Skip to main content
SpringerLink
Log in

Demographic Responses to Multigeneration Cadmium Exposure in Two Strains of the Freshwater Gastropod, Biomphalaria glabrata

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

A life table response experiment (LTRE) was used to quantify the population-level effects of continuous, multigeneration cadmium exposure on two strains of the freshwater gastropod, Biomphalaria glabrata: the parasite-resistant BS90 and parasite-susceptible NMRI strains. Snails were exposed to waterborne cadmium for three consecutive generations. Survival, growth, and reproduction were measured empirically and incorporated into a stage-based, deterministic population model. Cadmium significantly affected hatching success, time to maturity, and juvenile and adult survival in both strains. There were significant effects of generation on fecundity, hatching success, time to maturity and juvenile survival in NMRI, and time to maturity and adult survival in BS90. Cadmium significantly affected the population growth rate, λ, in BS90. Cadmium, generation, and the cadmium × generation interaction had significant effects on λ in NMRI. At the high cadmium exposure, λ for NMRI showed a decrease from generation 1 to generation 2, followed by an increase from generation 2 to generation 3. The λ value in high-cadmium BS90 steadily decreased over the three generations, while NMRI at this same concentration was similar to the controls. The results indicate that strain-specific differences in response to multigeneration cadmium exposure are evident in B. glabrata. Moreover, effects seen in the first generation are not necessarily indicative of effects in subsequent generations. Changes in λ over the course of the three-generation exposure suggest that acclimation and/or adaptation to cadmium may have occurred, particularly in NMRI at the high cadmium exposure level.

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

  • Allah AT, Wanas MWS, Thompson SN (1997) Effects of heavy metals on survival and growth of Biomphalaria glabrata say (gastopoda: pulmonata) and interaction with schistosome infection. J Moll Stud 63:79–86. doi:10.1093/mollus/63.1.79

    Article  Google Scholar 

  • Barata C, Baird DJ, Mitchell SE, Soares AMVM (2002) Among- and within-population variability in tolerance to cadmium stress in natural populations of Daphnia magna: implications for ecological risk assessment. Environ Toxicol Chem 21:1058–1064. doi :10.1897/1551-5028(2002)021<1058:AAWPVI>2.0.CO;2

    Article  CAS  Google Scholar 

  • Barnthouse LW, Munns WR, Sorensen MT (eds) (2008) Population-level ecological risk assessment. Taylor and Francis/CRC Press, Boca Raton

  • Bengtsson G, Gunnarsson T, Rundgren S (1985) Influence of metals on reproduction, mortality and population growth in Onychiurus armatus (collembola). J Appl Ecol 22:967–978. doi:10.2307/2403244

    Article  CAS  Google Scholar 

  • Brewster-Geisz KK, Miller TJ (2000) Management of the sandbar shark (Carcharhinus plumbeus): implications of a stage-based model. Fish Bull 98:236–249

    Google Scholar 

  • Caswell H (1989) Analysis of life table response experiments.i. Decomposition of effects on population growth rate. Ecol Model 46:221–237. doi:10.1016/0304-3800(89)90019-7

    Article  CAS  Google Scholar 

  • Caswell H (1996a) Analysis of life table response experiments. ii. Alternative parameterizations for size- and stage-structured models. Ecol Model 88:73–92. doi:10.1016/0304-3800(95)00070-4

    Article  Google Scholar 

  • Caswell H (1996b) Demography meets ecotoxicology: untangling the population level effects of toxic substances. In: Newman MC, Jagoe CH (eds) Ecotoxicology: a hierarchical approach. CRC Press/Lewis Publishers, Boca Raton, pp 255–292

  • Caswell H (2000) Prospective and retrospective analyses: their roles in conservation biology. Ecology 81:619–627

    Article  Google Scholar 

  • Crowder LB, Crouse DT, Heppell SS, Martin TH (1994) Predicting the impact of turtle excluder devices on loggerhead sea turtle populations. Ecol Appl 4:437–445. doi:10.2307/1941948

    Article  Google Scholar 

  • de Kroon H, Plaisier A, van Groenendael J, Caswell H (1986) Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67:1427–1431. doi:10.2307/1938700

    Article  Google Scholar 

  • Forbes VE, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556. doi :10.1897/1551–5028(1999)018<1544:ITPCRO>2.3.CO;2

    Article  CAS  Google Scholar 

  • Guan R, Wang W-X (2006a) Comparison between two clones of Daphnia magna: effects of multigenerational cadmium exposure on toxicity, individual fitness, and biokinetics. Aquat Toxicol 76:217–229. doi:10.1016/j.aquatox.2005.10.003

    Article  CAS  Google Scholar 

  • Guan R, Wang W-X (2006b) Multigenerational cadmium acclimation and biokinetics in Daphnia magna. Environ Poll 141:343–352. doi:10.1016/j.envpol.2005.08.036

    Article  CAS  Google Scholar 

  • Janssen CR, De Schamphelaere K, Heijerick D, Muyssen B, Lock K, Bossuyt B, Vangheluwe M, Van Sprang P (2000) Uncertainties in the environmental risk assessment of metals. Hum Ecol Risk Assess 6:1003–1018. doi:10.1080/10807030091124257

    Article  CAS  Google Scholar 

  • Kammenga JE, Busschers M, Van Straalen NM, Jepson PC, Bakker J (1996) Stress induced fitness reduction is not determined by the most sensitive life-cycle trait. Funct Ecol 10:106–111. doi:10.2307/2390268

    Article  Google Scholar 

  • Klerks PL, Weiss JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Poll 45:173–205. doi:10.1016/0269-7491(87)90057-1

    Article  CAS  Google Scholar 

  • Kuhn A, Munns WR Jr, Poucher S, Champlin D, Lussier S (2000) Prediction of population-level response from mysid toxicity test data using population modeling techniques. Environ Toxicol Chem 19:2364–2371. doi :10.1897/1551-5028(2000)019<2364:POPLRF>2.3.CO;2

    Article  CAS  Google Scholar 

  • Levin L, Caswell H, Bridges T, DiBacco C, Cabrera D, Plaia G (1996) Demographic responses of estuarine polychaetes to pollutants: life table response experiments. Ecol Appl 6:1295–1313. doi:10.2307/2269608

    Article  Google Scholar 

  • Lingjaerde OC, Stenseth NC, Kristoffersen AB, Smith RH, Moe SJ, Read JM, Daniels S, Simkiss K (2001) Exploring the density-dependent structure of blowfly populations by nonparametric additive modeling. Ecology 82:2645–2658

    Google Scholar 

  • Miller TJ (2003) Incorporating space into models of blue crab populations. Bull Mar Sci 72:567–588

    Google Scholar 

  • Münzinger A, Guarducci M-L (1988) The effect of low zinc concentrations on some demographic parameters of Biomphalaria glabrata (say), mollusca: gastropoda. Aquat Toxicol 12:51–61. doi:10.1016/0166-445X(88)90019-7

    Article  Google Scholar 

  • Muyssen BTA, Janssen CR (2004) Multi-generation cadmium acclimation and tolerance in Daphnia magna straus. Environ Poll 130:309–316. doi:10.1016/j.envpol.2004.01.003

    Article  CAS  Google Scholar 

  • Postma JF, Davids C (1995) Tolerance induction and life cycle changes in cadmium-exposed Chironomus riparius (diptera) during consecutive generations. Ecotoxicol Environ Saf 30:195–202. doi:10.1006/eesa.1995.1024

    Article  CAS  Google Scholar 

  • Raimondo S, McKenney CJ, Barron MG (2006) Application of perturbation simulations in population risk assessment for different life history strategies and elasticity patterns. Hum Ecol Risk Assess 12:983–999. doi:10.1080/10807030600826904

    Article  CAS  Google Scholar 

  • Rao TR, Sarma SS (1986) Demographic parameters of Brachionus patulus muller (rotifera) exposed to sublethal DDT concentrations at low and high food levels. Hydrobiologia 139:193–200. doi:10.1007/BF00028292

    Article  CAS  Google Scholar 

  • Richards CS, Knight K, Lewis FA (1992) Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol Today 8:171–174. doi:10.1016/0169-4758(92)90015-T

    Article  CAS  Google Scholar 

  • Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114. doi:10.1016/0166-445X(92)90026-J

    Article  CAS  Google Scholar 

  • Salice CJ, Miller TJ (2003) Population-level responses to long-term cadmium exposure in two strains for the freshwater gastropod, Biomphalaria glabrata: results from a life-table response experiment. Environ Toxicol Chem 22:678–688. doi :10.1897/1551-5028(2003)022<0678:PLRTLT>2.0.CO;2

    Article  CAS  Google Scholar 

  • Salice CJ, Roesijadi G (2002) Resistance to cadmium and parasite infection are inversely related in two strains of a freshwater gastropod. Environ Toxicol Chem 21:1398–1403. doi :10.1897/1551-5028(2002)021<1398:RTCAPI>2.0.CO;2

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Support from the following organizations is acknowledged: NIH Training Grant T32 ES-7263 to the Program in Toxicology, University of Maryland, Baltimore, and Graduate Student Association, University of Maryland, Baltimore. Fred Lewis of the Biomedical Research Institute kindly provided snails and invaluable advice on the biology and husbandry of Biomphalaria glabrata. This study was conducted at the University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory. Contribution No. 4201 of the University of Maryland Center for Environmental Science. U.S. Environmental Protection Agency is current address of designated author and is not affiliated with this research.

Author information

Authors and Affiliations

  1. Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, P.O. Box 38, Solomons, MD, 20688, USA

    Christopher J. Salice, Thomas J. Miller & G. Roesijadi

  2. U.S. EPA/OPP/EFED, 1200 Pennsylvania Avenue NW (7507P), Washington, DC, 20460, USA

    Christopher J. Salice

  3. Marine Sciences Division, Pacific Northwest National Laboratory, 1529 West Sequim Bay Road, Sequim, WA, 98382, USA

    G. Roesijadi

Authors
  1. Christopher J. Salice
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas J. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Roesijadi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher J. Salice.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salice, C.J., Miller, T.J. & Roesijadi, G. Demographic Responses to Multigeneration Cadmium Exposure in Two Strains of the Freshwater Gastropod, Biomphalaria glabrata . Arch Environ Contam Toxicol 56, 785–795 (2009). https://doi.org/10.1007/s00244-008-9203-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-008-9203-9

Keywords

Search

Navigation