Biogeochemistry

, Volume 130, Issue 1–2, pp 13–30 | Cite as

Base metal fluxes from fig trees to soil on Barro Colorado Island, Panama: potential contribution of the common frugivorous bat Artibeus jamaicensis

  • Tobias Messmer
  • Matthias Wiggenhauser
  • Hilario Espinosa Ortega
  • Larissa Albrecht
  • Marco Tschapka
  • Wolfgang Wilcke
Article

Abstract

The contribution of animals to element fluxes in ecosystems is little known. We therefore estimated the contribution of a common frugivorous bat species (Phyllostomidae: Artibeus jamaicensis) to the base metal fluxes (Ca, Mg, and K) from fig trees to soil in a tropical lowland forest on Barro Colorado Island (BCI) because figs provide large parts of the Ca required by these mammals. We chose three individual old-growth fig trees on each of four geological units of BCI varying in soil exchangeable base metal concentrations. To assess element fluxes, we determined internal base metal cycling via canopy exchange and litterfall, external input through bulk and dry deposition, and contributions of bats through pellets and bat faeces as well as element absorption in bats. Assuming a consumption of 20 % of the total fig production by A. jamaicensis, total mean fluxes from fig trees to soil were 24 ± 7 g m−2 year−1 for Ca, 4.6 ± 1.6 for Mg, and 21 ± 4 for K, respectively. The largest part of Ca and Mg was cycled as bulk litterfall (79 ± 9 and 62 ± 15 %, respectively) and of K as canopy leaching (56 ± 12 %). A. jamaicensis contributed 1.7 ± 0.5, 2.3 ± 0.6, and 6.1 ± 1.8 % to the total fluxes of Ca, Mg and K under fig trees, respectively. The contribution of A. jamaicensis to the base metal fluxes below the fig canopy was similar to that of bulk deposition. Our results demonstrate that the contribution of a single frugivorous mammal species to internal base metal cycling in a tropical ecosystem may be similarly important as bulk deposition and can have measurable effects on local soil fertility.

Keywords

Artibeus jamaicensis Canopy budget Ficus insipida Keystone species Litterfall Panama Species-specific nutrient cycling Tropical lowland forest 

References

  1. Albrecht L (2012) The role of figs in the nutritional landscape of the common fruit-eating bat Artibeus jamaicensis on Barro Colorado Island, Panamá. PhD Thesis. University of Ulm, GermanyGoogle Scholar
  2. Ballestrini R, Arisci S, Brizzio MC, Mosello R, Rogora M, Tagliaferri A (2007) Dry deposition of particles and canopy exchange: Comparison of wet, bulk and throughfall deposition at five forest sites in Italy. Atmos Environ 41:745–756CrossRefGoogle Scholar
  3. Barclay RMR (1994) Constraints on reproduction by flying vertebrates: energy and calcium. Am Nat 144:1021–1031CrossRefGoogle Scholar
  4. Barthold FK, Stallard RF, Elsenbeer H (2008) Soil nutrient–landscape relationships in a lowland tropical rainforest in Panama. For Ecol Manage 255:1135–1148CrossRefGoogle Scholar
  5. Bonaccorso FJ (1979) Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum. Biol Sci 4:359–408Google Scholar
  6. Cavelier J, Jaramillo M, Solis D, de León D (1997) Water balance and nutrient inputs in bulk precipitation in tropical montane cloud forest in Panama. J Hydrol 193:83–96CrossRefGoogle Scholar
  7. Chapin FS III (1980) The Mineral Nutrition of Wild Plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  8. Clark DB, Clark DA, Read JM (1998) Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J Ecol 86:101–112CrossRefGoogle Scholar
  9. Clark DB, Palmer MW, Clark DA (1999) Edaphic factors and the landscape-scale distributions of tropical rain forest trees. Ecology 80:2662–2675CrossRefGoogle Scholar
  10. Coley PD, Barone JA (1996) Herbivory and plant defences in Tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  11. Condit R, Engelbrecht BMJ, Pino D, Pérez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci USA 110:5064–5068CrossRefGoogle Scholar
  12. Dent DH, Bagchi R, Robinson D, Majalap-Lee N, Burslem DFRP (2006) Nutrient fluxes via litterfall and leaf litter decomposition vary across a gradient of soil nutrient supply in a lowland tropical rain forest. Plant Soil 288:197–215CrossRefGoogle Scholar
  13. Dieter D, Elsenbeer H, Turner BL (2010) Phosphorus fractionation in lowland tropical rainforest soils in central Panama. Catena 82:118–125CrossRefGoogle Scholar
  14. DIN ISO 19730 (2008) Soil quality—Extraction of trace elements from soil using ammonium nitrate solutionGoogle Scholar
  15. Feely KJ, Terborg JW (2005) The effects of herbivore density on soil nutrients and tree growth in tropical forest fragments. Ecology 86:116–124CrossRefGoogle Scholar
  16. Fonte SJ, Schowalter TD (2005) The Influence of a neotropical herbivore (Lamponius portoricensis) on nutrient cycling and soil processes. Oecologia 146:423–431CrossRefGoogle Scholar
  17. Foster RB, Brokaw NVL (1996) Structure and history of the vegetation of Barro Colorado Island. In: Leigh EG, Rand AS, Windsor DM (eds) The ecology of a tropical forest: Seasonal rhythms and long-term changes. Smithsonian Institute Press, Washington, DC, pp 67–82Google Scholar
  18. Golley F, McGinnis JT, Clements RG, Child GI, Duever MJ (1976) Mineral cycling in a tropical moist forest ecosystem. University of Georgia Press, AthensGoogle Scholar
  19. Handley CO, Leigh EG (1991) Diet and food supply. In: Handley CO, Wilson DO, Gardner AL (eds.). Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panamá. Smithsonian Contribution to Zoology 511, Smithsonian Institution Press, Washington, DC, pp 147–149.Google Scholar
  20. Handley CO, Morrison DW (1991) Foraging behaviour. In Handley CO, Wilson DO, Gardner AL (eds.). Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panamá. Smithsonian Contribution to Zoology 511, Smithsonian Institution Press, Washington, DC, pp 137–140Google Scholar
  21. Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. J Ecol 89:947–959CrossRefGoogle Scholar
  22. Hofhansl F, Wanek W, Drage S, Huber W, Weissenhofer A, Richter A (2011) Topography strongly affects atmospheric deposition and canopy exchange processes in different types of wet lowland rainforest, Southwest Costa Rica. Biogeochemistry 106:371–396CrossRefGoogle Scholar
  23. Holdridge LR, Budowski G (1956) Report of an ecological survey of the Republic of Panama. Caribb For 17:92–110Google Scholar
  24. Hollinger DY (1986) Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia 70:291–297CrossRefGoogle Scholar
  25. Hölscher D, Köhler L, Leuschner C, Kappelle M (2003) Nutrient fluxes in stemflow and throughfall in three successional stages of an upper montane rain forest in Costa Rica. J Trop Ecol 19:557–565CrossRefGoogle Scholar
  26. Hunter MD, Adl S, Pringle CM, Coleman DC (2003) Relative effects of macroinvertebrates and habitat on the chemistry of litter during decomposition. Pedobiologica 47:101–115CrossRefGoogle Scholar
  27. Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51CrossRefGoogle Scholar
  28. John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB (2006) Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci USA 104:864–869CrossRefGoogle Scholar
  29. Johnsson MJ, Stallard RF (1989) Physiographic controls on the composition of sediments derived from volcanic and sedimentary terrains on Barro Colorado Island, Panama. J Sed Res 59:768–781CrossRefGoogle Scholar
  30. Jordan CF (1978) Stem flow and nutrient transfer in a tropical rain forest. Oikos 31:257–263CrossRefGoogle Scholar
  31. Kalko EKV, Herre EA, Handley CO (1996) Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. J Biogeogr 23:565–576CrossRefGoogle Scholar
  32. Korine C, Kalko EKV, Herre EA (2000) Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs. Oecologia 123:560–568CrossRefGoogle Scholar
  33. Kwiecinski GG, Falzone M, Studier EH (2003) Milk concentration and postnatal accretion of minerals and nitrogen in two phyllostomid bats. J Mammal 84:926–936CrossRefGoogle Scholar
  34. Leigh EG (1999) Tropical forest ecology: a view from Barro Colorado Island. Oxford University Press, New YorkGoogle Scholar
  35. Levia DF, Frost EE (2003) A review and evaluation of stemflow literature in the hydrologic and biogeochemical cycles of forested and agricultural ecosystems. J Hydrol 274:1–29CrossRefGoogle Scholar
  36. Levia DF, Frost EE (2006) Variability of throughfall volume and solute inputs in wooded ecosystems. Prog Phys Geogr 30:605–632CrossRefGoogle Scholar
  37. Likens GE, Eaton JE (1970) A polyurethane stemflow collector for trees and shrubs. Ecology 51(938):939Google Scholar
  38. Lilienfein J, Wilcke W (2004) Water and element input into native, agri- and silvicultural ecosystems of the Brazilian savanna. Biogeochemistry 67:183–212CrossRefGoogle Scholar
  39. Macinnis-Ng CMO, Flores EE, Müller H, Schwendenmann L (2012) Rainfall partitioning into throughfall and stemflow and associated nutrient fluxes: land use impacts in a lower montane tropical region of Panama. Biogeochemistry 111:661–676CrossRefGoogle Scholar
  40. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  41. McDonald MA, Healey JR (2000) Nutrient cycling in secondary forests in the Blue Mountains of Jamaica. For Ecol Manage 139:257–278CrossRefGoogle Scholar
  42. McDowell WH (1998) Internal nutrient fluxes in a Puerto Rican rain forest. J Trop Ecol 14:521–536CrossRefGoogle Scholar
  43. McDowell WH, Likens GE (1988) Origin, composition, and flux of dissolved organic carbon in the Hubbard Brook Valley. Ecol Monogr 58:177–195CrossRefGoogle Scholar
  44. McLaughlin SB, Wimmer R (1999) Calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417CrossRefGoogle Scholar
  45. Messmer T, Elsenbeer H, Wilcke W (2014) High exchangeable calcium concentrations in soils on Barro Colorado Island, Panama. Geoderma 218:212–224CrossRefGoogle Scholar
  46. Michalzik B, Stadler B (2005) Importance of canopy herbivores to dissolved and particulate organic matter fluxes to the forest floor. Geoderma 127:227–236CrossRefGoogle Scholar
  47. Morrison DW (1978) Foraging ecology and energetics of the frugivorous bat Artibeus jamaicensis. Ecology 59:716–723CrossRefGoogle Scholar
  48. Nagy K, Milton K (1979) Energy metabolism and food consumption by howler monkeys. Ecology 60:475–480CrossRefGoogle Scholar
  49. O’Brien TG, Kinnaird MF, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC (1998) What’s so special about figs? Nature 392:668CrossRefGoogle Scholar
  50. Parker GG (1983) Throughfall and stemflow in the forest nutrient cycle. Adv Ecol Res 13:57–133CrossRefGoogle Scholar
  51. Potter CS, Ragsdale HL, Swank WT (1991) Atmospheric deposition and foliar leaching in a regenerating southern Appalachian forest canopy. J Ecol 79:97–115CrossRefGoogle Scholar
  52. Proctor J (1983) Mineral nutrients in tropical forests. Progr Phys Geogr 7:422–431CrossRefGoogle Scholar
  53. Radzi Abas M, Ahmad-Shah A, Nor Awang M (1992) Fluxes of ions in precipitation, throughfall and stemflow in an urban forest in Kuala Lumpur, Malaysia. Environ Pollut 75:209–213CrossRefGoogle Scholar
  54. Reynolds BC, Hunter MD (2001) Responses of soil respiration, soil nutrients, and litter decomposition to inputs from canopy herbivores. Soil Biol Biochem 33:1641–1652CrossRefGoogle Scholar
  55. Sayer EJ, Tanner EVT (2010) Experimental investigation of the importance of litterfall in lowland semi-evergreen tropical forest nutrient cycling. J Ecol 98:1052–1062CrossRefGoogle Scholar
  56. Stadler B, Michalzik B, Müller T (1998) Linking aphid ecology and ecosystem processes: the effect of spatial and temporal variability in aphid abundance on nutrient fluxes in a coniferous forest. Ecology 79:1514–1525CrossRefGoogle Scholar
  57. Stadler B, Solinger S, Michalzik B (2001) Insect herbivores and the nutrient flow from the canopy to the soil. Oecologia 126:104–113CrossRefGoogle Scholar
  58. Staelens J, Houle D, de Schrijver A, Neirynk J, Verheyen K (2008) Calculating dry deposition and canopy exchange with the canopy budget model: review of assumptions and application to two deciduous forests. Water Air Soil Pollut 191:149–169CrossRefGoogle Scholar
  59. Stern AA, Kunz TH, Studier EH, Oftedal OT (1997) Milk composition and lactational output in the greater spear-nosed bat, Phyllostomus hastatus. J Comp Physiol B 167:389–398CrossRefGoogle Scholar
  60. Stevenson PR, Guzmán-Caro DC (2010) Nutrient transport within and between habitats through seed dispersal processes by woolly monkeys in north-western Amazonia. Am J Primatol 72:992–1003CrossRefGoogle Scholar
  61. Studier EH, Kunz TH (1995) Accretion of nitrogen and minerals in suckling bats, Myotis velifer and Tadarida brasiliensis. J Mammal 76:32–42CrossRefGoogle Scholar
  62. Studier EH, Sevick SH, Ridley DM, Wilson DE (1994) Mineral and nitrogen concentrations in faeces of some Neotropical bats. J Mammal 75:674–680CrossRefGoogle Scholar
  63. Tanner EVJ (1980) Litterfall in montane rain forests of Jamaica and its relation to climate. J Ecol 68:833–848CrossRefGoogle Scholar
  64. Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 330–344Google Scholar
  65. Terborgh J, Wright SJ (1994) Effects of mammalian herbivores on plant recruitment in two Neotropical forests. Ecology 75:1829–1833CrossRefGoogle Scholar
  66. Tukey HB (1970) The leaching of substances from plants. Annu Rev Plant Phys 21:305–324CrossRefGoogle Scholar
  67. Ulrich B (1983) Interactions of forest canopies with atmospheric constituents: SO2, alkali and earth alkali cations and chloride. In: Ulrich B, Pankrath J (eds) Effects of accumulation of air pollutants in forest ecosystems. D. Reidel Publishing, Dordrecht, pp 33–45CrossRefGoogle Scholar
  68. Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 6:285–298CrossRefGoogle Scholar
  69. Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167CrossRefGoogle Scholar
  70. Wendelin MC, Runkle JR, Kalko EKV (2000) Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489–501CrossRefGoogle Scholar
  71. Wieder RK, Wright SJ (1995) Tropical forest litter dynamics and dry season irrigation on Barro Colorado Island, Panama. Ecology 76:1971–1979CrossRefGoogle Scholar
  72. Windsor DM (1990) Climate and moisture availability in a tropical forest: long-term environmental records from Barro Colorado Island, Panama. Smithsonian Contributions to Earth Sciences. Smithsonian Institution Press, Washington, DCGoogle Scholar
  73. Wolf A, Doughty CE, Malhi Y (2013) Lateral diffusion of nutrients by mammalian herbivores in a terrestrial ecosystem. PLoS One 8:1–10Google Scholar
  74. Woodring WP (1958) Geology of Barro Colorado Island, Canal Zone. Smithson Misc Collect 135:1–39Google Scholar
  75. Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625CrossRefGoogle Scholar
  76. Yavitt JB, Wright SJ, Wieder K (2004) Seasonal drought and dry-season irrigation influence leaf-litter nutrients and soil enzymes in a moist, lowland forest in Panama. Austral Ecol 29:177–188CrossRefGoogle Scholar
  77. Zimmermann A, Uber M, Zimmermann B, Levia DF (2015) Predictability of stemflow in a species-rich tropical forest. Hydrol Process 29:4947–4956CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Institute of GeographyUniversity of BernBernSwitzerland
  2. 2.Institute of Agricultural SciencesETH ZurichLindauSwitzerland
  3. 3.Smithsonian Tropical Research InstituteBalboaPanama
  4. 4.Institute of Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  5. 5.Institute of Geography and GeoecologyKarlsruhe Institute of Technology (KIT)KarlsruheGermany

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