Advertisement

Ecotoxicology

, Volume 25, Issue 3, pp 608–621 | Cite as

Effects of urban land-use on largescale stonerollers in the Mobile River Basin, Birmingham, AL

  • D. Iwanowicz
  • M. C. Black
  • V. S. Blazer
  • H. Zappia
  • W. Bryant
Article

Abstract

During the spring and fall of 2001 and the spring of 2002 a study was conducted to evaluate the health of the largescale stoneroller (Campostoma oligolepis) populations in streams along an urban land-use gradient. Sites were selected from a pool of naturally similar sub-basins (eco-region, basin size, and geology) of the Mobile River basin (MRB), using an index of urban intensity derived from infrastructure, socioeconomic, and land-use data. This urban land-use gradient (ULUG) is a multimetric indicator of urban intensity, ranging from 0 (background) to 100 (intense urbanization). Campostoma sp. have been used previously as indicators of stream health and are common species found in all sites within the MRB. Endpoints used to determine the effects of urban land-use on the largescale stoneroller included total glutathione, histology, hepatic apoptosis, condition factor and external lesions. Liver glutathione levels were positively associated with increasing urban land-use (r2 = 0.94). Histopathological examination determined that some abnormalities and lesions were correlated with the ULUG and generally increased in prevalence or severity with increasing urbanization. Liver macrophage aggregates were positively correlated to the ULUG. The occurrence of nucleosomal ladders (indicating apoptotic cell death) did not correspond with urban intensity in a linear fashion. Apoptosis, as well as prevalence and severity of a myxozoan parasite, appeared to have a hormetic dose–response relationship. The majority of the biomarkers suggested fish health was compromised in areas where the ULUG ≥ 36.

Keywords

Biomarkers Largescale stoneroller Campostoma Liver glutathione Urban land-use gradient (ULUG) 

Notes

Acknowledgments

The authors are grateful to Beth Frankenberry, Brian Caskey, Sue Hartley, Kristin Justice, Wyman Turner and Sandy Page for help in collecting the largescale stonerollers for our research. We would also like to thank Dr. Mark Myers, Dr. Jack Fournie, Bane Schill, and Dr. Christine Densmore for critical review of the draft manuscript. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

References

  1. Adams SM (2001) Biomarker/bioindicator response profiles of organisms can help differentiate between sources of anthropogenic stressors in aquatic ecosystems. Biomarkers 6:33–44CrossRefGoogle Scholar
  2. Arends MJ, Morris RG, Wyllie AH (1990) Apoptosis: the role of the endonuclease. Am J Pathol 136:593–608Google Scholar
  3. Atkins JB, Zappia H, Robinson JL, McPherson AK, Moreland RS, Johnston BF, Harvill JS (2004) Water quality in the Mobile River Basin, Alabama, Georgia, Mississippi, and Tennessee, 1999–2001: U.S. Geological Survey. Circular 1231:40Google Scholar
  4. Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834CrossRefGoogle Scholar
  5. Azevedo JS, Sarkis JES, Hortellani MA, Ladle RJ (2012) Are catfish (Arridae) effective bioindicators for Pb, Cd, Hg, Cu and Zn? Water Air Soil Pollut 223:3911–3922CrossRefGoogle Scholar
  6. Bailey GS, Goeger DE, Hendricks JD (1989) Factors influencing experimental carcinogenesis in laboratory fish models. In: Varanasi U (ed) Metabolism of polynuclear aromatic hydrocarbons in the aquatic environment. CRC Press, Boca Raton, pp 253–268Google Scholar
  7. Bellucci CJ, Becker ME, Beauchene M, Dunbar L (2013) Classifying the health of Connecticut streams using benthic macroinvertebrates with implications for water management. Environ Manag 51:1274–1283CrossRefGoogle Scholar
  8. Birge WJ, Proice DJ, Shaw JR, Wigginton C, Hogstrand C (2000) Metal body burden and biological sensors as ecological indicators. Environ Tox Chem 19:1199–1212CrossRefGoogle Scholar
  9. Blazer VS, Wolke RE, Brown J, Powell CA (1987) Piscine macrophage aggregate parameters as health monitors: effect of age, sex, relative weight, season and site quality in largemouth bass (Micropterus salmoides). Aquat Toxicol 10:199–215CrossRefGoogle Scholar
  10. Bryer PJ, Elliot JN, Willingham EJ (2006) The effects of coat tar-based paemet sealer on amphibian development and metamorphosis. Ecotoxicology 15:241–247CrossRefGoogle Scholar
  11. Burger J, Campbell KR, Campbell TS, Shukla T, Dixon C, Gochfeld M (2005) Use of central stonerollers (Cyprinidae: Campostoma anomalum) from Tennessee as a bioindicator of metal contamination. Environ Monit Assess 110:171–184CrossRefGoogle Scholar
  12. Calabrese EJ (2001) Apoptosis: biphasic dose responses. Crit Rev Toxicol 31:607–613CrossRefGoogle Scholar
  13. Calabrese EJ, Baldwin LA (2001a) U-shaped dose-response in biology, toxicology, and public health. Annu Rev Publ Health 22:15–33CrossRefGoogle Scholar
  14. Calabrese EJ, Baldwin LA (2001b) Hormesis: a generalizable and unifying hypothesis. Crit Rev Toxicol 31:353–424CrossRefGoogle Scholar
  15. Chang S, Zdanowicz VS, Murchelano RA (1998) Associations between liver lesions in winter flounder (Pleuronectes americanus) and sediment chemical contaminants from north-east United States estuaries. ICES J Mar Sci 55:954–969CrossRefGoogle Scholar
  16. Cohen J, Cohen P (1983) Applied multiple regression/correlation analysis for the behavioral science, 2nd edn. Lawrence Erlbaum Associates, Publishers, HillsdaleGoogle Scholar
  17. Colombo JC, Cappelletti N, Migoya MC, Speranza E (2007) Bioaccumulation of anthropoenic contaminants by detritivorous fish in the Río de la Plata estuary: 1-Aliphatic hydrocarbons. Chemosphere 68(11):2128–2135CrossRefGoogle Scholar
  18. Conners DE, Ringwood AH (2000) Effects of glutathione depletion on copper cytotoxicity in oysters (Crassostrea virginica). Aquat Toxicol 50:341–349CrossRefGoogle Scholar
  19. Cuffney TF, Zappia H, Giddings EMP, Coles JF (2005) Effects of urbanization on benthic macroinvertebrate assemblages in contrasting environmental settings: Boston, MA; Birmingham, AL; and Salt Lake City, UT. In: Brown LR, Gray RH, Hughes H, Meador MR (eds) Effects of urbanization on aquatic ecosystems. American Fisheries Society, Bethesda, pp 361–408Google Scholar
  20. DeLeve LD, Kaplowitz N (1991) Glutathione metabolism and its role in hepatotoxicity. Pharmacol Ther 52:287–305CrossRefGoogle Scholar
  21. Elkin K, Lanier S, Rebecca M (2013) The interrelationships of hydrology and biology in a Tennessee stream, USA. Ecohydrology 6:355–362CrossRefGoogle Scholar
  22. Fischer JD, Cleeton SH, Lyons TP, Miller JR (2012) Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 62:809–818CrossRefGoogle Scholar
  23. Fitzpatrick FA, WaiteIR, D’Arconte PJ, Meador MR, Maupin MA, Gurtz ME (1998). Revised methods for characterizing stream habitat in the National Water Quality Assessment Program: U.S. Geological Survey Water Resources Investigations Report 98-4052, p 67Google Scholar
  24. Giddings EA, Brown LR, Short TM, Meador MR (2006) Relation of fish communities to environmental conditions in urban streams of the Wasatch Front, Utah. West N Am Nat 66:155–168CrossRefGoogle Scholar
  25. Hester ET, Bauman KS (2013) Stream and retention pond thermal response to heated summer runoff from urban impervious surfaces. J Am Water Resour Assoc 49:328–342CrossRefGoogle Scholar
  26. Hill WR, Napolitano GE (1997) PCB Congener accumulation by periphyton, herbivores, and omnivores. Environ Contam Toxicol 32:449–455CrossRefGoogle Scholar
  27. Iannuzzi J, Butcher M, Iannuzzi T (2011) Evaluation of potential relationships between chemical contaminants in sediments and aquatic organisms from the lower Passaic River, New Jersey. Environ Toxicol Chem 30:1721–1728CrossRefGoogle Scholar
  28. Iwanowicz DD, Iwanowicz LR, Howerth EW, Schill WB, Blazer VS, Johnson RL (2013) Characterization of a new myxozoan species (Myxozoa: Myxobolidae: Myxosporea) in largescale stonerollers (Campostoma oligolepis) from the Mobile river basin (Alabama). J Parasitol 99:102–111CrossRefGoogle Scholar
  29. Johnson GC, Kidd RE, Journey CA, Zappia H, Atkins JB (2002) Environmental setting and water quality issues of the Mobile River basin, Alabama, Georgia, Mississippi, and Tennessee. Water Resource Inv Report 02-4162, Us Geological Survey, p 62Google Scholar
  30. Jonas WB (2001) The future of hormesis: what is the clinical relevance of hormesis? Crit Rev Toxicol 31:655–658CrossRefGoogle Scholar
  31. Kim JH, Oh HM, Kim IS, Lim BJ, An KG (2013) Ecological health assessments of an urban lotic ecosystem using a multimetric model along with physical habitat and chemical water quality assessments. Int J Environ Res 7:759–768Google Scholar
  32. Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanogr 44:925–931CrossRefGoogle Scholar
  33. Lai H-L, Gailucci VF, Gunderson DR, Donnelly RF (1996) Age determination in fisheries: methods and applications to stock assessment. In: Gallucci VF, Saila SB, Gustafson DJ, Rothschild BJ (eds) Stock assessment: quantitative methods and applications for small-scale fisheries. Lewis Publications, New YorkGoogle Scholar
  34. Lazorchak JM, McCormick FH, Henry TR, Herlithy AT (2003) Contamination in fish in streams of the mid-Atlantic region: An approach to regional indicator selection and wildlife assessment. Environ Toxicol Chem 22:545–553CrossRefGoogle Scholar
  35. Liu SZ, Zhang Y-C, Mu Y, Su X, Liu J-X (1996) Thymocyte apoptosis in response to low-dose radiation. Mutat Res 358:185–191CrossRefGoogle Scholar
  36. Lockshin RA, Zakeri Z (2001) Programmed cell death and apoptosis: origins of the theory. Nat Rev Mol Cell Bio 2:545–550CrossRefGoogle Scholar
  37. Luna LG (1992) Histopathological methods and color atlas of special stains and tissue artifacts. Am Histol, GaithersburgGoogle Scholar
  38. Marcogliese DJ, Pietrock M (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol 27:123–130CrossRefGoogle Scholar
  39. McMahon G, Cuffney T (2000) Quantifying urban intensity in drainage basins for assessing stream ecological conditions. J Am Wat Res Assoc 36:1247–1261CrossRefGoogle Scholar
  40. McMahon G, Gregonis SM, Waltman SW, Omernik JM, Thorson TD, Freeouf JA, Rodrick AH, Keys JE (2001) Developing a spatial framework of common ecological regions for the conterminous United States. Environ Manag 28:293–316CrossRefGoogle Scholar
  41. McPherson AK, Moreland RS, Atkins JB (2003) Occurrence and distribution of nutrients, suspended sediment, and pesticides in the Mobile River Basin, Alabama, Georgia, Mississippi, and Tennessee, 1999–2001. U.S. Geological Survey Water-Resources Investigations Report 03-4203, p 109Google Scholar
  42. Meador MR, Coles JF, Zappia H (2005) Comparison of fish assemblage responses to gradients of urban intensity in contrasting metropolitan areas: Birmingham, Alabama, and Boston, Massachusetts. In: Brown LR, Gray RH, Hughes H, Meador MR (eds) Effects of urbanization on aquatic ecosystems. American Fisheries Society, BethesdaGoogle Scholar
  43. Mettee MF, O’Neil PE, Pierson JM (1996) Fishes of Alabama and the mobile basin. Oxmoor House Inc, BirminghamGoogle Scholar
  44. Myers MS, Fournie JW (2002) Histopathological biomarkers as integrators of anthropogenic and environmental stressors. In: Adams SM (ed) Biological Indicators of Aquatic Ecosystem Stress. American Fisheries Society, BethesdaGoogle Scholar
  45. Nowell LH, Moran PW, Gilliom RJ, Calhoun DL, Ingersoll CG, Kemble NE, Kuivila KM, Phillips PJ (2013) Contaminants in stream sediments from seven United States Metropolitan Areas: Part I: distribution in relation to urbanization. Arch Environ Contam Toxicol 64:32–51CrossRefGoogle Scholar
  46. Osachoff HL, van Aggelan GC, Mommsen TP, Kennedy CJ (2013) Concentration-response relationships and temporal patterns in hepatic gene expression of Chinook salmon (Oncorhynchus tshawytscha) exposed to sewage. Comp Biochem Physiol D 8:32–44Google Scholar
  47. Otto DME, Moon TW (1995) 3,3’,4,4’-Tetrachlorobiphenyl effects on antioxidant enzymes and glutathione status in different tissues of rainbow trout. Pharmacol Toxicol 77:281–287CrossRefGoogle Scholar
  48. Paul MJ, Meyer JL (2001) Streams in the urban landscape. Ann Rev Ecol Syst 32:333–365CrossRefGoogle Scholar
  49. Rafferty SD, Blazer VS, Pinkney AE, Grazio JL, Obert EC, Boughton L (2009) A historical perspective on the “fish tumors or other deformities” beneficial use impairment at Great Lakes Areas of Concern. Great Lakes Res 35:496–506CrossRefGoogle Scholar
  50. Ramirez A, Engman A, Rosas KG, Perez-Reyes O, Martino-Cardona DM (2012) Urban impacts on tropical island streams: some key aspects influencing ecosystem response. Urban Ecosyst 15:315–325CrossRefGoogle Scholar
  51. Rocher B, Le Goff J, Peluhet L, Briand M, Manduzio H, Gallois J, Devier MH, Geffard O, Gricourt L, Augagneur S, Budzinski H, Pottier D, André V, Lebailly P, Cachot J (2006) Genotoxicant accumulation and cellular defense activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquat Toxicol 79:65–77CrossRefGoogle Scholar
  52. Sayeed I, Parvez S, Pandey S, Bin-Hafeez B, Haque R, Raisuddin S (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotox Environ Safe 56:295–301CrossRefGoogle Scholar
  53. Schmidt K, Staaks GBO, Pflugmacher S, Steinberg CEW (2005) Impact of PCB mixture (Aroclor 1254) and TBT and a mixture of both on swimming behavior, body growth and enzymatic biotransformation activities (GST) of young carp (Cyprinus carpio). Aquat Toxicol 71:49–59CrossRefGoogle Scholar
  54. Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic and metalloids in fish-a review. Environ Sci Pollut Res 20:2133–2149CrossRefGoogle Scholar
  55. Staley K, Blaschke AJ, Chun J (1997) Apoptotic DNA fragmentation is detected by a semi-quantitative ligation-mediated PCR of blunt DNA ends. Cell Death Differ 4:66–75CrossRefGoogle Scholar
  56. Tate CM, Cuffney TF, McMahon G, Giddings EMP, Coles JC, Zappia H (2005) Use of an urban intensity index to assess urban effects on streams in three contrasting environmental settings. In: Hughes H, Meador MR (eds) LR, Gray RH. Effects of urbanization on aquatic ecosystems. American Fisheries Society, Bethesda, pp 291–316Google Scholar
  57. van Dyk JC, Cochrane MJ, Wagenaar GM (2012) Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 87:301–331CrossRefGoogle Scholar
  58. Weaver LA, Garman GC (1994) Urbanization of a watershed and historical changes in a stream fish assemblage. Trans Am Fish Soc 123:162–172CrossRefGoogle Scholar
  59. Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design, 3rd edn. McGraw-Hill, New YorkGoogle Scholar
  60. Zandbergen PA (1998) Urban watershed ecological risk assessment using GIS: a case study of the Brunette River watershed in British Columbia, Canada. J Hazard Mater 61:163–173CrossRefGoogle Scholar
  61. Zappia H (2002) Organochlorine compounds and trace elements in fish tissue and streambed sediment in the Mobile River Basin in Alabama, Mississippi, and Georgia, 1998. U.S. Geological Survey Water-Resources Investigations Report 02-4160, p 34Google Scholar
  62. Zappia H, Cuffney T, McMahon G, Walsh S, Caskey B, Bryant W, Atkins JB (2005) Responses of fish, invertebrate, and algal communities to a gradient of urbanization in the Ridge and Valley Ecoregion of Alabama and Georgia. In: Brown LR, Gray RH, Hughes H, Meador MR (eds) Effects of urbanization on aquatic ecosystems. American Fisheries Society, BethesdaGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2016

Authors and Affiliations

  • D. Iwanowicz
    • 1
  • M. C. Black
    • 2
  • V. S. Blazer
    • 1
  • H. Zappia
    • 3
  • W. Bryant
    • 4
  1. 1.U.S. Geological SurveyNational Fish Health Research LaboratoryKearneysvilleUSA
  2. 2.Department of Environmental Health ScienceUniversity of GeorgiaAthensUSA
  3. 3.Center for Threat PreparednessGivenUSA
  4. 4.CK Associates Environmental ConsultantsBaton RougeUSA

Personalised recommendations