior to the dominance of created wetlands in the landscape; however, we found nonnative fish frequently in both created wetlands and boluses. Furthermore, urban nesting Wood Storks consumed large-bodied prey species that were more characteristic of created wetlands whereas Wood Storks nesting in natural wetlands consumed large-bodied prey more characteristic of natural wetlands. Overall, Wood Storks consumed prey that were more similar to the fish community in created wetlands than those in natural wetlands. These dietary patterns suggest that Wood Storks have behavioral plasticity in both foraging habitat and prey use to cope with HIREC. Conservation efforts for species existing in both natural and urban habitats should consider the importance of novel prey and foraging habitats, as they may assist in sustaining populations in a rapidly changing world.
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All data are available upon request.
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Primary analyses were done using a non-code-based software, PRIMER-7. Information on these analyses are available by request.
References
Baronsky AD, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA (2011) Has the Earth’s six mass extinction already arrived? Nature 471:51–57. https://doi.org/10.1038/nature09678
Borkhataria RR, Frederick PC, Keller RA, Collazo JA (2012) Temporal variation in local wetland hydrology influences postdispersal survival of juvenile Wood Storks (Mycteria americana). Auk 129:517–528. https://doi.org/10.1525/auk.2012.11244
Botson BA, Gawlik DE, Trexler JC (2016) Mechanisms that generate resource pulses in a fluctuating wetland. PLoS One 11:e0158864. https://doi.org/10.1371/journal.pone.0158864
Brousseau P, Lefebvre J, Giroux JF (1996) Diet of ring-billed gull chicks in urban and non-urban colonies in Quebec. Col Waterbirds 19:22–30. https://doi.org/10.2307/1521803
Bryan AL Jr, Gariboldi JC (1998) Food of nestling Wood Storks in coastal Georgia. Col Waterbirds 21:152–158. https://doi.org/10.2307/1521902
Cattau CE, Fletcher RJ Jr, Reichert BE, Kitchens WM (2016) Counteracting effects on a nonnative prey on the demography of a native predator culminate in positive population growth. Ecol Appl 26:1952–1968. https://doi.org/10.1890/15-1020.1
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Clarke KR, Gorley RN (2015) Plymouth routines in multivariate ecological research. Getting started with PRIMER 7. http://updates.primer-e.com/primer7/manuals/Getting_started_with_PRIMER_7.pdf
Clarke KR, Green RH (1988) Statistical design and analysis for ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226. https://doi.org/10.3354/meps046213
Cowell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Plant Ecol 5:3–21. https://doi.org/10.1093/jpe/rtr044
Dahl TE (2011) Status and trends of wetlands in the conterminous United States 2004 to 2009. Department of the Interior, US Fish and Wildlife Service, Washington, DC, USA
DeAngelis DL, Trexler JC, Cosner C, Obaza A, Jopp F (2010) Fish population dynamics in a seasonally varying wetland. Ecol Modell 221:1131–1137. https://doi.org/10.1016/j.ecolmodel.2009.12.021
Depkin FC, Coulter MC, Bryan AL Jr (1992) Food of nestling Wood Storks in east-central Georgia. Col Waterbirds 15:219–225. https://doi.org/10.2307/1521455
Dorn NJ, Cook MI, Herring G, Boyle RA, Nelson J, Gawlik DE (2011) Aquatic prey switching and urban foraging by the White Ibis Eudocimus albus are determined by wetland hydrological conditions. Ibis 153:323–335. https://doi.org/10.1111/j.1474-919X.2011.01101.x
Evans BA, Gawlik DE (2020) Urban food subsidies reduce natural food limitations and reproductive costs for a wetland bird. Sci Rep 10:14021. https://doi.org/10.1038/s41598-020-70934-x
Fidorra JC, Frederick PC, Evers DC, Meyer KD (2016) Selection of human-influenced and natural wetlands by Great Egrets at multiple scales in the southeastern USA. Condor 118:46–56. https://doi.org/10.1650/CONDOR-14-117.1
Francis RJ, Kingsford RT, Murray-Hudson M, Brandis KJ (2021) Urban waste no replacement for natural foods—Marabou storks in Botswana. J Urban Ecol 7:1–10. https://doi.org/10.1093/jue/juab003
Frederick PC, Gawlik DE, Ogden JC, Cook MI, Lusk M (2009) The white ibis and wood stork as indicators for restoration of the Everglades system. Ecol Indic 9:S83–S95. https://doi.org/10.1016/j.ecolind.2008.10.012
Frederick PC, Spalding MG (1994) Factors affecting reproductive success of wading birds (Ciconiiformes) in the Everglades ecosystem. In: Davis SM, Ogden JC (eds) Everglades: The ecosystem and its restoration St. Lucie Press, Delray Beach, Florida, pp 659–692
Gawlik DE (2000) South Florida wading bird report. South Florida Water Management District, West Palm Beach, Florida
Gawlik DE (2002) The effects of prey availability on the numerical response of wading birds. Ecol Monogr 72:329–346. https://doi.org/10.1890/0012-9615(2002)072[0329:TEOPAO]2.0.CO;2
Gawlik DE, Evans BA, Klassen JA, Gottlieb A, Cyriacks W (2017) Wood Stork use of roadway corridor features in South Florida. Report to the Florida Department of Transportation, Fort Lauderdale, Florida
Gienapp P (2012) Migration. In: Wong BBM, Candolin U (eds) Behavioural responses to a changing world. Oxford University Press, Oxford, pp 80–92
Gilbert NI, Correia RA, Silva JP, Pacheco C, Catry I, Atkinson PW, Gill JA, Franco AMA (2016) Are white storks addicted to junk food? Impacts of landfill use on the movement and behavior of resident white storks (Ciconia ciconia) from a partially migratory population. Mov Ecol 4:7. https://doi.org/10.1186/s40462-016-0070-0
González J (1997) Seasonal variation in the foraging ecology of the Wood Stork in the southern llanos of Venezuela. Condor 99:671–680. https://doi.org/10.2307/1370479
Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S, Crawford RJM, Ryan PG (2008) A junk-food hypothesis for gannets feeding on fishery waste. Proc R Soc B 275:1149–1156. https://doi.org/10.1098/rspb.2007.1763
Gunderson LH, Loftus WF (1993) The Everglades. In: (Martin WH, Boyce SG, Echternact AC (eds) Biodiversity of the Southeastern United States: lowland terrestrial communities Wiley, New York, pp 199–255
Herring HK, Gawlik DE (2011) Resource selection functions for Wood Stork foraging habitat in the southern Everglades. Waterbirds 34:133–142. https://doi.org/10.1675/063.034.0201
Hsieh TC, Ma KH, Chao A (2016) iNEXT: iNterpolation and EXTrapolation for species diversity. R package 2.0.12. http://chao.stat.nthu.edu.tw/blog/software-download/. Accessed 16 June 2018
Ishiyama N, Sueyoshi M, Watanabe N, Nakamura F (2016) Biodiversity and rarity distributions of native freshwater fish in an agricultural landscape: the importance of β diversity between and within water-body types. Aquat Conserv 26:416–428. https://doi.org/10.1002/aqc.2583
Jakubas D (2004) The response of the grey heron to a rapid increase of the Round Goby. Waterbirds 27:304–307. https://doi.org/10.1675/1524-4695(2004)027[0304:TROTGH]2.0.CO;2
Jordan F, Coyne S, Trexler JC (1997) Sampling fishes in vegetated habitats: effects of habitat structure on sampling characteristics in the 1–m2 throw trap. T Am Fish Soc 126:1012–1020. https://doi.org/10.1577/1548-8659(1997)126%3c1012:SFIVHE%3e2.3.CO;2
Kahl MP Jr (1964) Food ecology of the wood stork (Mycteria americana) in Florida. Ecol Monogr 34:97–117. https://doi.org/10.2307/1948449
King RS, Richardson CJ, Urban DL, Romanowicz EA (2004) Spatial dependency of vegetation-environment linkages in an anthropogenically influenced wetland ecosystem. Ecosystems 7:75–97
Klassen JA, Gawlik DE (2018) Changing diets as a means to predict species adaptability to human-induced rapid environmental change. J Field Ornithol 89:126–139
Kline JL, Loftus WF, Kotun K, Trexler JC, Rehage JS, Lorenz JJ, Robinson M (2014) Recent fish introductions into Everglades National Park: an unforeseen consequence of water management? Wetlands 34:175–187. https://doi.org/10.1007/s13157-012-0362-0
Kushlan JA (1976) Wading bird predation in a seasonally fluctuating pond. Auk 93:464–476
Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford
Langston JN, Schofield PJ, Hill JE, Loftus WF (2010) Salinity tolerance of the African jewelfish Hemichromis letourneuxi, a nonnative cichlid in South Florida USA. Copeia 3:475–480. https://doi.org/10.1643/CP-09-069
Loftus WF, Kushlan JA (1987) Freshwater fishes of southern Florida. Bull Fla State Mus Biol Sci 31:147–344
Lopéz-Sepulcre A, Kokko H (2012) Understanding behavioural responses and their consequences. In: Wong BBM, Candolin U (eds) Behavioural responses to a changing world. Oxford University Press, Oxford, pp 3–15
Massemin-Challet S, Gendner JP, Samtmann S, Pichegru L, Wulgué A, Maho YL (2006) The effect of migration strategy and food availability on White Stork Ciconia ciconia breeding success. Ibis 148:503–508. https://doi.org/10.1111/j.1474-919X.2006.00550.x
Nuttle WK (1997) Measurement of wetland hydroperiod using harmonic analysis. Wetlands 17:82–89. https://doi.org/10.1007/BF03160720
Oaks JL, Gilbert M, Virani MZ, Watson RT, Meteyer CU, Rideout BA, Shivaprasad HL, Ahmed S, Chaudhry MJI, Arshad M, Mahmood S, Ali A, Khan AA (2004) Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427:630–633. https://doi.org/10.1038/nature02317
Ogden JC, Kushlan JA, Tilmant JT (1976) Prey selectivity by the wood stork. Condor 78:324–330. https://doi.org/10.2307/1367691
Ogden JC (1994) A comparison of wading bird nesting dynamics, 1931–1946 and 1974–1989 as an indication of changes in ecosystem conditions in the southern Everglades. In: Davis S, Ogden JC (eds) Everglades: The Ecosystem and its Restoration St. Lucie Press, Delray Beach, Florida, pp 533–570
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790. https://doi.org/10.1126/science.293.5536.1786
Plaza PI, Lambertucci SA (2017) How are garbage dumps impacting vertebrate demography, health, and conservation? Glob Ecol Conserv 12:9–20. https://doi.org/10.1016/j.gecco.2017.08.002
Pomeroy D, Kibuule M (2017) Increasingly urban Marabou Storks start breeding four months early in Kampala, Uganda. Ostrich 88:261–266. https://doi.org/10.2989/00306525.2017.1308443
R Development Core Team (2017) R: A language and environment for statistical computing. R 3.2.4. Vienna, Austria: R Foundation for Statistical Computing
Ramo C, Busto B (1992) Nesting failure of the Wood Stork in a neotropical wetland. Condor 94:777–781. https://doi.org/10.2307/1369265
Rehage JS, Trexler JC (2006) Assessing the net effect of anthropogenic disturbance on aquatic communities in wetlands: community structure relative to distance form canals. Hydrobiologia 569:359–373. https://doi.org/10.1007/s10750-006-0142-z
Reichert B, Cattau C, Kitchens W, Fletcher R, Olbert J, Pias K, Zweig C (2011) Snail Kite Demography annual report 2011. Interim Report to the U.S. Army Corps of Engineers, Jacksonville, Florida
Rodgers JA Jr, Smith HT (1995) Set-Back Distances to Protect Nesting Bird Colonies from Human Disturbance in Florida. Conserv Biol 9:89–99. https://doi.org/10.1046/j.1523-1739.1995.09010089.x
Rodgers JA Jr, Schwikert ST (2002) Buffer-zone distances to protect foraging and loafing waterbirds from disturbance by personal watercraft and outboard-powered boats. Conserv Biol 16:216–224
Rosenthal GG, Stuart-Fox D (2012) Environmental disturbance and animal communication. In: Wong BBM Candolin U (eds) Behavioural responses to a changing world. Oxford University Press, Oxford, pp 16–31
Ruffino L, Salo P, Koivisto E, Banks PB, Korpimäk E (2014) Reproductive responses of birds to experimental food supplementation: a meta-analysis. Front Zoo 11:80. https://doi.org/10.1186/s12983-014-0080-y
Schofield PJ, Loftus WF, Kobza RM, Cook MI, Sloane DH (2010) Tolerance of nonindigenous cichlid fishes (Cichlasoma urophthalmus, Hemichromis letourneuxi) to low temperature: laboratory and field experiments in South Florida. Biol Invasions 12:2241–2457. https://doi.org/10.1007/s10530-009-9654-6
Shafland PL, Pestrak JM (1982) Lower lethal temperatures for fourteen nonnative fishes in Florida. Environ Biol Fishes 7:149–156. https://doi.org/10.1007/BF00001785
Shafland P, Gestring KB, Stanford MS (2008) Florida’s exotic freshwater fishes—2007. Florida Scientist 71:220–245
Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 3:367–387. https://doi.org/10.1111/j.1752-4571.2010.00166.x
Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088. https://doi.org/10.1016/j.anbehav.2013.02.017
Snell-Rood EC (2013) An overview of evolutionary causes and consequences of behavioural plasticity. Anim Behav 85:1004–1011. https://doi.org/10.1016/j.anbehav.2012.12.031
Sol D, Lapiedra O, Gonzalez-Lagos C (2013) Behavioural flexibility for life in the city. Anim Behav 85:1101–1112
Thabethe V, Downs CT (2018) Citizen science reveals widespread supplemental feeding of African woolly-necked storks in suburban areas of KwaZulu-Natal, South Africa. Urban Ecosyt 21:965–973. https://doi.org/10.1007/s11252-018-0774-6
Tortosa FS, Caballero JM, Reyes-López J (2002) Effect of rubbish dumps on breeding success in the White Stork in Southern Spain. Waterbirds 25:39–43. https://doi.org/10.1675/1524-4695(2002)025[0039:EORDOB]2.0.CO;2
Trexler JC, Loftus WF, Jordan F, Lorenz JJ, Chick JH, Kobza RM (2000) Empirical assessment of fish introduction in a subtropical wetland: an evaluation of contrasting views. Biol Invasions 2:265–277. https://doi.org/10.1023/A:1011488118444
Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev Camb Philos Soc 86:640–657
United States Fish and Wildlife Service (USFWS) (1996) Revised recovery plan for the U.S. breeding population of the wood stork. U. S. Fish and Wildlife Service. Atlanta, Georgia, p 41
United States Fish and Wildlife Service (USFWS) (2014) Reclassification of the U.S. breeding population of the Wood Stork from endangered to threatened. Federal Register 79:37078–37103
United States Fish and Wildlife Service (USFWS) (2015) Wood Stork Southeast US Nesting from 1975 to 2015. U.S. Fish and Wildlife North Florida Ecological Services Office. https://www.fws.gov/northflorida/woodstorks/wood-storks.htm. Accessed 17 Jun 2018
Van Guilder MA, Seefelt NE (2013) Double-crested Cormorant (Phalacrocorax auritus) chick bioenergetics following round goby (Neogobius melanostomus) invasion and implementation of cormorant population control. J Great Lakes Res 39:153–161. https://doi.org/10.1016/j.jglr.2012.12.019
Van Houtan KS, Pimm SL, Halley JM, Bierregaard RO, Lovejoy TE (2007) Dispersal of Amazonian birds in continuous and fragmented forest. Ecol Lett 10:219–229. https://doi.org/10.1111/j.1461-0248.2007.01004.x
Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:26212626. https://doi.org/10.1371/journal.pbio.0060325
Wong BBM, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673. https://doi.org/10.1093/beheco/aru183
Acknowledgements
We are grateful to the many individuals who provided substantial assistance in the field, including Lauren Haag, Jenna May, Carl Santangelo, Victor Benavides, Alissa Gulette, Sarah Staton, Zara Mansoor, and Ashley Jackson. We also thank Wendy Cyriacks and Andrew Gottlieb, for their assistance in project management and field data collection. We are also grateful to Rindy Anderson, Nathan Dorn, Colin Hughes, Kate Shlepr, and two anonymous reviewers for invaluable comments on drafts of this manuscript.
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This research was supported by the Florida Department of Transportation (BDV27-922-02).
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Betsy Evans, Jessica Klassen, and Dale Gawlik designed the study and developed the methods. Betsy Evans and Jessica Klassen collected the data. Betsy Evans analyzed the data and wrote the manuscript. Dale Gawlik and Jessica Klassen provided substantial feedback and edited all versions of the manuscript.
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Research techniques were approved by the Florida Atlantic University Institutional Animal Care and Use Committee (IACUC; Protocol A14-11, A14-28), US Fish and Wildlife Service (TE65550A), Big Cypress National Preserve (BICY-2014-SCI-0014), Everglades National Park (EVER-2014/2016-SCI-0021), Florida Fish and Wildlife Conservation Commission (S-15-02), and the Miccosukee Tribe of Indians of Florida.
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Evans, B.A., Klassen, J.A. & Gawlik, D.E. Dietary flexibility of Wood Storks in response to human-induced rapid environmental change. Urban Ecosyst 25, 705–718 (2022). https://doi.org/10.1007/s11252-021-01181-9
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DOI: https://doi.org/10.1007/s11252-021-01181-9