Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH ARTICLE

Pharmaceuticals and personal care products alter growth and function in lentic biofilms

Lawton Shaw A B C , Chuyen Phung B and Michael Grace B
+ Author Affiliations
- Author Affiliations

A Athabasca University, Centre for Science, 1 University Drive, Athabasca, AB, T9S 3A3, Canada.

B Water Studies Centre, School of Chemistry, Monash University, Clayton, Vic. 3800, Australia.

C Corresponding author. Email: lawton.shaw@athabascau.ca

Environmental Chemistry 12(3) 301-306 https://doi.org/10.1071/EN14141
Submitted: 29 July 2014  Accepted: 9 December 2014   Published: 1 April 2015

Environmental context. Pharmaceuticals and personal care products are routinely found in waters discharged from treatment plants and in surrounding aquatic ecosystems. Despite the widespread occurrence of these biologically active agents, there is limited understanding of their potential effects on key ecosystem processes such as primary production, ecosystem respiration and algal growth. This paper examines the effects of five common pharmaceuticals on the rates of these fundamental processes.

Abstract. Pharmaceutical diffusing substrates were used to study in situ responses of aquatic biofilms in an urbanised lentic ecosystem to five pharmaceutical and personal care products (PPCPs; caffeine, cimetidine, ciprofloxacin, diphenhydramine and metformin). The pharmaceutical diffusing substrates consisted of porous biofilm substrates placed atop a mass of agar amended with 2.5 mM of the PPCP compound of interest. Over 21 days, biofilms growing on the substrata were exposed to slow diffusion of the PPCP through the agar and porous substrate. Algal biomass was suppressed by exposure to diphenhydramine (–81 %) and ciprofloxacin (–50 %). Gross primary production was completely suppressed by diphenhydramine exposure but stimulated by caffeine (+39 %) and cimetidine (+46 %). For heterotroph biofilms, community respiration was suppressed by exposure to diphenhydramine (–24 %). To characterise PPCP exposure, rates of diffusion from the pharmaceutical diffusing substrates were measured at 10, 20 and 30 °C. Diffusion was Fickian for all compounds and all temperatures. Diffusion coefficients, D, were in the range 1.5 × 10–10 to 1.1 × 10–9 m2 s–1. From diffusion data, average release rates over 21 days were typically 30–50 ng min–1 cm–2 at 20 °C. The results show that PPCPs can dramatically affect rates of key ecological processes, and the relationship between release rate and ambient concentration of PPCPs is discussed.

Additional keywords: caffeine, cimetidine, ciprofloxacin, diffusion coefficient, diphenhydramine, metformin.


References

[1]  E. J. Rosi-Marshall, T. V. Royer, Pharmaceutical compounds and ecosystem function: an emerging research challenge for aquatic ecologists. Ecosystems 2012, 15, 867.
Pharmaceutical compounds and ecosystem function: an emerging research challenge for aquatic ecologists.CrossRef | 1:CAS:528:DC%2BC38Xht1agsr%2FL&md5=12308bca4d8c19b3718fb5d5763f9b2aCAS |

[2]  D. W. Kolpin, E. T. Furlong, M. T. Meyer, E. M. Thurman, S. D. Zaugg, L. B. Barber, H. T. Buxton, Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. Environ. Sci. Technol. 2002, 36, 1202.
Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance.CrossRef | 1:CAS:528:DC%2BD38XhslOitLg%3D&md5=f0269d81d6dec20b45d0f0cd32be0a16CAS | 11944670PubMed |

[3]  S. D. Kim, J. Cho, I. S. Kim, B. J. Vanderford, S. A. Snyder, Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res. 2007, 41, 1013.
Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters.CrossRef | 1:CAS:528:DC%2BD2sXhsFCnsLY%3D&md5=e4138a7c44066eacf3d134743a26e887CAS | 16934312PubMed |

[4]  M. J. Focazio, D. W. Kolpin, K. K. Barnes, E. T. Furlong, M. T. Meyer, S. D. Zaugg, L. B. Barber, M. E. Thurman, A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States – II. Untreated drinking water sources. Sci. Total Environ. 2008, 402, 201.
A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States – II. Untreated drinking water sources.CrossRef | 1:CAS:528:DC%2BD1cXps1elsro%3D&md5=99fbc4244d475a82d6297bcae523a2adCAS | 18433838PubMed |

[5]  J. Fick, H. Söderström, R. H. Lindberg, C. Phan, M. Tysklind, D. G. J. Larsson, Contamination of surface, ground, and drinking water from pharmaceutical production. Environ. Toxicol. Chem. 2009, 28, 2522.
Contamination of surface, ground, and drinking water from pharmaceutical production.CrossRef | 1:CAS:528:DC%2BD1MXhsV2lt7bI&md5=3f1c986955e5d99b7186ec2ef0bf1d82CAS | 19449981PubMed |

[6]  D. G. J. Larsson, C. de Pedro, N. Paxeus, Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J. Hazard. Mater. 2007, 148, 751.
Effluent from drug manufactures contains extremely high levels of pharmaceuticals.CrossRef | 1:CAS:528:DC%2BD2sXpslOqurs%3D&md5=953ea802779cfd175848f92a386fabcaCAS |

[7]  P. J. Phillips, S. G. Smith, D. W. Kolpin, S. D. Zaugg, H. T. Buxton, E. T. Furlong, K. Esposito, B. Stinson, Pharmaceutical formulation facilities as sources of opioids and other pharmaceuticals to wastewater treatment plant effluents. Environ. Sci. Technol. 2010, 44, 4910.
Pharmaceutical formulation facilities as sources of opioids and other pharmaceuticals to wastewater treatment plant effluents.CrossRef | 1:CAS:528:DC%2BC3cXmvFKmtb0%3D&md5=0f1c0cd34f0a10b809fedf15cfb654caCAS | 20521847PubMed |

[8]  G. W. Minshall, Autotrophy in stream ecosystems. Bioscience 1978, 28, 767.
Autotrophy in stream ecosystems.CrossRef |

[9]  B. A. Wilson, V. H. Smith, F. deNoyelles, C. K. Larive, Effects of three pharmaceutical and personal care products on natural freshwater algal assemblages. Environ. Sci. Technol. 2003, 37, 1713.
Effects of three pharmaceutical and personal care products on natural freshwater algal assemblages.CrossRef | 1:CAS:528:DC%2BD3sXhvF2mu7o%3D&md5=c98a2a1f20e70d66f006924b9e85e17eCAS | 12775039PubMed |

[10]  J. R. Lawrence, B. Zhu, G. D. W. Swerhone, J. Roy, L. I. Wassenaar, E. Topp, D. R. Korber, Comparative microscale analysis of the effects of triclosan and triclocarban on the structure and function of river biofilm communities. Sci. Total Environ. 2009, 407, 3307.
Comparative microscale analysis of the effects of triclosan and triclocarban on the structure and function of river biofilm communities.CrossRef | 1:CAS:528:DC%2BD1MXjslaiur4%3D&md5=61c9014bfd843809dcd881776b56c235CAS | 19275956PubMed |

[11]  M. Ricart, H. Guasch, M. Alberch, D. Barceló, C. Bonnineau, A. Geiszinger, M. Farré, J. Ferrer, F. Ricciardi, A. M. Romaní, S. Morin, L. Proia, L. Sala, D. Sureda, S. Sabater, Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms. Aquat. Toxicol. 2010, 100, 346.
Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms.CrossRef | 1:CAS:528:DC%2BC3cXht1OmtLbF&md5=78bccd2ab6f39eace5c9d208c1537059CAS | 20855117PubMed |

[12]  E. L. Quinlan, C. T. Nietch, K. Blocksom, J. M. Lazorchak, A. L. Batt, R. Griffiths, D. J. Klemm, Temporal dynamics of periphyton exposed to tetracycline in stream mesocosms. Environ. Sci. Technol. 2011, 45, 10684.
Temporal dynamics of periphyton exposed to tetracycline in stream mesocosms.CrossRef | 1:CAS:528:DC%2BC3MXhsVSqtr%2FK&md5=7020e066164fafef3b104464e4195af2CAS | 22050031PubMed |

[13]  P. D. Hoppe, E. J. Rosi-Marshall, H. A. Bechtold, The antihistamine cimetidine alters invertebrate growth and population dynamics in artificial streams. Freshwater Science 2012, 31, 379.
The antihistamine cimetidine alters invertebrate growth and population dynamics in artificial streams.CrossRef |

[14]  M. Bergheim, R. Gminski, B. Spangenberg, M. Dębiak, A. Bürkle, V. Mersch-Sundermann, K. Kümmerer, R. Gieré, Recalcitrant pharmaceuticals in the aquatic environment: a comparative screening study of their occurrence, formation of phototransformation products and their in vitro toxicity. Environ. Chem. 2014, 11, 431.
Recalcitrant pharmaceuticals in the aquatic environment: a comparative screening study of their occurrence, formation of phototransformation products and their in vitro toxicity.CrossRef | 1:CAS:528:DC%2BC2cXhsVWlurvL&md5=d316901f0359699f8e4d565c5f43c9b9CAS |

[15]  G. Fairchild, G. Winfield, R. L. Lowe, W. B. Richardson, Algal periphyton growth on nutrient-diffusing substrates: an in situ bioassay. Ecology 1985, 66, 465.
Algal periphyton growth on nutrient-diffusing substrates: an in situ bioassay.CrossRef | 1:CAS:528:DyaL2MXkvVOju70%3D&md5=44094c35ce662cacb911e674e608510bCAS |

[16]  J. L. Tank, M. J. Bernot, E. J. Rosi-Marshall, Nitrogen limitation and uptake, in Methods in Stream Ecology (Eds F. R. Hauer, G. A. Lamberti) 2006, pp. 213–238 (Academic Press: San Diego, CA).

[17]  T. J. Hoellein, J. L. Tank, J. J. Kelly, E. J. Rosi-Marshall, Seasonal variation in nutrient limitation of microbial biofilms colonizing organic and inorganic substrata in streams. Hydrobiologia 2010, 649, 331.
Seasonal variation in nutrient limitation of microbial biofilms colonizing organic and inorganic substrata in streams.CrossRef | 1:CAS:528:DC%2BC3cXmtVyksr4%3D&md5=53f62c3ff50ae640722b8845c928dfe9CAS |

[18]  A. R. Bunch, M. J. Bernot, Distribution of non-prescription pharmaceuticals in central Indiana streams and effects on sediment microbial activity. Ecotoxicology 2011, 20, 97.
Distribution of non-prescription pharmaceuticals in central Indiana streams and effects on sediment microbial activity.CrossRef | 1:CAS:528:DC%2BC3MXjtFChsg%3D%3D&md5=653259d6966f83f796572dfdb328d6a8CAS | 21069566PubMed |

[19]  E. J. Rosi-Marshall, D. W. Kincaid, H. A. Bechtold, T. V. Royer, M. Rojas, J. J. Kelly, Pharmaceuticals suppress algal growth and microbial respiration and alter bacterial communities in stream biofilms. Ecol. Appl. 2013, 23, 583.
Pharmaceuticals suppress algal growth and microbial respiration and alter bacterial communities in stream biofilms.CrossRef | 23734487PubMed |

[20]  A. T. Rugenski, A. M. Marcarelli, H. A. Bechtold, R. S. Inouye, Effects of temperature and concentration on nutrient release rates from nutrient diffusing substrates. J. N. Am. Benthol. Soc. 2008, 27, 52.
Effects of temperature and concentration on nutrient release rates from nutrient diffusing substrates.CrossRef |

[21]  J. L. Tank, W. K. Dodds, Nutrient limitation of epilithic and epixylic biofilms in ten North American streams. Freshw. Biol. 2003, 48, 1031.
Nutrient limitation of epilithic and epixylic biofilms in ten North American streams.CrossRef | 1:CAS:528:DC%2BD3sXls1CnsLg%3D&md5=4ab41575d46c4a900649a929c32ec6aeCAS |

[22]  C. J. Lorenzen, Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol. Oceanogr. 1967, 12, 343.
Determination of chlorophyll and pheopigments: spectrophotometric equations.CrossRef | 1:CAS:528:DyaF1cXovFOqsQ%3D%3D&md5=762c228fd84d8dff7d2c774cf741c7cbCAS |

[23]  E. Willingham, Endocrine-disrupting compounds and mixtures: unexpected dose–response. Arch. Environ. Contam. Toxicol. 2004, 46, 265.
| 1:CAS:528:DC%2BD2cXhvFOltr8%3D&md5=cf86b829625187b17e93841ed2f67645CAS | 15106679PubMed |

[24]  H.-C. Flemming, J. Wingender, The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623.
| 1:CAS:528:DC%2BC3cXpsFWlur4%3D&md5=f482c23d63f2792971b4c9ef971b97c1CAS | 20676145PubMed |

[25]  T. K. Haack, A. M. Gordon, Nutritional relationships among microorganisms in an epilithic biofilm community. Microb. Ecol. 1982, 8, 115.
Nutritional relationships among microorganisms in an epilithic biofilm community.CrossRef | 1:CAS:528:DyaL3sXhsVWltQ%3D%3D&md5=8ad2914e8520b6909aedfd5099e6bfe0CAS | 24225806PubMed |

[26]  A. M. Romaní, S. Sabater, Effect of primary producers on the heterotrophic metabolism of a stream biofilm. Freshw. Biol. 1999, 41, 729.
Effect of primary producers on the heterotrophic metabolism of a stream biofilm.CrossRef |

[27]  G. M. Carr, A. Morin, P. A. Chambers, Bacteria and algae in stream periphyton along a nutrient gradient. Freshw. Biol. 2005, 50, 1337.
Bacteria and algae in stream periphyton along a nutrient gradient.CrossRef |

[28]  J. L. Ford, K. Mitchell, P. Rowe, D. J. Armstrong, P. N. C. Elliott, C. Rostron, J. E. Hogan, Mathematical modelling of drug release from hydroxypropylmethylcellulose matrices: effect of temperature. Int. J. Pharm. 1991, 71, 95.
Mathematical modelling of drug release from hydroxypropylmethylcellulose matrices: effect of temperature.CrossRef | 1:CAS:528:DyaK3MXisFeqt7g%3D&md5=70ccedf338b4c3c860482c725fd69988CAS |

[29]  R. H. H. Guy, Calculations of drug release rates from cylinders. Int. J. Pharm. 1981, 8, 159.
Calculations of drug release rates from cylinders.CrossRef | 1:CAS:528:DyaL3MXksV2gsLg%3D&md5=395c70933ecfd2c279389e19d3131950CAS |

[30]  J. Hadgraft, Calculation of drug release rates from controlled release devices. The slab. Int. J. Pharm. 1979, 2, 177.
Calculation of drug release rates from controlled release devices. The slab.CrossRef | 1:CAS:528:DyaE1MXkslyrs7Y%3D&md5=3e67a102ae0bdecc07dd14ef1854e90fCAS |

[31]  N. A. Peppas, J. J. Sahlin, A simple equation for the description of solute release. III. Coupling of diffusion and relaxation. Int. J. Pharm. 1989, 57, 169.
A simple equation for the description of solute release. III. Coupling of diffusion and relaxation.CrossRef | 1:CAS:528:DyaK3cXhtVClu74%3D&md5=3c152d914d72a462fc2b7b2cb4aafc7eCAS |

[32]  P. L. P. Ritger, N. A. Peppas, A simple equation for description of solute release. II. Fickian and anomalous release from swellable devices. J. Control. Release 1987, 5, 37.
A simple equation for description of solute release. II. Fickian and anomalous release from swellable devices.CrossRef | 1:CAS:528:DyaL2sXkvVeku7s%3D&md5=5debbb5d2a38f22759a607efd99579a3CAS |

[33]  D. R. Lide, CRC Handbook of Chemistry and Physics, 86th edn 2005 (Taylor & Francis: Boca Raton, FL).

[34]  T. R. Engel, P. Reid, Physical Chemistry 2006 (Pearson Education, Inc.: San Francisco, CA).



Rent Article (via Deepdyve) Export Citation Cited By (5)