Advertisement

Marine Biology

, 166:50 | Cite as

Predictors of foraging plasticity by greater flamingo (Phoenicopterus roseus) in intertidal soft sediments

  • Kirti N. GihwalaEmail author
  • Deena Pillay
  • Melvin Varughese
Original paper

Abstract

Numerous studies have emphasised the importance of apex predators in determining community dynamics and broader functioning in marine ecosystems. However, less understood is the ecology of plastic foraging behaviours employed by predators, with drivers of foraging plasticity being a particular knowledge gap in marine sediments. In June/July 2015, we assessed the role of traits and abundance of prey assemblages in influencing decisions made by greater flamingos Phoenicopterus roseus to employ different foraging behaviours in intertidal sandflat ecosystems in Langebaan Lagoon, on the west coast of South Africa (33°11′27″S, 18°07′37″E and 33°03′54″S, 17°58′07″E). Greater flamingos feed by either (1) creating pits, which involves flamingos stirring up deep sediments with their feet or (2) creating channels, in which their inverted bills are swept from side to side on the sediment surface. RandomForest modelling techniques indicated that both pit- and channel-foraging strategies were linked to low macrofaunal biomass in sediment patches, indicating that smaller prey items may be preferred targets for consumption. Channel foraging was linked mainly to the abundance of surface-associated fauna, suggesting that this feeding technique was predominantly a surficial foraging strategy. The probability of pit foraging increased with increasing concentrations of benthic microalgae, suggesting that high microalgal biomass may be linked to pit foraging. Overall, this study adds to knowledge on the role of flamingos as predators in marine sediments, by highlighting biotic predictors of foraging plasticity. The study demonstrates the relevance of understanding potential drivers of foraging plasticity in developing a predictive understanding of predator impacts in heterogeneous ecosystems.

Notes

Acknowledgements

Funding for the research was provided by the National Research Foundation (NRF). We thank the students of the Biological Sciences Department, University of Cape Town, for field and laboratory assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional (University of Cape Town) guidelines for the care and use of animals were followed. Due to the observational nature of the study, animal ethics approval was not required.

Supplementary material

227_2019_3497_MOESM1_ESM.pdf (543 kb)
Supplementary material 1 (PDF 543 kb)

References

  1. Abu-Mostafa YS, Magdon-Ismail M, Lin H (2012) Learning from data. AML Book, SingaporeGoogle Scholar
  2. Allen RP (1956) The Flamingos: their life history and survival. Research Report #5 of the National Audubon Society. National Audubon Society, New YorkGoogle Scholar
  3. Arengo F, Baldassarre GA (1999) Resource variability and conservation of American Flamingos in coastal wetlands of Yucatán, Mexico. J Wildl Manag 63(4):1201–1212.  https://doi.org/10.2307/3802838 CrossRefGoogle Scholar
  4. Bell WJ (1991) Searching behaviour. Chapman & Hall, LondonGoogle Scholar
  5. Bildstein KL, Baldassarre GA, Arengo F (2000) Flamingo science: current status and future needs. Waterbirds 23:206–211.  https://doi.org/10.1650/CONDOR-17-187.1 CrossRefGoogle Scholar
  6. Boyd IL, Arnould JPY, Barton T, Croxall JP (1994) Foraging behaviour of Antarctic fur seals during periods of contrasting prey abundance. J Anim Ecol 63(3):703–713.  https://doi.org/10.2307/5235 CrossRefGoogle Scholar
  7. Branch GM, Griffith CL, Branch ML, Beckley LE (2010) Two oceans: a guide to the marine life of southern Africa. Struik Nature, Cape TownGoogle Scholar
  8. Brown C, King C, Mossbarger S, Barron J (2005) Flamingo husbandry guidelines. American Zoo and Aquarium Association, Silver SpringGoogle Scholar
  9. Carpenter SR, Cole JJ, Kitchell JF, Pace ML (2010) Trophic cascades in lakes: lessons and prospects. In: Terborgh J, Estes JA (eds) Trophic cascades: predators, prey and the changing dynamics of nature. Island Press, Washington, DCGoogle Scholar
  10. Cherel Y, Connan M, Jaeger A, Richard P (2014) Seabird year-round and historical feeding ecology: blood and feather δ13C and δ15N values document foraging plasticity of small sympatric petrels. Mar Ecol Prog Ser 505:267–280.  https://doi.org/10.3354/meps10795 CrossRefGoogle Scholar
  11. Christie ND (1976) A numerical analysis of the distribution of a shallow sublittoral sand macrofauna along a transect at Lamberts Bay, South Africa. Trans R Soc S Afr 42(2):149–172.  https://doi.org/10.1080/00359197609519906 CrossRefGoogle Scholar
  12. Compton JS (2001) Holocene sea-level fluctuations inferred from the evolution of depositional environments of the southern Langebaan Lagoon salt marsh, South Africa. Holocene 11:395–405.  https://doi.org/10.1191/095968301678302832 CrossRefGoogle Scholar
  13. Day JH (1959) The biology of Langebaan Lagoon: a study of the effect of shelter from wave action. Trans R Soc S Afr 35:475–547.  https://doi.org/10.1080/00359195909519025 CrossRefGoogle Scholar
  14. de Edelenyi FS, Goumidi L, Bertrais S, Phillips C, MacManus R, Roche H, Planells R, Lairon D (2008) Prediction of the metabolic syndrome status based on dietary and genetic parameters, using Random Forest. Genes Nutr 3:173–176.  https://doi.org/10.1007/s12263-008-0097-y CrossRefGoogle Scholar
  15. Desroy N, Warembourg C, Dewarumez JM, Dauvin JC (2002) Macrobenthic resources of the shallow soft-bottom sediments in the eastern English Channel and southern North Sea. ICES J Mar Sci 60:120–131.  https://doi.org/10.1006/jmsc.2002.1333 CrossRefGoogle Scholar
  16. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252.  https://doi.org/10.5253/arde.v68.p225 CrossRefGoogle Scholar
  17. Duffy JE, Reynolds PL, Boström C, Coyer JA, Cusson M, Donadi S et al (2015) Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative-experimental approach. Ecol Lett 18(7):696–705.  https://doi.org/10.1111/ele.12448 CrossRefPubMedGoogle Scholar
  18. Ebrahim A, Olds AD, Maxwell PS, Pitt KA, Burfeind DD, Connolly RM (2014) Herbivory in a subtropical seagrass ecosystem: separating the functional role of different grazers. Mar Ecol Prog Ser 511:83–91.  https://doi.org/10.3354/meps10901 CrossRefGoogle Scholar
  19. Flemming BW (1977) Langebaan Lagoon: a mixed carbonate-siliciclastic tidal environment in a semi-arid climate. Sediment Geol 18:61–95.  https://doi.org/10.1016/0037-0738(77)90006-9 CrossRefGoogle Scholar
  20. Gerbersdorf SU, Wieprecht S (2015) Biostabilization of cohesive sediments: revisiting the role of abiotic conditions, physiology and diversity of microbes, polymeric secretion, and biofilm architecture. Geobiology 13:68–97.  https://doi.org/10.1111/gbi.12115 CrossRefPubMedGoogle Scholar
  21. Gihwala KN, Pillay D, Varughese M (2017) Differential impacts of foraging plasticity by greater flamingo (Phoenicopterus roseus) on intertidal soft-sediments. Mar Ecol Prog Ser 569:227–242.  https://doi.org/10.3354/meps12069 CrossRefGoogle Scholar
  22. Glassom D, Branch GM (1997) Impact of predation by greater flamingos Phoenicopterus ruber on the macrofauna of two southern African lagoons. Mar Ecol Prog Ser 149:1–12.  https://doi.org/10.3354/meps149001 CrossRefGoogle Scholar
  23. Greeff JM, Whiting MJ (2000) Foraging-Mode Plasticity in the lizard Platysaurus broadleyi. Herpetologica 56:402–407Google Scholar
  24. Hines AH, Comtois KL (1985) Vertical distribution of infauna in sediments of a subestuary of central Chesapeake Bay. Estuaries 8(3):296–304.  https://doi.org/10.2307/1351490 CrossRefGoogle Scholar
  25. Holme NA (1964) Methods of sampling the benthos. In: Russel FS (ed) Advances in marine biology. Academic, LondonGoogle Scholar
  26. Hurlbert SH, Chang CC (1983) Ornitholimnology: effects of grazing by the Andean flamingo (Phoenicoparrus andinus). Proc Natl Acad Sci 80(15):4766–4769.  https://doi.org/10.1073/pnas.80.15.4766 CrossRefPubMedGoogle Scholar
  27. IBM (2015) IBM SPSS statistics 22 core systems user’s guide. IBM Corporation, ArmonkGoogle Scholar
  28. James G, Witten D, Hastie T, Tibshirani R (2013) An introduction to statistical learning: with applications in R. Springer, New YorkCrossRefGoogle Scholar
  29. Jenkin PM (1957) The filter-feeding and food of flamingos (Phoenicopteri). Philos Trans R Soc Lond B Biol Sci 240:401–493.  https://doi.org/10.1098/rstb.1957.0004 CrossRefGoogle Scholar
  30. Johnson RG (1967) The vertical distribution of the infauna of a sand flat. Ecology 48(4):571–578.  https://doi.org/10.2307/1936501 CrossRefGoogle Scholar
  31. Johnson AR (1997) Phoenicopterus ruber Greater Flamingo. BWP Update 1:15–23Google Scholar
  32. Johnson A, Cezilly F (2007) The greater Flamingo. T & AD Poyser, LondonGoogle Scholar
  33. Katano O (2011) Effects of individual differences in foraging of pale chub on algal biomass through trophic cascades. Environ Biol Fishes 92:101–112.  https://doi.org/10.1007/s10641-011-9820-4 CrossRefGoogle Scholar
  34. Kristjánsson TO, Jónsson JE, Svavarsson J (2013) Spring diet of common eiders (Somateria mollissima) in Breiðafjo¨rður, West Iceland, indicates non-bivalve preferences. Polar Biol 36:51–59.  https://doi.org/10.1007/s00300-012-1238-8 CrossRefGoogle Scholar
  35. Lemon WC (1991) Fitness consequences of foraging behavior in the zebra finch. Nature 352:153–155.  https://doi.org/10.1038/352153a0 CrossRefGoogle Scholar
  36. Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2(3):18–22Google Scholar
  37. Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48(1):25–34.  https://doi.org/10.2307/1313225 CrossRefGoogle Scholar
  38. MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19(2):186–201.  https://doi.org/10.2307/1352224 CrossRefGoogle Scholar
  39. Miller TJ (2002) Assemblages, communities, and species interactions. In: Fuimann LE, Werner RG (eds) Fishery science: the unique contributions of early life stages. Blackwell Publishing, OxfordGoogle Scholar
  40. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692.  https://doi.org/10.1016/j.tree.2005.08.002 CrossRefPubMedGoogle Scholar
  41. Molles MC (2015) Ecology: concepts and applications, 7th edn. McGraw-Hill Education, New YorkGoogle Scholar
  42. Monaghan P, Walton P, Wanless S, Uttley JD, Burns MD (1994) Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding guillemots Uria aalge. Ibis 136:214–222.  https://doi.org/10.1111/j.1474-919X.1994.tb01087.x CrossRefGoogle Scholar
  43. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR et al (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101.  https://doi.org/10.1126/science.1121129 CrossRefGoogle Scholar
  44. Nolet BA, Fuld VN, van Rijswijk MEC (2006) Foraging costs and accessibility as determinants of giving-up densities in a swan-pondweed system. Oikos 112:353–362.  https://doi.org/10.1111/j.0030-1299.2006.13463.x CrossRefGoogle Scholar
  45. Otto SB, Berlow EL, Rank NE, Smiley J, Brose U (2008) Predator diversity and identity drive interaction strength and trophic cascades in a food web. Ecology 89:134–144.  https://doi.org/10.1890/07-0066.1 CrossRefPubMedGoogle Scholar
  46. Ouellet JF, Vanpe C, Guillemette M (2013) The body size-dependent diet composition of North American sea ducks in winter. PLoS One 8:e65667.  https://doi.org/10.1371/journal.pone.0065667 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75.  https://doi.org/10.1086/282400 CrossRefGoogle Scholar
  48. Paine RT (1971) A short-term experimental investigation of resource partitioning in a New Zealand rocky intertidal habitat. Ecology 52(6):1096–1106.  https://doi.org/10.2307/1933819 CrossRefGoogle Scholar
  49. Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010) Foraging plasticity in a pelagic seabird species along a marine productivity gradient. Mar Ecol Prog Ser 398:259–274.  https://doi.org/10.3354/meps08319 CrossRefGoogle Scholar
  50. Pettex E, Lorentsen SH, Grémillet D, Gimenez O, Barrett RT, Pons JB, Bohec CL, Bonadonna F (2012) Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity. Mar Biol 159:2743–2756.  https://doi.org/10.1007/s00227-012-2035-1 CrossRefGoogle Scholar
  51. Pienkowski MW (1983) Surface activity of some intertidal invertebrates in relation to temperature and the foraging behaviour of their shorebird predators. Mar Ecol Prog Ser 11:141–150CrossRefGoogle Scholar
  52. Pillay D, Branch GM (2011) Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanogr Mar Biol Annu Rev 49:137–192.  https://doi.org/10.1201/b11009-5 CrossRefGoogle Scholar
  53. Pillay D, Branch GM, Forbes AT (2007a) The influence of bioturbation by the sandprawn Callianassa kraussi on feeding and survival of the bivalve Eumarcia paupercula and the gastropod Nassarius kraussianus. J Exp Mar Biol Ecol 344:1–9.  https://doi.org/10.1016/j.jembe.2006.10.044 CrossRefGoogle Scholar
  54. Pillay D, Branch GM, Forbes AT (2007b) Experimental evidence for the effects of the thalassinidean sandprawn Callianassa kraussi on macrobenthic communities. Mar Biol 152(3):611–618.  https://doi.org/10.1007/s00227-007-0715-z CrossRefGoogle Scholar
  55. Pillay D, Branch GM, Forbes AT (2007c) Effects of Callianassa kraussi on microbial biofilms and recruitment of macrofauna: a novel hypothesis for adult-juvenile interactions. Mar Ecol Prog Ser 347:1–14.  https://doi.org/10.3354/meps07054 CrossRefGoogle Scholar
  56. Pillay D, Branch GM, Forbes AT (2008) Habitat change in an estuarine embayment: anthropogenic influences and a regime shift in biotic interactions. Mar Ecol Prog Ser 370:19–31.  https://doi.org/10.3354/meps07631 CrossRefGoogle Scholar
  57. Pillay D, Branch GM, Steyn A (2009) Complex effects of the gastropod Assiminea globulus on benthic community structure in a marine-dominated lagoon. J Exp Mar Biol Ecol 380:47–52.  https://doi.org/10.1016/j.jembe.2009.08.016 CrossRefGoogle Scholar
  58. Pillay D, Branch GM, Griffiths CL, Williams C, Prinsloo A (2010) Ecosystem change in a South African marine reserve (1960–2009): role of seagrass loss and anthropogenic disturbance. Mar Ecol Prog Ser 415:35–48.  https://doi.org/10.3354/meps08733 CrossRefGoogle Scholar
  59. Pillay D, Branch GM, Dawson J, Henry D (2011) Contrasting effects of ecosystem engineering by the cordgrass Spartina maritima and the sandprawn Callianassa kraussi in a marine-dominated lagoon. Estuar Coast Shelf Sci 91:169–176.  https://doi.org/10.1016/j.ecss.2010.10.010 CrossRefGoogle Scholar
  60. Putman R, Wratten SD (1984) Principles of ecology. Croom Helm, LondonGoogle Scholar
  61. Reynolds PL, Richardson JP, Duffy JE (2014) Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol Oceanogr 59(3):1053–1064.  https://doi.org/10.4319/lo.2014.59.3.1053 CrossRefGoogle Scholar
  62. Richman SE, Lovvorn JR (2004) Relative foraging value to lesser scaup ducks of native and exotic clams from San Francisco Bay. Ecol Appl 14:1217–1231.  https://doi.org/10.1890/03-5032 CrossRefGoogle Scholar
  63. Richman SE, Lovvorn JR (2009) Predator size, prey size and threshold food densities of diving ducks: does a common prey base support fewer large animals? J Anim Ecol 78:1033–1042.  https://doi.org/10.1111/j.1365-2656.2009.01556.x CrossRefPubMedGoogle Scholar
  64. Ronconi RA, Burger AE (2008) Limited foraging flexibility: increased foraging effort by a marine predator does not buffer against scarce prey. Mar Ecol Prog Ser 366:245–258.  https://doi.org/10.3354/meps07529 CrossRefGoogle Scholar
  65. Suryan RM, Irons DB, Benson J (2000) Prey switching and variable foraging strategies of black-legged kittiwakes and the effect on reproductive success. Condor 102:374–384.  https://doi.org/10.2307/1369650 CrossRefGoogle Scholar
  66. Swennen C (1976) Wadden seas are rare, hospitable and productive. In: Smart M (ed) Proceedings of the international conference on conservation of wetlands and waterfowl, Heiligenhafen. International Waterfowl Research Bureau, SlimbridgeGoogle Scholar
  67. Touw WG, Bayjanov JR, Overmars L, Backus L, Boekhorst J, Wels M, van Hijum SA (2012) Data mining in the life sciences with Random Forest: a walk in the park or lost in the jungle? Brief Bioinform 14:315–326.  https://doi.org/10.1093/bib/bbs034 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Underhill LG (1987) Waders (Charadrii) and other waterbirds at Langebaan Lagoon, South Africa, 1975–1986. Ostrich 58:145–155.  https://doi.org/10.1080/00306525.1987.9633896 CrossRefGoogle Scholar
  69. Vareschi E (1978) The ecology of the lake Nakuru (Kenya). I. Abundance and feeding of Lesser Flamingo. Oeclogia 32:11–35.  https://doi.org/10.1007/BF00344687 CrossRefGoogle Scholar
  70. Whalen MA, Duffy JE, Grace JB (2013) Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94(2):510–520.  https://doi.org/10.1890/12-0156.1 CrossRefPubMedGoogle Scholar
  71. Zajac RN (1985) The effects of sublethal predation on reproduction in the spionid polychaete Polydora ligni Webster. J Exp Mar Biol Ecol 88(1):1–19.  https://doi.org/10.1016/0022-0981(85)90197-2 CrossRefGoogle Scholar
  72. Zweers G, de Jong F, Berkhoudt H, Vanden Berge JC (1995) Filter feeding in Flamingos (Phoenicopterus ruber). Condor 97:297–324.  https://doi.org/10.2307/1369017 CrossRefGoogle Scholar
  73. Zydelis R, Richman SE (2015) Foraging behaviour, ecology, and energetics of sea ducks. In: Savard JPL, Derksen DV, Esler D, Eadie JM (eds) Ecology and conservation of North American Sea ducks. CRC Press, Boca RatonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological Science, Marine Research InstituteUniversity of Cape TownCape TownSouth Africa
  2. 2.Department of Statistical Sciences, Centre for Statistics in Ecology, Environment and ConservationUniversity of Cape TownCape TownSouth Africa

Personalised recommendations