Long-distance seed dispersal by straw-coloured fruit bats varies by season and landscape

Global Ecology and Conservation

Volumn 7, Issue , 2016, Pages 12-24

  Abedi Lartey, Michael ^a,b,c   Dechmann, Dina K N ^a,b   Wikelski, Martin ^a,b,c   Scharf, Anne K ^a,b,c   Fahr, Jakob ^a,b  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c University of Konstanz   (Germany)

Author keywords

Eidolon; Foraging; Fragmentation; Gut passage; Seasonality

Indexed keywords

EID: 84964994954     PISSN: None     EISSN: 23519894     Source Type: Journal    
DOI: 10.1016/j.gecco.2016.03.005     Document Type: Article

References (77)

1. Alcantara J., Rey P., Valera F., Sanchez-Lafuente A. Factors shaping the seedfall pattern of a bird-dispersed plant. Ecology 2000.
2. Amelon S.K., Dalton D.C., Millspaugh J.J., Wolf S.A. Radiotelemetry; techniques and analysis. Ecological and Behavioral Methods for the Study of Bats 2009, 57-77. The Johns Hopkins University Press, Baltimore. T. Kunz, S. Parsons (Eds.).
3. Anderson J.T., Nuttle T., Saldaña Rojas J.S., Pendergast T.H., Flecker A.S. Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc. Biol. Sci. 2011, 278:3329-3335. 10.1098/rspb.2011.0155.
4. Ayensu, E.S., 1974. Plant and bat interactions in West Africa. Ann. Missouri Bot. Gard. Vol. 61, No. 3. (accessed 22.12.14). http://www.jstor.org/stable/2395025?seq%3D1#page_scan_tab_contents.
5. Bacles C.F.E., Lowe A.J., Ennos R.A. Effective seed dispersal across a fragmented landscape. Science 2006, 311:628. 10.1126/science.1121543.
6. Baker K.S., Todd S., Marsh G.A., Crameri G., Barr J., Kamins A.O., Peel A.J., Yu M., Hayman D.T.S., Nadjm B., Mtove G., Amos B., Reyburn H., Nyarko E., Suu-Ire R., Murcia P.R., Cunningham A.a., Wood J.L.N., Wang L.-F. Novel, potentially zoonotic paramyxoviruses from the African straw-colored fruit bat Eidolon helvum. J. Virol. 2013, 87:1348-1358.
7. Baldwin J.W., Whitehead S.R. Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats. Oecologia 2015, 177:453-466. 10.1007/s00442-014-3096-2.
8. Blake S., Deem S.L., Mossimbo E., Maisels F., Walsh P. Forest elephants: tree planters of the Congo. Biotropica 2009, 41:459-468. 10.1111/j.1744-7429.2009.00512.x.
9. Cain M.L., Milligan B.G., Strand A.E. Long-distance seed dispersal in plant populations. Am. J. Bot. 2000, 87:1217-1227.
10. Campbell M.O.N. Traditional forest protection and woodlots in the coastal savannah of Ghana. Environ. Conserv. 2004, 31:225-232. 10.1017/S0376892904001389.
11. Campos-Arceiz A., Blake S. Megagardeners of the forest-The role of elephants in seed dispersal. Acta Oecol. 2011, 37:542-553. 10.1016/j.actao.2011.01.014.
12. Clark J.S., Lewis M., McLachlan J.S., HilleRisLambers J. Estimating population spread: what can we forecast and how well?. Ecology 2003, 84:1979-1988. 10.1890/01-0618.
13. Clauss M., Streich W.J., Nunn C.L., Ortmann S., Hohmann G., Schwarm A., Hummel J. The influence of natural diet composition, food intake level, and body size on ingesta passage in primates. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2008, 150:274-281. 10.1016/j.cbpa.2008.03.012.
14. Damschen E.I., Brudvig L.A., Haddad N.M., Levey D.J., Orrock J.L., Tewksbury J.J. The movement ecology and dynamics of plant communities in fragmented landscapes. Proc. Natl. Acad. Sci. USA 2008, 105:19078-19083. 10.1073/pnas.0802037105.
15. de la Peña-Domene M., Martínez-Garza C., Palmas-Pérez S., Rivas-Alonso E., Howe H.F. Roles of birds and bats in early tropical-forest restoration. PLoS One 2014, 9:e104656. 10.1371/journal.pone.0104656.
16. Delignette-Muller M.L., Dutang C. fitdistrplus: An R Package for fitting distributions. J. Stat. Softw. 2015, 64:1-34.
17. Devineau J.-L. Seasonal rhythms and phenological plasticity of savanna woody species in a fallow farming system (south-west Burkina Faso). J. Trop. Ecol. 1999, 15:497-513.
18. Fahr J., Abedi-Lartey M., Esch T., Machwitz M., Suu-Ire R., Wikelski M., Dechmann D.K.N. Pronounced seasonal changes in the movement ecology of a highly gregarious central-place forager, the African straw-coloured fruit bat (Eidolon helvum). PLoS One 2015, 10:e0138985. 10.1371/journal.pone.0138985.
19. Fahr J., Kalko E.K.V. Biome transitions as centres of diversity: habitat heterogeneity and diversity patterns of West African bat assemblages across spatial scales. Ecography 2011, 34:177-195. (Cop.). 10.1111/j.1600-0587.2010.05510.x.
20. Foley J.A., Defries R., Asner G.P., Barford C., Bonan G., Carpenter S.R., Chapin F.S., Coe M.T., Daily G.C., Gibbs H.K., Helkowski J.H., Holloway T., Howard E.A., Kucharik C.J., Monfreda C., Patz J.A., Prentice I.C., Ramankutty N., Snyder P.K. Global consequences of land use. Science 2005, 309:570-574.
21. Fritz S.A., Purvis A. Phylogenetic diversity does not capture body size variation at risk in the world's mammals. Proc. Biol. Sci. 2010, 277:2435-2441. 10.1098/rspb.2010.0030.
22. Fujita M.S., Tuttle M.D. Flying foxes (Chiroptera: Pteropodidae): Threatened animals of key ecological and economic importance. Conserv. Biol. 1991, 5:455-463. 10.1111/j.1523-1739.1991.tb00352.x.
23. Gannon W.L., Sikes R.S. Guidelines of the American society of mammalogists for the use of wild mammals in research. J. Mammal. 2007, 88:809-823. Animal care and use committee of the ASM. 10.1644/06-MAMM-F-185R1.1.
24. Hall J.B., Swaine M.D. Classification and ecology of closed-canopy forest in Ghana. J. Ecol. 1976, 64:913-951.
25. Hamilton, M.B., 1999. Tropical tree gene flow and seed dispersal 401, pp. 129-130. http://dx.doi.org/10.1038/43597.
26. Hayman D.T.S., McCrea R., Restif O., Suu-Ire R., Fooks A.R., Wood J.L.N., Cunningham A.A., Rowcliffe J.M. Demography of straw-colored fruit bats in Ghana. J. Mammal. 2012, 93:1393-1404. 10.1644/11-MAMM-A-270.1.
27. Hayman D.T.S., Yu M., Crameri G., Wang L.-F., Suu-Ire R., Wood J.L.N., Cunningham A.a. Ebola virus antibodies in fruit bats, Ghana, West Africa. Emerg. Infect. Diseases 2012, 18:1207-1209. 10.3201/eid1807.111654.
28. Heer K., Albrecht L., Kalko E.K.V. Effects of ingestion by neotropical bats on germination parameters of native free-standing and strangler figs (Ficus sp., Moraceae). Oecologia 2010, 163:425-435. 10.1007/s00442-010-1600-x.
29. Hilton T.E. The Accra plains: Landforms of a coastal savanna of Ghana. Z. Geomorphol. 1966, 10:369-386.
30. Hodgkison R., Balding S.T., Zubaid A., Kunz T.H. Fruit Bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest. Biotropica 2003, 35:491-502. 10.1111/j.1744-7429.2003.tb00606.x.
31. Huggel-Wolf H., Huggel-Wolf M.L. Biology of Eidolon helvum Kerr (Megachiroptera). Acta Trop. 1965, 22:1-10.
32. Jenik J., Hall J.B. Plant communities of the Accra plains, Ghana. Folia Geobot. Phytotaxon. 1976, 11:163-212.
33. Kamins A.O., Restif O., Ntiamoa-Baidu Y., Suu-Ire R., Hayman D.T.S., Cunningham A.A., Wood J.L.N., Rowcliffe J.M. Uncovering the fruit bat bushmeat commodity chain and the true extent of fruit bat hunting in Ghana, West Africa. Biol. Cons. 2011, 144:3000-3008.
34. Kays R., Jansen P.A., Knecht E.M.H., Vohwinkel R., Wikelski M. The effect of feeding time on dispersal of Virola seeds by toucans determined from GPS tracking and accelerometers. Acta Oecol. 2011, 37:625-631. 10.1016/j.actao.2011.06.007.
35. Kunz T.H., Braun de Torrez E., Bauer D., Lobova T., Fleming T.H. Ecosystem services provided by bats. Ann. New York Acad. Sci. 2011, 1223:1-38. 10.1111/j.1749-6632.2011.06004.x.
36. Lenz J., Fiedler W., Caprano T., Friedrichs W., Gaese B.H., Wikelski M., Böhning-Gaese K. Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. Proc. Biol. Sci. 2011, 278:2257-2264. 10.1098/rspb.2010.2383.
37. Marshall A.G. Old World phytophagous bats (Megachiroptera) and their food plants: a survey. Zool. J. Linn. Soc. 1985, 83:351-369. 10.1111/j.1096-3642.1985.tb01181.x.
38. Mayaux P., Holmgren P., Achard F., Eva H., Stibig H.-J., Branthomme A. Tropical forest cover change in the 1990s and options for future monitoring. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:373-384. 10.1098/rstb.2004.1590.
39. McConkey K.R., Prasad S., Corlett R.T., Campos-Arceiz A., Brodie J.F., Rogers H., Santamaria L. Seed dispersal in changing landscapes. Biol. Cons. 2012, 146:1-13. 10.1016/j.biocon.2011.09.018.
40. McCullough J., Alonso L.E., Naskrecki P., Wright H.E., Osei-Owusu Y. A Rapid Biological Assessment of the Atewa Range Forest Reserve, Eastern Ghana 2007, Conservation International, Washington, D.C., 248 pp.
41. Mueller T., Lenz J., Caprano T., Fiedler W., Böhning-Gaese K., Elphick C. Large frugivorous birds facilitate functional connectivity of fragmented landscapes. J. Appl. Ecol. 2014.
42. Munin R., Costa P.da, Fischer E. Differential ingestion of fig seeds by a Neotropical bat, Platyrrhinus lineatus. Mammal. Biol. Z. für Säugetierkd. 2011, 76:772-774.
43. Muscarella R., Fleming T.H. The role of frugivorous bats in tropical forest succession. Biol. Rev. Camb. Philos. Soc. 2007, 82:573-590. 10.1111/j.1469-185X.2007.00026.x.
44. Nakashima Y., Sukor J.A. Importance of common palm civets (Paradoxurus hermaphroditus) as a long-distance disperser for large-seeded plants in degraded forests. Tropics 2010, 18:221-229. 10.3759/tropics.18.221.
45. Nathan R. Long-distance dispersal of plants. Science 2006, 313:786-788. 10.1126/science.1124975.
46. Nathan R., Perry G., Cronin J.T., Strand A.E., Cain M.L. Methods for estimating long-distance dispersal. Oikos 2003, 103:261-273. 10.1034/j.1600-0706.2003.12146.x.
47. Nathan R., Schurr F.M., Spiegel O., Steinitz O., Trakhtenbrot A., Tsoar A. Mechanisms of long-distance seed dispersal. Trends Ecol. Evol. 2008, 23:638-647. 10.1016/j.tree.2008.08.003.
48. Oleksy R., Racey P.A., Jones G. High-resolution GPS tracking reveals habitat selection and the potential for long-distance seed dispersal by Madagascan flying foxes Pteropus rufus. Glob. Ecol. Conserv. 2015, 3:678-692. 10.1016/j.gecco.2015.02.012.
49. O'Mara M.T., Wikelski M., Dechmann D.K.N. 50 years of bat tracking: device attachment and future directions. Methods Ecol. Evol. 2014, 5:311-319. 10.1111/2041-210X.12172.
50. Ossa G., Kramer-Schadt S., Peel A.J., Scharf A.K., Voigt C.C. The movement ecology of the straw-colored fruit bat, Eidolon helvum, in Sub-Saharan Africa assessed by stable isotope ratios. PLoS One 2012, 7. e45729.
51. Ozawa H., Watanabe A., Uchiyama K., Saito Y., Ide Y. Influence of long-distance seed dispersal on the genetic diversity of seed rain in fragmented Pinus densiflora populations relative to pollen-mediated gene flow. J. Hered. 2013, 104:465-475. 10.1093/jhered/est022.
52. Peel A.J., Sargan D.R., Baker K.S., Hayman D.T.S., Barr J.a., Crameri G., Suu-Ire R., Broder C.C., Lembo T., Wang L.-F., Fooks A.R., Rossiter S.J., Wood J.L.N., Cunningham A.a. Continent-wide panmixia of an African fruit bat facilitates transmission of potentially zoonotic viruses. Nature Commun. 2013, 4:2770.
53. Rautenbach I.L. A new technique for the efficient use of Macro-Mistnets. Koedoe 1986, 28:81-86. 10.4102/koedoe.v28i1.538.
54. R Development Core Team, 2015. R: A language and environment for statistical computing.
55. Richter H.V., Cumming G.S. Food availability and annual migration of the straw-colored fruit bat (Eidolon helvum). J. Zool. 2006, 268:35-44. 10.1111/j.1469-7998.2005.00020.x.
56. Richter H.V., Cumming G.S. First application of satellite telemetry to track African straw-coloured fruit bat migration. J. Zool. 2008, 275:172-176. 10.1111/j.1469-7998.2008.00425.x.
57. Roberts B.J., Catterall C.P., Eby P., Kanowski J. Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS One 2012, 7:e42532. 10.1371/journal.pone.0042532.
58. Rosevear, D.R., The Bats of West Africa. Trustees of the British Museum (Natural History), 1965.
59. Ruckdeschel P., Kohl M. General purpose convolution algorithm in S4 classes by means of FFT. J. Stat. Softw. 2014, 59:1-25.
60. Russo S.E., Portnoy S., Augspurger C.K. Incorporating animal behavior into seed dispersal models: Implications for seed shadows. Ecology 2006, 87:3160-3174. 10.1890/0012-9658(2006)87[3160:IABISD]2.0.CO;2.
61. Scanlon A.T., Petit S., Tuiwawa M., Naikatini A. High similarity between a bat-serviced plant assemblage and that used by humans. Biol. Cons. 2014, 174:111-119. 10.1016/j.biocon.2014.03.023.
62. Schupp E.W. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 1993, 107-108:15-29.
63. Seltzer C.E., Ndangalasi H.J., Cordeiro N.J. Seed dispersal in the dark: shedding light on the role of fruit bats in Africa. Biotropica 2013, 45:450-456. 10.1111/btp.12029.
64. Shilton L.A., Altringham J.D., Compton S.G., Whittaker R.J. Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc. R. Soc. B Biol. Sci. 1999, 266:219-223. 10.1098/rspb.1999.0625.
65. Taylor D.A.R., Kankam B.O., Wagner M.R. The role of fruit bat, Eidolon helvum, in seed dispersal, survival, and germination in Milicia excelsa, a threatened West African hardwood. Research Advances in Restoration of Iroko as a Commercial Species in West Africa 2000, 29-39. Forestry Research Institute of Ghana (FORIG), Kumasi, Ghana. J.R. Cobbinah, M.R. Wagner (Eds.).
66. Thomas D.W. The annual migrations of three species of West African fruit bats (Chiroptera: Pteropodidae). Can. J. Zool. 1983, 61:2266-2272. 10.1139/z83-299.
67. Tsoar A., Shohami D., Nathan R. A movement ecology approach to study seed dispersal and plant invasion: an overview and application of seed dispersal by fruit bats. Fifty Years of Invasion Ecology: The Legacy of Charles Elton 2010, 103-119. Wiley-Blackwell, Oxford, UK. 10.1002/9781444329988.ch9. D.M. Richardson (Ed.).
68. Tsuji Y., Yangozene K., Sakamaki T. Estimation of seed dispersal distance by the bonobo, Pan paniscus, in a tropical forest in Democratic Republic of Congo. J. Trop. Ecol. 2009, 26:115. 10.1017/S0266467409990290.
69. Van Houtan K.S., Pimm S.L., Halley J.M., Bierregaard R.O., Lovejoy T.E. Dispersal of Amazonian birds in continuous and fragmented forest. Ecol. Lett. 2007, 10:219-229.
70. Wahaj S.A., Levey D.J., Sanders A.K., Cipollini M.L. Control of gut retention time by secondary metabolites in ripe solanum fruits. Ecology 1998, 79:2309-2319. 10.1890/0012-9658(1998)079[2309:COGRTB]2.0.CO;2.
71. Wang B.C., Smith T.B. Closing the seed dispersal loop. Trends Ecol. Evol. 2002, 17:379-386. 10.1016/S0169-5347(02)02541-7.
72. Webala P.W., Musila S., Makau R. Roost occupancy, roost site selection and diet of straw-coloured fruit bats (Pteropodidae: Eidolon helvum) in western Kenya: the need for continued public education. Acta Chiropt. 2014, 16:85-94. 10.3161/150811014X683291.
73. Wenny D.G. Advantages of seed dispersal: A re-evaluation of directed dispersal. Evol. Ecol. Res. 2001, 3:51-74.
74. Westcot D.A., Dennis A.J., Preston C., Watts J.H., Crossman N.D. Incorporating dispersal ecology into the management of plant invasions. 15th Australian Weeds Conference, Papers and Proceedings, Adelaide, South Australia, 24-28 September 2006: Managing Weeds in a Changing Climate 2006, 80-82. Weed Management Society of South Australia.
75. Westcott D., Bentrupperbäumer J., Bradford M.G., McKeown A. Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. Oecologia 2005, 146:57-67.
76. Whitehead S.R., Quesada M.F.O., Bowers M.D. Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats. Oikos 2015, 10.1111/oik.02210.
77. Willson M.F. Dispersal mode, seed shadows, and colonization patterns. Vegetatio 1993, 107-108:261-280. 10.1007/BF00052229.