Skip to main content

Advertisement

Log in

Pattern of natural 15N abundance in lakeside forest ecosystem affected by cormorant-derived nitrogen

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Waterbirds are one of the most important groups of organisms inhabiting the land–water interface, especially with regard to mediating the transport of materials from the aquatic to the terrestrial environment. The great cormorant (Phalacrocorax carbo) is a colonial piscivorous bird that transports nutrients from fresh water to forest. We measured cormorant-derived nitrogen at two nesting colonies on the Isaki Peninsula and Chikubu Island at Lake Biwa, Japan, and analyzed the long-term effects of cormorant colonization on the forest nitrogen cycle, and the mechanisms of nitrogen retention. Three sites were examined in each colony: a currently occupied area, a previously occupied but now abandoned area, and a control area never colonized by cormorants. High nitrogen stable isotope ratios of cormorant excreta, the forest floor, mineral soil, and living plants showed cormorant-derived nitrogen in both occupied and abandoned areas. The relationship between δ15N and N content showed that the high δ15N of the excreta and N turnover in the soil were important at the occupied sites, whereas high δ15N of litter was important at the abandoned sites. Physiological changes of various organisms are also important for the N decomposition process. In conclusion, cormorant-derived nitrogen remains in the forest ecosystem as a result of two cormorant activities: heavy deposition of excreta and collection of nitrogen-rich nest material. Colony stage (occupied, abandoned, or never inhabited) and historical change of N decomposition process of an area can be identified from the relationship between δ15N and N content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • J. D. Aber W. McDowell K. Nadelhoffer A. Magill G. Berntson M. Kamakea S. McNulty W. Currie L. Rustad I. Fernandez (1998) ArticleTitleNitrogen saturation in temperate forest ecosysytems: hypotheses revisited BioScience 48 921–934 Occurrence Handle10.2307/1313296

    Article  Google Scholar 

  • R. Amundson W. T. Baisden (2000) Stable isotope tracers and mathematical models in soil organic matter studies O. E. Sala (Eds) et al. Methods in Ecosystem Science Springer-Verlag New York 117–137

    Google Scholar 

  • E. G. Bligh W. J. Dyer (1959) ArticleTitleA rapid method of total lipid extraction and purification Canadian Journal of Biochemistry and Physiology 37 911–917 Occurrence Handle13671378 Occurrence Handle1:CAS:528:DyaG1MXhtVSgt70%3D

    PubMed  CAS  Google Scholar 

  • J. M. Bremner (1996) N-Total D. L. Sparks (Eds) et al. Methods of Soil Analysis. Part 3. SSSA Book Ser. 5 SSSA & ASA Madison 1085–1121

    Google Scholar 

  • S. R. Carpenter N. F. Caraco D. L. Correll R. W. Howarth A. N. Sharpley V. H. Smith (1998) ArticleTitleNonpoint pollution of surface waters with phosphorus and nitrogen Ecological Applications 8 559–568 Occurrence Handle10.2307/2641247

    Article  Google Scholar 

  • P. D. Erskine D. M. Bergstrom S. Schmidt G. R. Stewart C. E. Tweedie J. D. Shaw (1998) ArticleTitleSubantarctic Macquarie Island – a model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance Oecologia 117 187–193 Occurrence Handle10.1007/s004420050647

    Article  Google Scholar 

  • R. D. Evans J. R. Ehleringer (1993) ArticleTitleA break in the nitrogen cycle in aridlands? Evidence from δ15N of soils Oecologia 94 314–317 Occurrence Handle10.1007/BF00317104

    Article  Google Scholar 

  • S. Fujiwara A. Takayanagi (2001) ArticleTitleThe influence of the common cormorant (Phalacrocorax carbo hanedae Kuroda) on forest decline Applied Forest Science 10 85–90

    Google Scholar 

  • C. T. Garten SuffixJr. (1993) ArticleTitleVariations in foliar 15N abundance and the availability of soil nitrogen on Walker Branch Watershed Ecology 74 2098–2113 Occurrence Handle10.2307/1940855

    Article  Google Scholar 

  • M. E. Gillham (1956) ArticleTitleEcology of the Pembrokeshire Islands V. Manuring by the colonial seabirds and mammals, with a note on seed distribution by gulls Journal of Ecology 44 429–454 Occurrence Handle10.2307/2256831

    Article  Google Scholar 

  • S. Hobara K. Koba T. Osono N. Tokuchi A. Ishida K. Kameda (2005) ArticleTitleNitrogen and phosphorus enrichment and balance in forests colonized by cormorants: implications of the influence of soil adsorption Plant & Soil 268 89–101 Occurrence Handle10.1007/s11104-004-0231-6 Occurrence Handle1:CAS:528:DC%2BD2MXks1ers7s%3D

    Article  CAS  Google Scholar 

  • S. Hobara T. Osono K. Koba N. Tokuchi S. Fujiwara K. Kameda (2001) ArticleTitleForest floor quality and N transformations in a temperate forest affected by avian-derived N deposition Water, Air, and Soil Pollution 130 679–684 Occurrence Handle10.1023/A:1013869115132

    Article  Google Scholar 

  • K. A. Hobson R. G. Clark (1992) ArticleTitleAssessing avian diets using stable isotopes I: turnover of 13C in tissues Condor 94 181–188

    Google Scholar 

  • K. Hobson J. F. Piatt J. Pitocchelli (1994) ArticleTitleUsing stable isotopes to determine seabird trophic relationships Journal of Animal Ecology 63 786–798 Occurrence Handle10.2307/5256

    Article  Google Scholar 

  • International Lake Environment Committee Foundation (ILEC), 1995. Compact-size Edition of Data Book of World Lake Environments – A Survey of the State of World Lakes – Asia and Oceania. Miyagawa Printing Co. Ltd., Otsu, 672 pp

  • A. Ishida (1996a) ArticleTitleEffects of the common cormorant, Phalacrocorax carbo, on evergreen forests in two nest sites at Lake Biwa, Japan Ecological Research 11 193–200 Occurrence Handle10.1007/BF02347685

    Article  Google Scholar 

  • A. Ishida (1996b) ArticleTitleChanges of soil properties in the colonies of the common cormorant, Phalacrocorax carbo Journal of Forest Research 1 31–35 Occurrence Handle10.1007/BF02348337

    Article  Google Scholar 

  • A. Ishida T. Matsuzawa K. Kameda M. Narusue (2000) ArticleTitleThe population increase of the Great Cormorant Phalacrocorax carbo and its damaging effect on fisheries and trees in Japan – The present situation, the problems in each and future measures Strix 18 1–28

    Google Scholar 

  • K. Ishizuka (1966) ArticleTitleEcology of the ornithocoprophilous plant communities on breeding places of the black-tailed gull, Larus crassirostris, along the coast of Japan Ecological Review 16 229–244

    Google Scholar 

  • P. A. Johnsgard (1993) Cormorants, Darters, and Pelicans of the World Smithsonian Institution Press Washington 445

    Google Scholar 

  • K. Kameda A. Ishida M. Narusue (2003) ArticleTitleThe population increase of the Great Cormorant Phalacrocorax carbo hanedae in Japan: conflicts with fisheries and trees and future perspectives Vogelwelt 124 IssueIDSuppl. 27–33

    Google Scholar 

  • K. Kameda T. Matsubara H. Mizutani Y. Yamada (2002) ArticleTitleDiet and foraging site selection of the Great Cormorant in Japan Japanese Journal of Ornithology 51 12–28 Occurrence Handle10.3838/jjo.51.12

    Article  Google Scholar 

  • H. Kawanabe (1999) Biological and cultural diversities in Lake Biwa, an ancient lake H. Kawanabe G. W. Coulter A. C. Roosevelt (Eds) Ancient Lakes and People Kenobi Productions Ahent 17–41

    Google Scholar 

  • K. Koba N. Tokuchi E. Wada T. Nakajima G. Iwatsubo (1997) ArticleTitleIntermittent denitrification: the application of a 15N natural abundance method to a forested ecosystem Geochimica et Cosmochimica Acta 61 5043–5050 Occurrence Handle10.1016/S0016-7037(97)00284-6 Occurrence Handle1:CAS:528:DyaK1cXjsFem

    Article  CAS  Google Scholar 

  • K. Koba N. Tokuchi T. Yoshioka E. A. Hobbie G. Iwatsubo (1998) ArticleTitleNatural abundance of nitrogen−15 in a forest soil Soil Science Society of America Journal 62 778–781 Occurrence Handle1:CAS:528:DyaK1cXks1eqtrg%3D Occurrence Handle10.2136/sssaj1998.03615995006200030034x

    Article  CAS  Google Scholar 

  • K. Koba K. Takahashi A. Kohzu (1999) ArticleTitleA review of stable isotope studies of nitrogen dynamics in soil–plant systems in forest ecosystems Japanese Journal of Ecology 49 47–51

    Google Scholar 

  • K. Koba M. Hirobe L. Koyama A. Kohzu N. Tokuchi K. J. Nadelhoffer E. Wada H. Takeda (2003) ArticleTitleNatural 15N abundance of plants and soil N in a temperate coniferous forest Ecosystems 6 457–469 Occurrence Handle10.1007/s10021-002-0132-6 Occurrence Handle1:CAS:528:DC%2BD3sXotVemsLw%3D

    Article  CAS  Google Scholar 

  • L. Koyama N. Tokuchi (2003) ArticleTitleEffects of NO 3 availability on NO 3 use in seedlings of three woody shrub species Tree Physiology 23 281–288 Occurrence Handle12566264

    PubMed  Google Scholar 

  • H. J. Lindeboom (1984) ArticleTitleThe nitrogen pathway in a penguin rookery Ecology 65 269–277 Occurrence Handle10.2307/1939479 Occurrence Handle1:CAS:528:DyaL2cXhtFKkurk%3D

    Article  CAS  Google Scholar 

  • J. G. McColl J. Burger (1976) ArticleTitleChemical inputs by a colony of Franklin’s gulls nesting in cattails American Midland Naturalist 96 270–280 Occurrence Handle10.2307/2424068 Occurrence Handle1:CAS:528:DyaE2sXhsVGnsrs%3D

    Article  CAS  Google Scholar 

  • Y. Maesako (1997) ArticleTitleEffects of streaked shearwaters (Calonectris leucomelas) burrowing on the lucidophyllous forest in Ohshima Island, Japan Vegetation Science 14 61–74

    Google Scholar 

  • H. Mizutani E. Wada (1988) ArticleTitleNitrogen and carbon isotope ratios in seabird rookeries and their ecological implications Ecology 69 340–349 Occurrence Handle10.2307/1940432

    Article  Google Scholar 

  • H. Mizutani H. Hasegawa E. Wada (1986) ArticleTitleHigh nitrogen isotope ratio for soils of seabird rookeries Biogeochemistry 2 221–247 Occurrence Handle10.1007/BF02180160 Occurrence Handle1:CAS:528:DyaL28Xmt1Giu7g%3D

    Article  CAS  Google Scholar 

  • H. Mizutani Y. Kabaya P. J. Moors T. W. Speir G. L. Lyon (1991) ArticleTitleNitrogen isotope ratios identify deserted seabird colonies Auk 108 960–964

    Google Scholar 

  • C. P. H. Mulder S. N. Keall (2001) ArticleTitleBurrowing seabirds and reptiles: impacts on seeds, seedlings and soils in an island forest in New Zealand Oecologia 127 350–360 Occurrence Handle10.1007/s004420000600

    Article  Google Scholar 

  • K. J. Nadelhoffer B. Fry (1988) ArticleTitleControls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter Soil Science Society of America Journal 52 1633–1640 Occurrence Handle10.2136/sssaj1988.03615995005200060024x

    Article  Google Scholar 

  • K. J. Nadelhoffer B. Fry (1994) Nitrogen isotope studies in forest ecosystems K. Lajtha R. H. Michener (Eds) Stable Isotopes in Ecology and Environmental Science Blackwell Scientific Publications London 22–44

    Google Scholar 

  • K. Ohrui M. J. Mitchell (1997) ArticleTitleNitrogen saturation of Japanese forested watersheds Ecological Applications 7 391–401 Occurrence Handle10.2307/2269507

    Article  Google Scholar 

  • T. Osono S. Hobara S. Fujiwara K. Koba K. Kameda (2002) ArticleTitleAbundance, diversity, and species composition of fungal communities in a temperate forest affected by excreta of the Great Cormorant Phalacrocorax carbo Soil Biology & Biochemistry 34 1537–1547 Occurrence Handle10.1016/S0038-0717(02)00123-2 Occurrence Handle1:CAS:528:DC%2BD38Xps12ltrc%3D

    Article  CAS  Google Scholar 

  • G. A. Polis S. D. Hurd (1996) ArticleTitleLinking marine and terrestrial food webs: Allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities American Naturalist 147 396–423 Occurrence Handle10.1086/285858

    Article  Google Scholar 

  • G. A. Polis K. O. Winemiller (1996) Food Webs: Integration of Patterns & Dynamics Chapman & Hall New York 472

    Google Scholar 

  • G. A. Polis W. B. Anderson R. D. Holt (1997) ArticleTitleToward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs Annual Review of Ecology and Systematics 28 289–316 Occurrence Handle10.1146/annurev.ecolsys.28.1.289

    Article  Google Scholar 

  • G. V. N. Powell J. W. Fourqurean W. J. Kenworthy J. C. Zieman (1991) ArticleTitleBird colonies cause seagrass enrichment in a subtropical estuary: observational and experimental evidence Estuarine, Coastal and Shelf Science 32 567–579 Occurrence Handle10.1016/0272-7714(91)90075-M

    Article  Google Scholar 

  • D. Robinson (2001) ArticleTitleδ15N as an integrator of the nitrogen cycle Trends in Ecology and Evolution 16 153–162 Occurrence Handle11179580 Occurrence Handle10.1016/S0169-5347(00)02098-X

    Article  PubMed  Google Scholar 

  • Shiga Prefecture, 1997. Report of the Assessment of Vegetation Damage on Chikubu Island by the Great Cormorant. Shiga Prefecture, 110 pp. (in Japanese)

  • W. H. Schlesinger (1997) Biogeochemistry: An Analysis of Global Change Academic Press San Diego 588

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kayoko Kameda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kameda, K., Koba, K., Hobara, S. et al. Pattern of natural 15N abundance in lakeside forest ecosystem affected by cormorant-derived nitrogen. Hydrobiologia 567, 69–86 (2006). https://doi.org/10.1007/s10750-006-0052-0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-006-0052-0

Keywords

Navigation