Skip to main content

Advertisement

SpringerLink
Log in

Interspecific variation in the diets of herbivores in an industrial environment: implications for exposure to fluoride emissions

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Atmospheric fluorides (gaseous and particulate) are deposited on, and absorbed by, vegetation. Ingested fluoride accumulates in calcified tissues of vertebrates, and if it is excessive, it may lead to dental and skeletal fluorosis. The prevalence, form and severity of the effects vary greatly between species. Foraging strategy can be an important determinant of fluoride exposure in herbivores, because foliar fluoride concentrations vary between plant species, for example, according to vertical and lateral position in the vegetation. We combined microhistological analysis of diet and analysis of foliar fluoride levels to examine interspecific variation in dietary fluoride exposure of macropodid marsupials (swamp wallaby Wallabia bicolor, red-necked wallaby Notamacropus rufogriseus and eastern grey kangaroo Macropus giganteus), in the buffer zone of an aluminium smelter in Victoria, Australia. Dietary niche differentiation between species was evident. The swamp wallaby and the red-necked wallaby were browsers or mixed feeders, depending on the classification system used. The eastern grey kangaroo was a grazer, consuming almost entirely grasses. However, foliar fluoride did not vary significantly between the main plant groups consumed. Our results indicate that interspecific variation in diet at this site is unlikely to explain variation in fluoride exposure.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arnesen AKM (1997) Availability of fluoride to plants grown in contaminated soils. Plant Soil 191:13–25

    Article  CAS  Google Scholar 

  • Boivin G, Chavassieux P, Chapuy MC, Baud CA, Meunier PJ (1990) Skeletal fluorosis: histomorphometric findings. J Bone Miner Res 5:S185–S189

    Article  Google Scholar 

  • Boulton IC, Cooke JA, Johnson MS (1994) Fluoride accumulation and toxicity in wild small mammals. Environ Pollut 85:161–167

    Article  CAS  Google Scholar 

  • Bowen SE (1988) Spatial and temporal patterns in the fluoride content of vegetation around two aluminum smelters in the Hunter Valley, New-South-Wales. Sci Total Environ 68:97–111

    Article  CAS  Google Scholar 

  • Carlson KJ, Jashashvili T, Houghton K, Westaway MC, Patel BA (2013) Joint loads in marsupial ankles reflect habitual bipedalism versus quadrupedalism. PLoS One 8:1–9

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Coulson G, Hill J, McKenzie J, Walters B (2000) The Smelter in the Park: managing wildlife for biodiversity. In: Craig JL, Mitchell N, Saunders DA (eds) Nature conservation 5: nature conservation in production environments: managing the matrix. Surrey Beatty & Sons, Chipping Norton, pp 360–371

    Google Scholar 

  • Crompton AW, Owerkowicz T, Skinner J (2010) Masticatory motor pattern in the koala (Phascolarctos cinereus): a comparison of jaw movements in marsupial and placental herbivores. J Exp Zool Part A A 313(A):564–578

    Article  Google Scholar 

  • Davis NE, Coulson G, Forsyth DM (2008) Diets of native and introduced mammalian herbivores in shrub-encroached grassy woodland, south-eastern Australia. Wildl Res 35:684–694

    Article  Google Scholar 

  • Davison AW (1983) Uptake, transport and accumulation of soil and airborne fluorides by vegetation. In: Shupe JL, Peterson HB, Leone MC (eds) Fluorides: effects on vegetation, animals and humans. Paragon Press, Salt Lake City, pp 61–82

    Google Scholar 

  • Davison AW, Blakemore J, Craggs C (1979) The fluoride content of forage as an environmental quality standard for the protection of livestock. Environ Pollut 20:279–296

    Article  CAS  Google Scholar 

  • Davison AW, Rand AW, Betts WE (1973) Measurement of atmospheric fluoride concentrations in urban areas. Environ Pollut 5:23–33

    Article  CAS  Google Scholar 

  • De Lange HJ, Lahr J, Van der Pol JJ, Wessels Y, Faber JH (2009) Ecological vulnerability in wildlife: an expert judgment and multicriteria analysis tool using ecological traits to assess relative impact of pollutants. Environ Toxicol Chem 28:2233–2240

    Article  Google Scholar 

  • Death CE, Coulson G, Kierdorf U, Kierford H, Morris W, Hufschmid J (2015) Dental fluorosis and skeletal fluoride content as biomarkers of excess fluoride exposure in marsupials. Sci Total Environ 533:528–541

    Article  CAS  Google Scholar 

  • Death CE (2016) Industrial fluoride toxicosis in Australian marsupials. PhD Thesis, The University of Melbourne.

  • Di Stefano J, Newell GR (2008) Diet selection by the swamp wallaby (Wallabia bicolor): feeding strategies under conditions of changed food availability. J Mammal 89:1540–1549

    Article  Google Scholar 

  • Di Stefano J, York A, Swan M, Greenfield A, Coulson G (2009) Habitat selection by the swamp wallaby (Wallabia bicolor) in relation to diel period, food and shelter. Austral Ecol 34:143–155

    Article  Google Scholar 

  • Divan AM Jr, Oliva MA, Ferreira FA (2008) Dispersal pattern of airborne emissions from an aluminium smelter in Ouro Preto, Brazil, as expressed by foliar fluoride accumulation in eight plant species. Ecol Indic 8:454–461

    Article  CAS  Google Scholar 

  • Doley D (1986) Plant-fluoride relationships. Bookbuilders Ltd, Hong Kong

    Google Scholar 

  • Ellis BA, Russell EM, Dawson TJ, Harrop CJF (1977) Seasonal changes in the diet preferences of free-ranging red kangaroos, euros and sheep in Western NSW. Aust Wildl Res 4:127–144

    Article  Google Scholar 

  • Everett ET (2011) Fluoride’s effects on the formation of teeth and bones, and the influence of genetics. J Dental Res 90:552–560

    Article  CAS  Google Scholar 

  • Fejerskov O, Thylstrup A, Larsen MJ (1977) Clinical and structural features and possible pathogenic mechanisms of dental fluorosis. Scand J Dent Res 85:510–534

    CAS  Google Scholar 

  • Forsyth DM, Davis NE (2011) Diets of non-native sambar deer in Australia estimated by macroscopic versus microhistological rumen analysis. J Wildl Manag 75:1488–1497

    Article  Google Scholar 

  • Garrott RA, Eberhardt LL, Otton JK, White PJ, Chaffee MA (2002) A geochemical trophic cascade in Yellowstone’s geothermal environments. Ecosystems 5:659–666

    Article  CAS  Google Scholar 

  • Gleeson J, Gleeson D (2012) Reducing the impacts of development on wildlife. CSIRO Publishing, Melbourne

    Google Scholar 

  • Green K, Davis NE, Robinson WA (2014a) Diet of the broad-toothed rat Mastacomys fuscus (Rodentia:Muridae) in the alpine zone of the Snowy Mountains, Australia. Aust Zool 37:225–233

    Article  Google Scholar 

  • Green K, Davis NE, Robinson WA (2014b) Does diet constrain the occupation of high elevations by macropods? A comparison between Macropus rufogriseus and Wallabia bicolor. Aust Mammal 36:219–228

    Google Scholar 

  • Green K, Davis NE, Robinson WA, McAuliffe J, Good RB (2013) Diet selection by European hares (Lepus europaeus) in the alpine zone of the Snowy Mountains, Australia. Eur J Wildl Res 59:693–703

    Article  Google Scholar 

  • Hansen RM, Mugambi MM, Bauni SM (1985) Diets and trophic ranking of ungulates in the Northern Serengeti. J Wildl Manag 49:823–829

    Article  Google Scholar 

  • Harrington J (1976) The diet of the swamp wallaby, Wallabia bicolor, at Diamond Flat. PhD, University of New England, New South Wales

    Google Scholar 

  • Hill GJE (1978) Preliminary assessment of defecation patterns for the eastern grey kangaroo (Macropus giganteus). Aust Zool 19:291–300

    Google Scholar 

  • Hofmann RR, Stewart DRM (1972) Grazer or browser: a classification based on the stomach-structure and feeding habits of East African ruminants. Mammalia 36:226–240

    Article  Google Scholar 

  • Hollis CJ, Robertshaw JD, Harden RH (1986) Ecology of the swamp wallaby (Wallabia bicolor) in northeastern New South Wales.1. Diet. Aust Wildl Res 13:355–365

    Article  Google Scholar 

  • Horn HS (1966) Measurement of "overlap" in comparative ecological studies. Am Nat 100:419–424

    Article  Google Scholar 

  • Hufschmid J, Beveridge I, Coulson G, Gould J (2011) Bone fluoride concentrations of eastern grey kangaroos (Macropus giganteus) resident near an aluminium smelter in south-eastern Australia. Ecotoxicology 20:1378–1387

    Article  CAS  Google Scholar 

  • Hufschmid J, Beveridge I, Coulson G, Walker G, Shen P, Reynolds E, Charles J (2015) Skeletal pathology of eastern grey kangaroos (Macropus giganteus) exposed to high environmental fluoride levels in south-eastern Australia. J Comp Pathol 153:167–184

    Article  CAS  Google Scholar 

  • Jarman PJ, Phillips CM (1989) Diets in a community of macropod species. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat-kangaroos, vol 1. Surrey Beatty and Sons, Chipping Norton, pp 143–149

    Google Scholar 

  • Kierdorf H, Kierdorf U, Sedlacek F, Erdelen M (1996a) Mandibular bone fluoride levels and occurrence of fluoride induced dental lesions in populations of wild red deer (Cervus elaphus) from central Europe. Environ Pollut 93:75–81

    Article  CAS  Google Scholar 

  • Kierdorf U, Bahelkova P, Sedlacek F, Kierdorf H (2012) Pronounced reduction of fluoride exposure in free-ranging deer in North Bohemia (Czech Republic) as indicated by the biomarkers skeletal fluoride content and dental fluorosis. Sci Total Environ 414:686–695

    Article  CAS  Google Scholar 

  • Kierdorf U, Kierdorf H (1999) Dental fluorosis in wild deer: its use as a biomarker of increased fluoride exposure. Environ Monit Assess 57:265–275

    Article  CAS  Google Scholar 

  • Kierdorf U, Kierdorf H, Fejerskov O (1993) Fluoride-induced developmental changes in enamel and dentine of European roe deer (Capreolus capreolus L.) as a result of environmental pollution. Arch Oral Bio 38:1071–1081

    Article  CAS  Google Scholar 

  • Kierdorf U, Kierdorf H, Sedlacek F, Fejerskov O (1996b) Structural changes in fluorosed dental enamel of red deer (Cervus elaphus L.) from a region with severe environmental pollution by fluorides. J Anat 188:183–195

    Google Scholar 

  • Kinhill (1980) Alcoa Portland Aluminium smelter. Environmental Effects Statement and Draft Environmental Impact Statement, Melbourne

    Google Scholar 

  • Lundholm JT, Richardson PJ (2010) Habitat analogues for reconciliation ecology in urban and industrial environments. J Appl Ecol 47:966–975

    Article  Google Scholar 

  • MacLean DC, Schneider RE, Weinstein LH (1969) Accumulation of fluoride by forage crops. Contrib Boyce Thompson Inst PI Res 7:165–166

    Google Scholar 

  • Mallett KJ, Cooke BD (1986) The ecology of the common wombat in South Australia. Nature Conservation Society of South Australia, Adelaide

    Google Scholar 

  • McBee K, Bickham JW (1990) Mammals as bioindicators of environmental toxicity. In: Genoways HH (ed) Current Mammalogy, vol 2. Plenum Press, New York and London, pp 37–82

    Google Scholar 

  • Merchant JC (2008) Swamp wallaby (Wallabia bicolor). In: Van Dyck S, Strahan R (eds) The mammals of Australia, 3rd edn. Reed New Holland, Sydney, pp 404–405

    Google Scholar 

  • Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons. Clarendon Press, Oxford

    Google Scholar 

  • Mitchell AD, Dowling BJ, Scheltema JH (1981) The effects of gaseous fluoride on Australian vegetation.1. Results of an 8 year sampling program in the vicinity of an aluminum smelter. Clean Air 15:28–32

    Google Scholar 

  • Murphy CE, Sinclair TR, Knoerr KR (1977) An assessment of the use of forests as sinks for the removal of atmospheric sulphur dioxide. J Environ Qual 6:388–396

    Article  CAS  Google Scholar 

  • Murray F (1981) Effects of fluorides on plant communities around an aluminium smelter. Environ Pollut A, Ecol Biol 24:45–56

    Article  CAS  Google Scholar 

  • Murray F (1982) Ecosystems as sinks for atmospheric fluoride. In: Fluoride emissions: their monitoring and effects on vegetation and ecosystems. Academic Press Australia, Sydney, pp 191–205

    Google Scholar 

  • Narayan D, Agrawal M, Pandey J, Singh J (1994) Changes in vegetation characteristics downwind of an aluminium factory in India. Ann Bot 73:557–565

    Article  Google Scholar 

  • Newman J, Newman RK, Schreiber (1988) Air pollution and wildlife toxicology: an overlooked problem. Environ Toxicol Chem 7:381–390

    Article  CAS  Google Scholar 

  • Norbury GL (1988) Microscopic analysis of herbivore diets—a problem and a solution. Aust Wildl Res 15:51–57

    Article  Google Scholar 

  • NPI (2014) National Pollutant Inventory, Fluoride compounds from all sources, 2013/2014 data within Australia. http://www.npi.gov.au/npidata/action/load/individual-facility-detail/criteria/state/null/year/2014/jurisdiction-facility/00004729. Accessed June 30th 2015

  • O’Connor JA, Horsman DC (1982) Fluoride levels in vegetation and ambient air in the Portland (Victoria) area. In: Murray F (ed) Fluoride emissions: their monitoring and effects on vegetation and ecosystems. Academic Press, Sydney, pp 77–92

    Google Scholar 

  • Osawa R (1990) Feeding strategies of the swamp wallaby, Wallabia bicolor, on North Stradbroke Island, Queensland. I: composition of diets. Aust Wildl Res 17:615–621

    Article  Google Scholar 

  • Palamara J, Phakey PP, Rachinger WA, Sanson GD, Orams HJ (1984) On the nature of the opaque and translucent enamel regions of some macropodinae (Macropus giganteus, Wallabia bicolor and Peradorcas concinna). Cell Tissue Res 238:329–337

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ (2003) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • R Core Team. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria, 2014.

  • Ross PS, De Swart RL, Van Loveren H, Osterhaus ADME, Vos JG (1996) The immunotoxicity of environmental contaminants to marine wildlife: a review. Annu Rev Fish Dis 6:151–165

    Article  Google Scholar 

  • Salatas JH, Booth PN, Gard NW, O’Boyle RA, Mackay CE (2009) Risk assessment as a decision-making tool for treatment of emissions at a new aluminum smelter in Iceland: 3. Ecological assessment. Hum Ecol Risk Assess 15:469–502

    Article  CAS  Google Scholar 

  • Sanson GD (1989) Morphological adaptations of teeth to diets and feeding in the Macropodoidea. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat-kangaroos, vol 1. Surrey Beatty and Sons, Chipping Norton, pp 151–168

    Google Scholar 

  • Schultz M, Kierdorf U, Sedlacek F, Kierdorf H (1998) Pathological bone changes in the mandibles of wild red deer (Cervus elaphus L.) exposed to high environmental levels of fluoride. J Anat 193:431–442

    Article  CAS  Google Scholar 

  • Shupe JL (1980) Clinicopathologic features of fluoride toxicosis in cattle. J Anim Sci 51:746–758

    CAS  Google Scholar 

  • Shupe JL, Olson AE, Peterson HB, Low JB (1984) Fluoride toxicosis in wild ungulates. J Am Vet Med 185:1295–1300

    CAS  Google Scholar 

  • Smith WH (1974) Air pollution—effects on the structure and function of the temperate forest ecosystem. Environ Pollut 6:111–129

    Article  CAS  Google Scholar 

  • Southwell C (1987) Activity pattern of the eastern grey-kangaroo, Macropus giganteus. Mammalia 51:211–223

    Article  Google Scholar 

  • Sprent JA, McArthur C (2002) Diet and diet selection of two species in the macropodid browser-grazer continuum: do they eat what they ‘should’? Aust J Zool 50:183–192

    Article  Google Scholar 

  • Storr GM (1961) Microscopic analysis of faeces, a technique for ascertaining the diet of herbivorous mammals. A J Biol Sci 14:157–165

    Google Scholar 

  • Suttie JS, Dickie R, Clay AB, Nielsen P, Mahan WE, Baumann DP, Hamilton RJ (1987) Effects of fluoride emissions from a modern primary aluminum smelter on a local population of white-tailed deer (Odocoileus virginianus). J Wildl Dis 23:135–143

    Article  CAS  Google Scholar 

  • Suttie JW (1969) Fluoride content of commercial dairy concentrates and alfalfa forage. J Ag Food Chem 17:1350–1352

    Article  CAS  Google Scholar 

  • Suttie JW (1980) Nutritional aspects of fluoride toxicosis. J Anim Sci 51:759–766

    CAS  Google Scholar 

  • Taylor R (1983) The diet of the eastern grey kangaroo and wallaroo in areas of improved and native pasture in the New England tablelands. Wildl Res 10:203–211

    Article  Google Scholar 

  • USEPA (1979) Primary Aluminium Draft Guidelines for control of fluoride emissions from existing primary aluminium plants. United States Environmental Protection Agency. Office of air quality planning and standards, North Carolina

    Google Scholar 

  • USEPA (1993) Wildlife exposure factors handbook vol 1. USEPA, Washington D.C

    Google Scholar 

  • Vikøren T, Stuve G (1996) Fluoride exposure in cervids inhabiting areas adjacent to aluminum smelters in Norway. II Fluorosis. J Wildl Dis 32:181–189

    Article  Google Scholar 

  • Vikøren T, Stuve G, Frøslie A (1996) Fluoride exposure in cervids inhabiting areas adjacent to aluminum smelters in Norway. I Residue levels. J Wildl Dis 32:169–180

    Article  Google Scholar 

  • Walton KC (1984) Fluoride in fox bone near an aluminium reduction plant in Anglesey, Wales, and elsewhere in the United Kingdom. Environ Pollut, B 7:273–280

    Article  CAS  Google Scholar 

  • Weatherell JA, Weidmann SM (1959) The skeletal changes of chronic experimental fluorosis. J Pathol Bacteriol 78:233–241

    Article  CAS  Google Scholar 

  • Weinstein LH, Davison AW (2003) Native plant species suitable as bioindicators and biomonitors for airborne fluoride. Environ Pollut 125:3–11

    Article  CAS  Google Scholar 

  • Weinstein LH, Davison AW (2004) Fluoride in the environment. CABI Publishing, Oxon

    Google Scholar 

  • Weir A, McLeod J, Adams CE (1995) The winter diet and parasitic fauna of a population of red-necked wallabies Macropus rufogriseus recently introduced to Scotland. Mammal Rev 25:111–116

    Article  Google Scholar 

  • WHO (2000) Fluorides - Air Quality Guidelines. WHO, Copenhagen

    Google Scholar 

  • Wood MS (2002) Resource partitioning in sympatric populations of red-necked and black wallabies. PhD Thesis, Deakin University

Download references

Acknowledgments

We thank Jodie Gould (Portland Aluminium) for technical assistance and contributions to the manuscript and Ron Jeffries (Portland Aluminium) for practical assistance. We would like to acknowledge assistance from Ian Beveridge, Catharina Vendl, Paul Benham and Ian Freeman (The University of Melbourne, Faculty of Veterinary and Agricultural Sciences). Portland Aluminium funded and provided logistical support for this research. Comments by two anonymous reviewers greatly improved the manuscript.

Author information

Authors and Affiliations

  1. School of BioSciences, The University of Melbourne, Melbourne, Victoria, Australia

    Naomi E. Davis & Graeme Coulson

  2. Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

    Clare E. Death & Jasmin Hufschmid

  3. Portland Aluminium, Quarry Rd, Portland, Victoria, Australia

    Lora Newby

Authors
  1. Naomi E. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Clare E. Death
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Graeme Coulson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lora Newby
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jasmin Hufschmid
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naomi E. Davis.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davis, N.E., Death, C.E., Coulson, G. et al. Interspecific variation in the diets of herbivores in an industrial environment: implications for exposure to fluoride emissions. Environ Sci Pollut Res 23, 10165–10176 (2016). https://doi.org/10.1007/s11356-016-6234-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6234-z

Keywords

Search

Navigation