The effects of veterinary antibiotics on soil microbial communities Heike Schmitt 2005

195 Pages·2005·4.23 MB·English

The effects
of veterinary antibiotics
on soil microbial communities

Heike Schmitt
2005

The effects
of veterinary antibiotics
on soil microbial communities

De effecten van veterinaire antibiotica
op bacteriëngemeenschappen in de bodem

(met een samenvatting in het Nederlands)

Proefschrift
ter verkrijging van de graad van doctor
aan de Universiteit Utrecht
op gezag van de Rector Magnificus, Prof. Dr. W. H. Gispen,
ingevolge het besluit van het College voor Promoties
in het openbaar te verdedigen
op 27 mei 2005 des middags te 12.45 uur
door
Heike Schmitt
geboren op 9 december 1972 te Hamburg
Promotoren:
Prof. Dr. C.J. van Leeuwen (Institute for Risk Assessment Sciences, Utrecht University)
Prof. Dr. W. Seinen (Institute for Risk Assessment Sciences, Utrecht University)

Copromotoren:
Dr. Patrick van Beelen (RIVM)
Dr. Eric Smit (RIVM)

This study was financially supported by a grant from the European Union (ERAVMIS,
EVKT1-CT-1999-00003) and by the RIVM. The work described in this thesis was partly
carried out at the National Institute for Public Health and the Environment (RIVM, Bilthoven,
The Netherlands), in cooperation with the Institute for Risk Assessment Sciences (IRAS,
Utrecht, The Netherlands).

The effects of veterinary antibiotics on soil microbial communities.
Heike Schmitt, Universiteit Utrecht, Faculteit Biologie, IRAS, 2005
ISBN 90-8559-056-6

Cover photographs: pigs at the Utrecht University Farm Tolakker
Printing: Optima Grafische Communicatie B.V., Rotterdam
Het gevoel is verstandig, en het denken is gevoelig.
Connie Palmen, De Vriendschap

INDEX
CHAPTER 1 GENERAL INTRODUCTION 1
CHAPTER 2 OPTIMISATION OF THE ANALYSIS OF COMMUNITY-LEVEL PHYSIO-
LOGICAL PROFILES 27
CHAPTER 3 EFFECTS OF ANTIBIOTICS ON SOIL MICROORGANISMS: TIME AND
NUTRIENTS INFLUENCE POLLUTION- INDUCED COMMUNITY
TOLERANCE 51
CHAPTER 4 POLLUTION-INDUCED COMMUNITY TOLERANCE OF SOIL MICROBIAL
COMMUNITIES CAUSED BY THE ANTIBIOTIC
SULFACHLOROPYRIDAZINE 71
CHAPTER 5 EFFECTS OF VETERINARY ANTIBIOTICS ON SOIL BACTERIA:
COMMUNITY STRUCTURE, PHYSIOLOGICAL PROFILE, AND INDUCED
TOLERANCE 87
CHAPTER 6 ON THE LIMITS OF TOXICANT-INDUCED TOLERANCE: CO-TOLERANCE
AND VARIATION FOR THE EXAMPLE OF ANTIBIOTIC EFFECTS 109
CHAPTER 7 TETRACYCLINES AND TETRACYCLINE RESISTANCE IN AGRICULTURAL
SOILS – MICROCOSM AND FIELD STUDIES 127
CHAPTER 8 GENERAL DISCUSSION 147
SYNOPSIS 172
NEDERLANDSE SAMENVATTING 175
DEUTSCHE ZUSAMMENFASSUNG 179
LIST OF ABBREVIATIONS 182
DANKWOORD 183
CURRICULUM VITAE 186
LIST OF PUBLICATIONS 187

CHAPTER 1
GENERAL INTRODUCTION

Clearly if microbial diversity means nothing
and cannot be measured the reader will be well
advised to turn the page and seek enlightenment
and advancement elsewhere.
And yet one cannot help but wonder.
Thomas P. Curtis and William T. Sloan
GENERAL INTRODUCTION
VETERINARY PHARMACEUTICALS
Pharmaceuticals are designed to interfere with biological systems. Once they reach
environmental compartments in significant concentrations, effects can thus also be expected
on environmental species (Kümmerer 2001). Compared with pesticides and biocides, the
environmental risks of pharmaceuticals have been studied less frequently. Still, during the last
few years, human and veterinary drugs received increasingly more attention1. Recently, their
possibly drastic effects were illustrated by the finding that the pain killer diclofenac led to
population declines in vultures due to contamination of carcasses (Oaks et al. 2004).
Veterinary drugs form a very heterogeneous group of chemicals, used for a wide range of
purposes in companion and farm animals. In the Netherlands, the number of active ingredients
amounts to 200 (Gezondheidsraad 2001). Volume-wise, the anthelmintics and antibiotics are
the most important groups, both represented by a range of compound classes (FEDESA
1999). Both are used in animal husbandry: anthelmintics to control worms, and antibiotics to
cure bacterial infections.
The main entry route of veterinary drugs into the environment is via soil. Manure of treated
farm animals often contains significant amounts of the active ingredients or degradation
products, and these can reach agricultural soils with the application of manure as fertiliser.
Other minor exposure routes include fish farming (Halling-Sørensen et al. 1998). Reviews of
(veterinary) drugs indicate soil effect studies are relatively scarce as compared with aquatic
studies (Halling-Sørensen et al. 1998, Thiele-Bruhn 2003, Boxall et al. 2004). Effect-wise, the
two most important groups of veterinary pharmaceuticals (Boxall et al. 2003a) are again the
anthelmintics and the antibiotics. Anthelmintics have strong effects on insects that are part of
the dung pat fauna (Herd 1995). As seen in single species tests and as expected from their
mode of action (Backhaus et al. 1997, Holten Lützhøft et al. 1999), antibiotics are highly toxic
to environmental bacteria. Further, they have the potential to induce resistance in human
pathogens (WHO 2001).
A current prioritisation exercise emphasised the potential environmental risk of many
antibiotics for herd treatment (Boxall et al. 2003b). Some ecto-and endoparasitic
anthelmintics, coccidiostats, and antifungal compounds were also assigned to the highest risk
class. The many data gaps for the latter precluded a full assessment, though, illustrating the
paucity of ecotoxicological and analytical data for many veterinary drugs in the terrestrial
environment (Lahr 2004).
In Europe, human and veterinary drugs belong to the substances requiring an authorisation
procedure (Directives 2001/82/EC and 2001/83/EC (European Community 2001a, b)). An
evaluation of their potential environmental risks became a goal of the authorisation of
veterinary drugs more than ten years ago (Directive 1990/676/EEC (European Economic
Community 1990) and Directive 92/18/EEC (European Economic Community 1992)).

1 The number of relevant publications in the Current Contents database started to rise exponentially in 2001 from
around three to 19 per year, when stringent selection criteria are used ((pharmaceuti* or human drug* or
veterinary drug*) and (ecotoxicol* or environmental fate)
2