Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  van Leeuwen, Casper H A ^a,b   van der Velde, Gerard ^b,c   van Lith, Bart ^a   Klaassen, Marcel ^a,d  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c NATURALIS BIODIVERSITY CENTER   (Netherlands)

^d DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANAS PLATYRHYNCHOS; ANIMAL BEHAVIOR; AQUATIC SPECIES; ARTICLE; BATHYOMPHALUS CONTORTUS; BIOLOGICAL TRAIT; BITHYNIA LEACHII; CALORIC INTAKE; CONTROLLED STUDY; DIGESTIVE SYSTEM; FECES ANALYSIS; FEEDING BEHAVIOR; HYDROBIA ULVAE; MALE; MIGRANT BIRD; NONHUMAN; ORGANISMAL INTERACTION; POPULATION DISPERSAL; POPULATION MOVEMENT PATTERN; POTAMOPYRGUS ANTIPODARUM; QUANTITATIVE STUDY; SNAIL; SURVIVAL TIME; WETLAND; ANIMAL; ANIMAL SHELL; DUCKS AND GEESE; EATING; FEMALE; GASTROINTESTINAL TRACT; HISTOLOGY; PARASITOLOGY; PHYSIOLOGY; POPULATION MIGRATION; TIME;

ALGAE; ANAS PLATYRHYNCHOS; AVES; GASTROPODA; HYDROBIA ULVAE; INVERTEBRATA;

ANIMAL MIGRATION; ANIMAL SHELLS; ANIMALS; ANSERIFORMES; AQUATIC ORGANISMS; EATING; FEMALE; GASTROINTESTINAL TRACT; MALE; SNAILS; TIME FACTORS;

EID: 84857776840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032292     Document Type: Article

References (79)

1. Darwin C, (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life London John Murray.
2. Kew H, (1893) The dispersal of shells: An inquiry into the means of dispersal possessed by fresh-water and land Mollusca London Kegan Paul, Trench, Trubner & Co.
3. Ridley HN, (1930) The distribution of plants throughout the world Ashord Reeve.
4. Levins R, (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bulletin of the ESA 15: 237-240.
5. Okamura B, Freeland JR, (2002) Gene flow and the evolutionary ecology of passively dispersing aquatic invertebrates. In: Bullock JM, Kenward RE, Hails RS, editors. Dispersal Ecology Oxford Blackwell Publishing pp. 194-216.
6. Brendonck L, Riddoch BJ, (1999) Wind-borne short-range egg dispersal in anostracans (Crustacea: Branchiopoda). Biol J Linn Soc 67: 87-95.
7. Caceres CE, Soluk DA, (2002) Blowing in the wind: a field test of overland dispersal and colonization by aquatic invertebrates. Oecologia 131: 402-408.
8. Nilsson C, Brown RL, Jansson R, Merritt DM, (2010) The role of hydrochory in structuring riparian and wetland vegetation. Biol Rev 85: 837-858.
9. Vanschoenwinkel B, Gielen S, Seaman M, Brendonck L, (2008) Any way the wind blows- frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos 117: 125-134.
10. Cousens RD, Hill J, French K, Bishop ID, (2010) Towards better prediction of seed dispersal by animals. Funct Ecol 24: 1163-1170.
11. Pollux BJA, (2011) The experimental study of seed dispersal by fish (ichthyochory). Freshw Biol 56: 197-212.
12. Bilton DT, Freeland JR, Okamura B, (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32: 159-181.
13. Figuerola J, Green AJ, (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47: 483-494.
14. Green AJ, Figuerola J, (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Divers Distrib 11: 149-156.
15. Kristiansen J, (1996) Dispersal of freshwater algae - a review. Hydrobiologia 336: 151-157.
16. Figuerola J, Green AJ, (2002) How frequent is external transport of seeds and invertebrate eggs by waterbirds? A study in Donana, SW Spain. Arch Hydrobiol 155: 557-565.
17. Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ, (2010) Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshw Biol 55: 1262-1273.
18. Raulings E, Morris KAY, Thompson R, Nally RM, (2011) Do birds of a feather disperse plants together? Freshw Biol 56: 1390-1402.
19. Atkinson KM, (1980) Experiments in dispersal of phytoplankton by ducks. Brit Phyc 15: 49-58.
20. Figuerola J, Green AJ, Black K, Okamura B, (2004) Influence of gut morphology on passive transport of freshwater bryozoans by waterfowl in Donana (southwestern Spain). Can J Zool 82: 835-840.
21. Charalambidou I, Santamaría L, (2005) Field evidence for the potential of waterbirds as dispersers of aquatic organisms. Wetlands 25: 252-258.
22. Green AJ, Sanchez MI, Amat F, Figuerola J, Hontoria F, et al. (2005) Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnol Oceanogr 50: 737-742.
23. Frisch D, Green AJ, (2007) Copepods come in first: rapid colonization of new temporary ponds. Fundam Appl Limn 168: 289-297.
24. Brochet AL, Gauthier-Clerc M, Guillemain M, Fritz H, Waterkeyn A, et al. (2010) Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia 637: 255-261.
25. Charalambidou I, Ketelaars HAM, Santamaría L, (2003) Endozoochory by ducks: influence of developmental stage of Bythotrephes diapause eggs on dispersal probability. Divers Distrib 9: 367-374.
26. Charalambidou I, Santamaría L, Figuerola J, (2003) How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts? Arch Hydrobiol 157: 547-554.
27. Soons MB, Van der Vlugt C, Van Lith B, Heil GW, Klaassen M, (2008) Small seed size increases the potential for dispersal of wetland plants by ducks. J Ecol 96: 619-627.
28. Cadée GC, (1988) Levende wadslakjes in bergeend faeces. Correspondentieblad van de Nederlandse Malacologische Vereniging 243: 443-444.
29. Green AJ, Sanchez MI, (2006) Passive internal dispersal of insect larvae by migratory birds. Biol Lett 2: 55-57.
30. Frisch D, Green AJ, Figuerola J, (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat Sci 69: 568-574.
31. Green AJ, Jenkins KM, Bell D, Morris PJ, Kingsford RT, (2008) The potential role of waterbirds in dispersing invertebrates and plants in arid Australia. Freshw Biol 53: 380-392.
32. Anders NR, Churchyard T, Hiddink JG, (2009) Predation of the shelduck Tadorna tadorna on the mud snail Hydrobia ulvae. Aquat Ecol 43: 1193-1199.
33. Cadée GC, (2011) Hydrobia as "Jonah in the whale": shell repair after passing through the digestive tract of shelducks alive. Palaios 26: 245-249.
34. Charalambidou I, Santamaría L, (2002) Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence. Acta Oecol 23: 165-176.
35. Proctor VW, Malone CR, DeVlaming V, (1967) Dispersal of aquatic organisms- viability of disseminules recovered from intestinal tract of captive killdeer. Ecology 48: 672-676.
36. Wesselingh FP, Cadée GC, Renema W, (1999) Flying high: on the airborne dispersal of aquatic organisms as illustrated by the distribution histories of the gastropod genera Tryonia and Planorbarius. Geol Mijnb 78: 165-174.
37. Albrecht C, Kroll O, Terrazas E, Wilke T, (2009) Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biol Invasions 11: 1821-1826.
38. Mills EL, Leach JH, Carlton JT, Secor CL, (1993) Exotic species in the Great Lakes- a history of biotic crises and anthropogenic introductions. J Gt Lakes Res 19: 1-54.
39. Stadler T, Frye M, Neiman M, Lively CM, (2005) Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail. Mol Ecol 14: 2465-2473.
40. Morley N, (2008) The role of the invasive snail Potamopyrgus antipodarum in the transmission of trematode parasites in Europe and its implications for ecotoxicological studies. Aquat Sci 70: 107-114.
41. Gittenberger E, Janssen AW, Kuijper WJ, Kuiper JG, Meijer T, et al. (2004) De Nederlandse zoetwatermollusken. Recente en fossiele weekdieren uit zoet en brak water. Utrecht: Nationaal Natuurhistorisch Museum Naturalis, European Invertebrate Survey-Nederland, KNNV Uitgeverij 2nd. ed. Nederlandse Fauna 2.
42. Alonso A, Castro-Diez P, (2008) What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614: 107-116.
43. Cramp S, Simmons KEL, (1977) The birds of the Western Palearctic: Volume 1 Oxford Oxford University Press.
44. Swanson GA, Meyer MI, Adomaitis VA, (1985) Foods consumed by breeding mallards on wetlands of south-central North Dakota. J Wildl Manag 49: 197-203.
45. Gruenhagen NM, Fredrickson LH, (1990) Food use by migratory female mallards in Northwest Missouri. J Wildl Manag 54: 622-626.
46. Baldwin JR, Lovvorn JR, (1994) Habitats and tidal accessibility of the marine foods of dabbling ducks and brant in Boundary Bay, British Columbia. Mar Biol 120: 627-638.
47. Rodrigues D, Figueiredo M, Fabiao A, (2002) Mallard (Anas platyrhynchos) summer diet in central Portugal rice-fields. Game Wildl Sci 10: 55-62.
48. Combs DL, Fredrickson LH, (1996) Foods used by male Mallards wintering in Southeastern Missouri. J Wildl Manag 60: 603-610.
49. Whilde A, (1977) The autumn and winter food of Mallard, Anas p. platyrhynchos (L.) and some other Irish wildfowl. The Irish Naturalists' Journal 19: 18-21.
50. Charalambidou I, Santamaría L, Jansen C, Nolet BA, (2005) Digestive plasticity in mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Funct Ecol 19: 513-519.
51. R-Development-Core-Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL Available: http://www.R-project.org.
52. Welham CVJ, (1994) Flight speeds of migrating birds- a test of maximum range speed predictions from 3 aerodynamic equations. Behav Ecol 5: 1-8.
53. Bruderer B, Boldt A, (2001) Flight characteristics of birds: I. radar measurements of speeds. Ibis 143: 178-204.
54. Bohonak AJ, Jenkins DG, (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6: 783-796.
55. Clauss M, Streich WJ, Schwarm A, Ortmann S, Hummel J, (2007) The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116: 209-216.
56. Clench MH, Mathias JR, (1995) Motility responses to fasting in the gastrointestinal-tract of 3 avian species. Condor 97: 1041-1047.
57. Figuerola J, Charalambidou I, Santamaría L, Green AJ, (2010) Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns. Naturwissenschaften 97: 555-565.
58. Traveset A, (1998) Effect of seed passage through vertebrate frugivores' guts on germination: a review. Perspect Plant Ecol Evol Syst 1: 151-190.
59. Traveset A, Rodriguez-Perez J, Pias B, (2008) Seed trait changes in dispersers' guts and consequences for germination and seedling growth. Ecology 89: 95-106.
60. Gibson JS, (1970) Function of operculum of Thais lapillus (L.) in resisting desiccation and predation. J Anim Ecol 39: 159-168.
61. Malone CR, (1965) Dispersal of freshwater gastropods by waterbirds. MSc thesis Texas Texas Technological College.
62. DeVlaming V, Proctor VW, (1968) Dispersal of aquatic organisms- viability of seeds revovered from droppings of captive killdeer and mallard ducks. Am J Bot 55: 20-26.
63. Castro G, Stoyan N, Myers JP, (1989) Assimilation efficiency in birds: A function of taxon or food type? Comp Biochem Physiol A Comp Physiol 92: 271-278.
64. Prop J, Vulink T, (1992) Digestion by barnacle geese in the annual cycle- the interplay between retention time and food quality. Funct Ecol 6: 180-189.
65. Afik D, Karasov WH, (1995) The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76: 2247-2257.
66. Evans PR, Herdson DM, Knights PJ, Pienkowski MW, (1979) Short-term effects of reclamation of part of Seal Sands, Teesmouth, on wintering waders and Shelduck. Oecologia 41: 183-206.
67. Zwarts L, Blomert AM, (1992) Why knot Calidris canutus take medium-sized Macoma balthica when 6 prey species are available. Mar Ecol Prog Ser 83: 113-128.
68. Boag DA, (1986) Dispersal in pond snails- potential role of waterfowl. Can J Zool Rev Can Zool 64: 904-909.
69. Newell R, (1962) Behavioural aspects of the ecology of Peringia (= Hydrobia) ulvae (Pennant) (Gasteropoda, Prosobranchia). Proc Zool Soc Lond 138: 49-75.
70. Hohenlohe PA, (2004) Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around Point Conception, California. Biol J Linn Soc 82: 169-187.
71. Wada S, Kawakami K, Chiba S, (2012) Snails can survive passage through a bird's digestive system. J Biogeogr 39: 69-73.
72. Campbell JW, (1947) The food of some British Wildfowl. Ibis 89: 429-432.
73. Charalambidou I, Santamaría L, Langevoord O, (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Funct Ecol 17: 747-753.
74. Pollux BJA, Santamaría L, Ouborg NJ, (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshw Biol 50: 232-242.
75. Figuerola J, Green AJ, Santamaría L, (2003) Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Glob Ecol Biogeogr 12: 427-436.
76. Figuerola J, Green AJ, Santamaría L, (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. J Ecol 90: 989-1001.
77. Kehoe FP, Ankney CD, Alisauskas RT, (1988) Effects of dietary fiber and diet diversity on digestive organs of captive mallards (Anas platyrhynchos). Can J Zool Rev Can Zool 66: 1597-1602.
78. Karasov WH, Levey DJ, (1990) Digestive-system trade-offs and adaptations of frugivorous passerine birds. Physiol Zool 63: 1248-1270.
79. Malone CR, (1965) Dispersal of plankton: Rate of food passage in mallard ducks. J Wildl Manag 29: 529-533.