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Published online 1 May 2008
Published in J Environ Qual 37:1238-1244 (2008)
DOI: 10.2134/jeq2007.0391
© 2008 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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TECHNICAL REPORTS

Organic Compounds in the Environment

Antibiotic Losses from Unprotected Manure Stockpiles

Holly A.S. Dollivera and Satish C. Guptab,*

a Dep. of Plant and Earth Science, Univ. of Wisconsin-River Falls, 410 S. 3rd St., River Falls, WI 54022
b Dep. of Soil, Water, and Climate, Univ. of Minnesota, 1991 Upper Buford Circle, St. Paul, MN 55108

* Corresponding author (sgupta{at}umn.edu).

Received for publication July 24, 2007.

   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusions
 REFERENCES
 
Manure management is a major concern in livestock production systems. Although historically the primary concerns have been nutrients and pathogens, manure is also a source of emerging contaminants, such as antibiotics, to the environment. There is a growing concern that antibiotics in manure are reaching surface and ground waters and contributing to the development and spread of antibiotic resistance in the environment. One such pathway is through leaching and runoff from manure stockpiles. In this study, we quantified chlortetracycline, monensin, and tylosin losses in runoff from beef manure stockpiles during two separate but consecutive experiments representing different weather conditions (i.e., temperature and precipitation amount and form). Concentrations of chlortetracycline, monensin, and tylosin in runoff were positively correlated with initial concentrations of antibiotics in manure. The highest concentrations of chlortetracycline, monensin, and tylosin in runoff were 210, 3175, and 2544 µg L–1, respectively. Relative antibiotic losses were primarily a function of water losses. In the experiment that had higher runoff water losses, antibiotic losses ranged from 1.2 to 1.8% of total extractable antibiotics in manure. In the experiment with lower runoff water losses, antibiotic losses varied from 0.2 to 0.6% of the total extractable antibiotics in manure. Manure analysis over time suggests that in situ degradation is an important mechanism for antibiotic losses. Degradation losses during manure stockpiling may exceed cumulative losses from runoff events. Storing manure in protected (i.e., covered) facilities could reduce the risk of aquatic contamination associated with manure stockpiling and other outdoor manure management practices.

Abbreviations: AFO, animal feeding operation • ELISA, enzyme-linked immunosorbent assay


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 Conclusions
 REFERENCES
 
MANURE management is a major issue in livestock production operations. More than 130 million metric tons (dry weight) of manure is produced annually from cattle, swine, and poultry operations in the USA (USDA-ERS, 2005). Manure is rich in macronutrients (N, P, and K), making it a valuable resource for crop production. The annual value of crop nutrients from beef manure alone exceeds $450 million (Eghball and Power, 1994). However, when improperly managed, manure can pose serious environmental risks (Burkholder et al., 2007). Agricultural pollution accounts for nearly 50% of the impaired surface waters in the USA, with approximately 20% of impairments directly attributed to livestock production (USEPA, 2002).

The majority of livestock are raised in confinement due to economic and production efficiencies. In the USA, there are more than 200,000 confined animal feeding operations (AFOs) (Gollehon et al., 2001). Although large-scale concentrated animal feeding operations account for <10% of total AFOs, they account for approximately half of total manure production (Gollehon et al., 2001). Manure from AFOs is commonly stored in stockpiles or lagoons before land-application (Eghball and Power, 1994; Moore et al., 1995; Cheng, 2003). It is estimated that more than 90% of dairy producers stockpile their manure (Morse Meyer et al., 1997). Although not widely practiced, alternative manure management techniques, such as composting, have been gaining increased attention because land availability for manure application is often limited in AFOs (Larney et al., 2003). Manure storage and composting often occurs in unprotected outdoor environments, which can lead to leaching and runoff of pollutants during precipitation events.

Historically, nutrients (Sweeten, 1998) and pathogens (Bicudo et al., 2003) have been the primary concerns in manure storage and use. However, animal manure can also be a source of emerging contaminants, such as antibiotics and antibiotic-resistant bacteria, to the environment. Antibiotics are routinely administered to livestock at subtherapeutic dosages (<200 g ton–1 feed) for growth promotion and prophylactic purposes. It is estimated that between 9 and 13 million kilograms of antibiotics are used annually in the USA for livestock purposes (Mellon et al., 2001; Shea, 2003). Only a small fraction of feed-mixed antibiotics is used by animals, resulting in high levels of unmetabolized antibiotics in manure (Kumar et al., 2005). A review by Kumar et al. (2005) found that antibiotic concentrations in manure ranged from trace levels to >200 mg kg–1 or L–1, with typical concentrations in the 1 to 10 mg kg–1 or L–1 range.

Antibiotics have been widely detected in surface and ground waters. A reconnaissance study of rivers across the USA found that approximately 50% of surface waters contain antibiotics (Kolpin et al., 2002). Antibiotics have also been detected in ground water (Lindsey et al., 2001). In general, antibiotic concentrations reported in aquatic environments are <10 µg L–1. The primary concern with antibiotics in aquatic environments is the development and spread of antibiotic resistance (Levy, 1992), along with toxicity toward aquatic species (Halling-Sørensen, 2000).

Studies of antibiotic transport in agricultural settings have largely focused on losses from land-application of manure (Kay et al., 2004, 2005; Burkhardt et al., 2005; Kreuzig et al., 2005; Davis et al., 2006; Dolliver and Gupta, 2008). In general, antibiotic concentrations in runoff from manure-applied agricultural land are <1 mg L–1, with relative mass losses <5% of the total antibiotics applied with manure.

Although land-application of manure is a source of antibiotics to the environment, there is a lack of information on antibiotic losses from on-site manure management practices, such as stockpiling or composting. The objective of this study was to quantify antibiotic losses associated with unprotected beef manure stockpiling. Antibiotics evaluated in this study were chlortetracycline, monensin, and tylosin, commonly used subtherapeutic antibiotics in beef production (Mellon et al., 2001).


   Materials and Methods
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 Conclusions
 REFERENCES
 
Manure Stockpiling and Runoff Collection
The study was conducted at the University of Wisconsin Agricultural Research Station near Lancaster, Wisconsin. The experiment was conducted during two separate but consecutive time periods: June 2005 through October 2005 (Experiment 1) and November 2005 through June 2006 (Experiment 2). Average air temperature during Experiment 1 was 19°C, compared with 3°C during Experiment 2. Precipitation data were obtained from a Wisconsin Cooperative Weather Station located across the road from the study site.

The experimental setup consisted of two replicate beef manure stockpiles, each measuring 2.7 by 2.7 m (Fig. 1 ). The stockpiles were constructed on a 12% slope, and the runoff was collected at the downslope end in a 5-cm-diameter PVC pipe with a slit along its length. Heavy-gauge plastic separated the manure from the soil underneath, thus preventing leachate from infiltrating into the soil. The lower end of the plastic sheet was fastened inside the slit of the PVC pipe; thus, all of the runoff from the manure stockpile emptied into the pipe. Runoff from the pipe was routed to a 19-L plastic bucket inside a 190-L plastic barrel. Water samples were manually collected from the bucket. During high flow events, excess runoff overflowed into the barrel. Manure stockpiles were isolated from the surrounding area using 16-gauge galvanized corrugated steel sheets (20.3 by 81.3 cm) that were pounded into the ground to approximately 15 cm depth.


Figure 1
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  		Fig. 1. Setup for the manure stockpiling experiment.

 
Beef manure was obtained from the same farm operation for both experiments; however, different feedlots were used due to limited manure availability. Both feedlots administered chlortetracycline, monensin, and tylosin at variable concentrations in feed rations. Each antibiotic was detected in manure.

Table 1 lists the physiochemical characteristics of antibiotics evaluated in this study. With the exception of monensin, these antibiotics are soluble in water. Chlortetracycline and tylosin are strongly sorbed to solids as indicated by high Kd values, which limits their mobility in the environment. Monensin is less attracted (i.e., has low Kd values) to solids.


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  		Table 1. Physicochemical characteristics of the antibiotics evaluated in this study.

 
In addition to the natural presence of antibiotics, manure was spiked with a small quantity (<0.5 kg feed additive Mg–1 manure) of feed-grade antibiotics. Monensin (176 g kg–1 product) (Rumensin 80; Elanco Animal Health, Greenfield, IN) was added during both experiments, whereas chlortetracycline (110 g kg–1 product) (Aueromycin 50; Alpharma, Inc., Bridgewater, NJ) and tylosin (88 g kg–1 product) (Tylan 40; Elanco Animal Health) were added only during Experiment 2. Testing of initial manure samples showed that mixing of feed-grade antibiotics did not have a measurable effect on antibiotic concentrations in manure, possibly due to adsorption onto manure. In both experiments, approximately 1500 kg of manure was formed into conical-shaped piles using a front-end bucket loader. After settling, manure covered the entire area, and the plastic liner was not exposed.

Runoff water was collected separately from each manure stockpile. Runoff included surface flow and percolation through the pile; although previous studies by Sirucek, Montgomery, and Moncrief (Minnesota Department of Agriculture and the University of Minnesota, personal communication) showed that the majority of flow from a turkey manure stockpile was surface runoff rather than percolation. Runoff samples (1 L) were retrieved immediately after each rainfall or snowmelt event and frozen at –20°C. Runoff volume was manually measured and recorded.

In addition to runoff water collection, manure samples were collected three times during each experiment (initial, middle, and final). During each sampling, a composite manure sample (approximately 1 kg) was obtained from each replicate manure pile, which included subsamples taken from three separate locations in the pile (i.e., top, middle, and bottom) at approximately 25 cm depth. After collection, manure samples were frozen at –20°C. All manure samples were analyzed for antibiotic concentrations, gravimetric moisture content, and ash content (550°C, 2 h). Initial manure samples were also analyzed for total carbon (Elementar Vario EL; Elementar Analysensysteme GmbH, Hanau, Germany) and dissolved organic carbon (0.45-µm filtered, HCl-acidified extract at 1:4 dilution) (Shimadzu TOC-V CSH/CSN; Shimadzu Scientific Instruments, Columbia, MD) by high-temperature combustion, total (Kjeldahl) nitrogen and total phosphorus by wet digestion, and pH (Peters, 2003). Due to differences in moisture content of the manure samples, data are reported on a dry-weight basis. Antibiotic concentrations for the middle and final manure sampling periods were adjusted for mass losses, as measured from ash content analysis. The adjustment was done using the following relationship:

Formula 1[1]
where CiADJ is the mass loss adjusted antibiotic concentration (mg kg–1 of initial dry weight) at sampling time i, Ci is the measured antibiotic concentration at time i, Ash0 is the ash content at time 0 (mg kg–1 of initial dry weight), and Ashi is the ash content at time i (mg kg–1 of dry weight of the manure at time i).

Antibiotic Analysis
Runoff samples were prepared for analysis by thawing at room temperature, mechanical homogenization (i.e., stir plate), and filtering though a nonsorptive 0.45-µm filter. Antibiotic analysis of solid material in runoff samples was not performed. Manure samples were prepared for analysis by thawing at room temperature followed by manual mixing/homogenization. Antibiotic analysis of manure samples included water-extractable and total-extractable antibiotics. For water-extractable antibiotics, 5 g of manure was mixed with 10 mL of nano-pure water, vortexed for 1 min, shaken on an end-over-end shaker for 15 min at 4°C, and centrifuged at 2000 g for 20 min, and the supernatant collected. This step was repeated with an additional 10 mL of nano-pure water. Supernatants were combined, centrifuged at 2000 g for 20 min, and filtered through a non-sorptive 0.45-µm filter. For total-extractable antibiotics, the remaining solids were mixed with 10 mL of an 80:20 (v/v) methanol:water solution, vortexed, shaken, and centrifuged, and the supernatant collected. This step was repeated with an additional 5 mL of the methanol:water solution. Both supernatants were combined, centrifuged, and filtered as described for the water extraction.

Antibiotic analysis was conducted using enzyme-linked immunosorbent assay (ELISA) kits. The basis of ELISA analysis is a highly specific and sensitive antibody–antigen reaction. Commercially available tetracycline (r-Biopharm, South Marshall, MI), monensin (Immuno-Diagnostic Reagents, Vista, CA), and tylosin (International Diagnostic Systems Corporation, St. Joseph, MI) ELISA kits for antibiotic residue analysis in food products were adapted for analysis of water and manure samples (Kumar et al., 2004; Dolliver, 2007). Analysis was performed using provided materials and standards as instructed by the manufacturer. Quantification was performed at the specified wavelength using a spectrophotometer (Molecular Devices, Sunnyvale, CA). The tetracycline kit had 100% cross-reactivity toward chlortetracycline (Kumar et al., 2004). However, there was no cross-reactivity for the antibiotics used in this study between kits. Limits of quantification were 0.25 µg L–1 for chlortetracycline and tylosin and 3.0 µg L–1 for monensin. Standard curves (r2 > 0.95) were constructed for each kit from standards run in triplicate.

Water samples were diluted 1:1 with kit-specific dilution buffer (provided), and manure samples were diluted ≥1:10 to eliminate effects associated with the sample matrix (Aga et al., 2003; Dolliver, 2007). Water and manure samples were run once, with approximately 30% of samples randomly selected for duplicate analysis. The coefficient of variation for intra- and inter-plate variability was <20%.


   Results
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
 Conclusions
 REFERENCES
 
Manure Characteristics
Manure characteristics were nearly similar in both experiments (Table 2 ). This was expected because the manures were obtained from the same farm operation. There was variability in antibiotic concentrations in manure between the two experiments, especially for tylosin (Table 3 ). In both experiments, total extractable monensin concentrations were the highest, ranging from 62 to 120 mg kg–1 dry weight, whereas chlortetracycline and tylosin levels were <10 mg kg–1 dry weight. The average coefficient of variation for antibiotic concentrations in manure exceeded 30%, indicating high variability. On a fresh-weight basis, total-extractable antibiotic concentrations in manure were <5 mg kg–1 for chlortetracycline and tylosin, which is within the range of concentrations reported for animal manure (Kumar et al., 2005). Limited information is available on monensin levels in manure. In this study, fresh-weight monensin concentrations were between 25 and 50 mg kg–1.


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  		Table 2. Characteristics of the manures used in this study. With the exception of pH and moisture content, data are reported on a dry weight basis.

 

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  		Table 3. Initial water and total-extractable antibiotic concentrations of manure (mean ± SD) in Experiment 1 and Experiment 2.

 
Water-extractable antibiotic concentrations ranged from approximately 25% of total extractable for monensin to 70% for chlortetracycline and tylosin (Table 3). Water-extractable antibiotics potentially represent the form most susceptible to transport during leaching and runoff from manure piles. The lower water extractability of monensin is likely a result of lower water solubility (<100 mg L–1) and a higher octanol–water partitioning coefficient (log Kow = 2.8–4.2) compared with chlortetracycline and tylosin (water solubility >500 mg L–1; log Kow <2.5) (Table 1).

Runoff Water Losses
Precipitation during Experiment 1 was 475 mm (Fig. 2 ), which was received as rainfall. Precipitation during Experiment 2 was similar (456 mm); however, snowfall (935 mm) accounted for 68 mm (water equivalent) of precipitation. Despite similar total precipitation, runoff events were more frequent and intense during Experiment 1 than Experiment 2 (Fig. 2). Total runoff (mean ± SD) during Experiment 1 was 10.4 ± 1.0 mm, whereas total runoff (mean ± SD) during Experiment 2 was 3.1 ± 1.3 mm. Runoff water losses from manure piles were <2% of total precipitation during Experiment 1 and <1% of total precipitation during Experiment 2.


Figure 2
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  		Fig. 2. Daily precipitation and runoff in Experiment 1 (A) and Experiment 2 (B).

 
Antibiotic Concentrations in Runoff
Antibiotic concentrations in runoff from manure piles were variable over time and between antibiotics and experiments (Fig. 3 ). Between the two experiments, there was a strong positive correlation (r2 = 0.7) between antibiotic concentrations in runoff (Table 4 ) and initial concentrations in manure (Table 3). For example, chlortetracycline and monensin concentrations in runoff from Experiment 1 were higher than Experiment 2 because of their higher initial concentration in manure during Experiment 1. Comparatively, tylosin concentrations in runoff from Experiment 2 were higher than Experiment 1 because of the higher concentration of tylosin in manure during Experiment 2. The highest concentrations of chlortetracycline, monensin, and tylosin in manure pile runoff were 210 (Experiment 1), 3175 (Experiment 1), and 2544 µg L–1 (Experiment 2), respectively.


Figure 3
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  		Fig. 3. Concentrations of chlortetracycline (A), monensin (B), and tylosin (C) in manure pile runoff in Experiment 1 and Experiment 2. Error bars represent SD of the mean.

 

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  		Table 4. Flow-weighted and peak antibiotic concentrations (mean ± SD) in Experiment 1 and Experiment 2.

 
Antibiotic Losses in Runoff
Despite differences in antibiotic concentrations in runoff water among antibiotics, relative losses of all three antibiotics were similar within each experiment (Table 5 ). During Experiment 1, relative mass losses in runoff ranged from 1.2 to 1.9% of the total extractable amount of a given antibiotic in manure. Comparatively, relative mass losses during Experiment 2 ranged from 0.2 to 0.6%, approximately 75% lower than Experiment 1. Overall, these low antibiotic losses in manure pile runoff may be due to strong antibiotic adsorption on manure solids (Tolls, 2001). Lower antibiotic losses during Experiment 2 are likely a result of approximately 70% less runoff in Experiment 2 than Experiment 1 and possibly cooler temperatures lowering the water solubility of antibiotics in the manure pile. This suggests that antibiotic losses in runoff from manure piles are primarily a function of water losses and weather conditions.


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  		Table 5. Absolute and relative antibiotic losses (mean ± SD) in Experiment 1 and Experiment 2.

 
Antibiotic Degradation in Manure
Along with losses in runoff, antibiotic losses may occur from biotic and abiotic degradation processes in manure piles. Although this study was not designed to evaluate antibiotic degradation, antibiotic analysis was conducted on a limited number of manure samples during both experiments. Although variability was high, our data suggest that relative mass losses due to degradation were >50% of initial extractable antibiotics in manure for all three antibiotics during Experiment 1 (Fig. 4 ). Losses due to degradation during Experiment 2 were considerably less (Fig. 4). Lower degradation losses during Experiment 2 could possibly be due to differences in weather conditions, such as temperature, which was lower during Experiment 2 than Experiment 1. Also, antibiotic degradation during Experiment 2 did not follow a consistent downward trend, possibly reflecting changes in manure characteristics due to climatic extremes (i.e., freeze/thaw conditions), which were not present during Experiment 1. Despite high variability, these data suggest that in situ antibiotic degradation is an important loss pathway and degradation losses may be much higher than cumulative losses from runoff events.


Figure 4
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  		Fig. 4. In situ degradation of chlortetracycline (A), monensin (B), and tylosin (C) in manure in Experiment 1 and Experiment 2. Data are fitted with a first-order decay function. Error bars represent SD of the mean.

 

   Discussion
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
Conclusions
 REFERENCES
 
The results from this study show that runoff from unprotected manure piles can contribute to antibiotic contamination of aquatic environments. Antibiotic concentrations in manure pile runoff increased with increasing concentration in manure; however, relative losses were primarily a function of runoff water losses. In general, concentrations and relative losses of antibiotics from manure piles are higher than those reported for the same compounds in surface runoff from manure-applied fields. For instance, Kay et al. (2005) reported a peak concentration of 72 µg L–1 for oxytetracycline, whereas tylosin was not detected in runoff during their study. Davis et al. (2006) reported a peak concentration of 3 µg L–1 for monensin, whereas chlortetryacline and tylosin concentrations were <0.5 µg L–1. Dolliver and Gupta (2008) reported peak concentrations of 0.5, 58, and 6 for chlortetracycline, monensin, and tylosin, respectively. Collectively, these values are substantially lower than the peak concentrations of 210, 3175, and 2544 µg L–1 reported in this study for chlortetracycline, monensin, and tylosin, respectively.

High antibiotic concentrations in manure pile runoff may contribute to the development and spread of antibiotic resistance in the environment. Several studies have linked the environmental occurrence of antibiotics to higher levels of antibiotic resistance (Nygaard et al., 1992; Pruden et al., 2006; Chander et al., 2007, 2008). Although the development and spread of antibiotic resistance has been given extensive attention, toxicity has generally been considered a minor issue with respect to antibiotic use in livestock production. This is largely because toxicity typically occurs at concentrations that exceed those reported in leachate or runoff from manure-applied fields. In this study, antibiotic concentrations from manure pile runoff exceeded toxicity thresholds in a few cases. For example, toxic effects from chlortetracycline and tylosin have been reported for Microcystis aeruginosa (cyanobacteria) at concentrations of 50 and 34 µg L–1, respectively (Halling-Sørensen, 2000). Similarly, chlortetracycline, monensin, and tylosin exhibit toxicity toward Selenastrum capricornutum (green algae) at concentrations of 3100, 980, and 1380 µg L–1, respectively (Elanco Products Company, 1989; Halling-Sørensen, 2000). Adverse impacts of chlortetracycline and monensin exposure have also been reported for Lemna gibba (duckweed) at concentrations of 219 and 998 µg L–1, respectively (Brain et al., 2004). Despite high concentrations and toxicity potential of antibiotics in manure pile runoff, the impacts are dissipated downstream due to dilution with receiving waters.

Storage of manure in protected (i.e., covered) as opposed to unprotected facilities could reduce or eliminate aquatic contamination concerns from manure pile runoff. However, this would require capital investment and may present other issues, such as manure handling difficulties, odors, pests, and pathogens. Along with reducing runoff losses, storing manure in protected facilities could be used as a mechanism to promote antibiotic degradation. Although research is limited, stockpiling and composting have been shown to reduce antibiotic concentrations in manure (De Liguoro et al., 2003; Arikan et al., 2007; Dolliver et al., 2008). However, data from this study show that even with similar manure sources/characteristics, degradation can be variable depending on weather conditions. Additional research is needed to determine the influence of manure characteristics and environmental conditions on antibiotic degradation in manure.


   Conclusions
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusions
REFERENCES
 
The results from this field study show that runoff from unprotected manure piles can contribute to antibiotic contamination of aquatic environments. In this study, runoff concentrations of chlortetracycline, monensin, and tylosin from unprotected manure piles increased with increasing concentration in manure; however, relative mass losses were primarily a function of water losses. Peak concentrations of chlortetracycline, monensin, and tylosin in manure pile runoff were 210, 3175, and 2544 µg L–1, respectively. Relative antibiotic losses ranged from approximately 0.4 to 1.5% of total extractable antibiotics in manure. Analysis of manure samples over time suggests that in situ degradation is an important antibiotic loss mechanism and that degradation losses may exceed cumulative losses from runoff events. Storing manure in protected (i.e., covered) facilities could reduce aquatic contamination risks associated with manure stockpiling or other outdoor manure management practices.


   ACKNOWLEDGMENTS
 
This research was supported in part by funds from the USDA-NRI program (grant number 2003-35102-13519) and the Rapid Agricultural Response Fund at the University of Minnesota. The authors thank Tim Wood, Doug Wiedenbeck, and the other field staff at the Lancaster, WI Agricultural Research Station for their assistance, along with the farmer who participated in this study.


   NOTES
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 NOTES
ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusions
 REFERENCES
 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.


   REFERENCES
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 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusions
 REFERENCES
 




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