Soil Accumulations and Movement
The Natural Resources Conservation Service (NRCS) defines soil health or soil quality as the continued capacity of the soil to function as a vital living ecosystem that sustains plants, animals, and humans (USDA-NRCS, 2023). Animal manure has been used for centuries as a source of nutrients in agriculture (Rayne and Aula, 2020). In many areas of the world today, land degradation resulting from erosion, desertification, tillage, and unsustainable agricultural practices have caused a significant decline in soil productivity on some land. At the same time, a growing global population is increasing the demand for food, which necessitates an increase in agricultural productivity. This requires improvements or restoration in the quality of agricultural lands. Manure, when managed properly, has been known to have beneficial effects on soil fertility and other soil properties, contributing to overall soil health. However, the presence of hormones and antibiotics in animal manure represents a significant concern with respect to the introduction of antibiotic residues to the environment and the development of antibiotic-resistant pathogens (Van Epps and Blaney, 2016).
Land application of agricultural waste containing antibiotic residues is an emerging concern, since the practice may lead to the spread of antibiotic resistance (Furtula et al., 2010; Olonitola et al., 2015). The antibiotic consumption patterns in agriculture vary across regions and countries around the world, and antibiotics that have been banned in the developed world are still being used in most developing countries. However, the antibiotic consumption profiles in many developing countries are greatly influenced by the misuse of antibiotics due to their easy availability over the counter, through unregulated supply chains, and the purchase without prescriptions.
Pathways of antibiotics into the environment
Antibiotics were first discovered in the 1940s and today, many different antibiotics are widely used around the world, mainly to treat and prevent infections in humans, plants and animals, but sometimes (in subtherapeutic doses) to promote growth and improve feed efficiency of animals (Conde-Cid et al., 2020). While antibiotics have contributed to a reduction in mortality and morbidity rates, their utilization in recent years particularly in veterinary medicine, has caused residues of these compounds to be present in a ubiquitous form in the environment, implying important risks for public health (Du and Liu, 2012). Antibiotics used in veterinary medicine can reach the soil mainly through spreading of manures as fertilizers, which is affected by the excretion rates of animals, since passage through their digestive systems will determine the degree of antibiotic degradation.
Antibiotics are often detected in unchanged form in manure from livestock farms. The concentrations detected vary depending on the animal species, the nature of the antibiotic, the geographical sampling area, and the type of livestock farm. Detection frequencies and antibiotic concentrations are usually higher in pig manures, followed by poultry and cattle (Kuppusamy et al., 2018). This is mainly because antibiotics are given in higher doses and more frequently to swine, followed by poultry and cattle (Van Boeckel et al., 2015). In most cases, excreted animal manure enters farm/pastureland unprocessed, as there is no regulation on the need for pretreatment of manure before application to the soil. Therefore, most of the antibiotics used in animal production are released into the environment by applying manures to crop soils (Xie et al., 2018).
Antibiotics and hormones may find their way into the environment by point-source or non-point source methods. Point source pollution originates from explicit sources such as pipe discharges from pharmaceutical manufacturing industries (Cardoso et al., 2014) and treated effluent discharged from wastewater treatment plants (Kibuye et al., 2019). Non-point sources of antibiotics may include surface runoff from agricultural fields that are amended with animal manure, which can transport antibiotics to surface water. Antibiotics that persist in manure can accumulate in the soil profile, be taken up by plants, and leach into groundwater. Veterinary antibiotics can also reach the soil from grazing livestock (Sharpley et al., 2006) where grazing livestock can excrete antibiotics in pastures.
The life cycles of veterinary antibiotics do not end once they have been administered to an animal. It is estimated that anywhere from 50 to 100 percent of a veterinary antibiotic will pass through a treated animal’s system either partially, or fully undegraded, depending on the type of antibiotic (Kim et al., 2010). While some antibiotics can break down fairly quickly (Larsson, 2014), others linger for much longer, where they can accumulate in higher concentrations in manure (Leventhal, 2019). In some locations, incorporation of animal manure onto agricultural soils has led to an accumulation of antibiotics in the soil profile (Kemper, 2008). Antibiotics can also accumulate into the environment through various pathways: leaching of soils, release of effluents into surface waters, and runoff from agricultural fields.
Degradation of antibiotics in soil depends not only on the catabolic activity of soil microorganisms, but also on properties of the soil, (i.e., soil type, organic matter content, pH, moisture content, temperature, soil texture, and oxygen status) (Cycoń et al., 2019). Antibiotic degradation also depends on the concentration of the antibiotic in the soil. Research indicates that high concentrations of antibiotics may prolong their persistence in soils, due to the inhibition of the activity of soil microorganisms (Pan and Chu, 2016). Most published data also indicates that the addition of different organic compounds, such as manure, biosolids, slurry, sludge, and compost into soils may contribute to changes in the rate of antibiotic degradation. In a review, Cycoń et al. (2019) indicated that the input of antibiotics into soils alters the structure and activity of microbial communities and the abundance of antimicrobial genes. However, it was concluded that results from studies in this field were often ambiguous, making environmental risk assessments related to the presence of antibiotics depend upon too many different factors to be reliable.
Detection of antibiotic residues in manure from cattle, poultry, and swine (the three most consumed livestock classes), as well as incomplete removal in typical waste management practices is a complex scenario given increasingly globalized food markets, increasing populations, developing countries, and greater urbanization that demands more food resources and often involves increasingly meat-centered diets (Van Epps and Blaney, 2016). The principles that guide antibiotic use in both agricultural and clinical settings vary between developed and developing countries, and often differs from one country to another. Van Boeckel et al. (2015) indicated that about 50 percent of antimicrobials are used incongruously, regardless of the setting, due to a lack of antimicrobial stewardship. Antimicrobial stewardship involves the choice, dosing, route, and duration of administration of a particular antimicrobial agent. It is defined as the administration of the right drug at the right dose, through the right route, at the right time, to the right patient, to ensure the best clinical outcome for treatment or prevention, thereby causing the least harm or toxicity in the patient and future patients (Doron and Davidson, 2011).
In many countries around the world, especially in developing countries, in addition to the use of antibiotics for reducing infections, antibiotics are also used for growth promotion (Kertz et al., 2017). In the U.S., the use of medically important antimicrobials for growth promotion in food-producing animals was eliminated by the Food and Drug Administration in 2017. However, 45 out of 155 countries are still using antimicrobials as a growth promoter according to the World Organization for Animal Health (OIE) (Wang et al., 2022). At present, there is an increasing trend toward restricted use of antibiotics in food animals. Therefore, it is important that the remaining 45 countries join the ban on use of antibiotics as growth regulators (Wang et al., 2022).
Hormones in animal manure
Manure is a renewable resource and an excellent source of macronutrients and micronutrients for crop production and has been used as an organic fertilizer for centuries. However, steroid hormones have recently emerged as environmental contaminants that fall under the category of endocrine disruptors. All vertebrates excrete hormones but most of the input of hormones in the environment can be traced to livestock production (Sosienski, 2017). Factors that can alter the hormone content of manure are ages of the animals, sex and reproductive state of the animal, and how the manure is stored and treated before application (Bartelt-Hunt et al., 2013). Before manure is applied on an agricultural field, it is often common practice to store manure in a holding facility and apply most of the manure at one time, generally in the spring before planting and/or in the fall after harvest.
Manure amendments to agricultural fields concurrently apply steroid hormones in addition to beneficial plant nutrients (Lange et al., 2002). When manure is applied to the field, it is not only the nutrients and organic matter that are applied, but also other compounds present in the manure, such as hormones and possibly antibiotics. There are two major movement pathways that manure-borne contaminants such as hormones can take once applied to the soil, surface runoff and leaching, both driven by precipitation. Surface runoff occurs when the contaminant of interest is soluble in water or is attached to soil particles and transported to a stream or waterway, and leaching takes place when the contaminant of interest becomes detached from its substrate and is transported through the soil profile by water movement (Sosienski, 2017). The chemical nature of hormone compounds causes the molecules to tend to associate with organic matter and soil particles, therefore the hypothesized primary transport mechanism for hormones from manure to waterways is mainly via surface runoff of eroded particles (Bera et al., 2011).
Hormones are lipophilic (fat soluble) organic molecules that generally do not dissolve in water (Arnon et al., 2008). Because of this, hormones tend to attach to sediment, soil particles, and organic matter; how tightly hormones bind with soil particles can be an indication of how likely the hormone will leach from the soil (U.S. EPA, 2013). Caron et al. (2010) found a positive correlation between sorption potential and soil organic carbon content, suggesting that hormone leaching and contributions to runoff may be minimized in soils with higher carbon content. Hormones in the environment typically degrade over time (U.S. EPA, 2013). The extent and rate of degradation can depend on a variety of factors such as the soil’s moisture content, temperature, and organic matter content, as well as the availability of light (Zhao et al., 2008). Microbial breakdown also appears to play a key role in the degradation of hormones; therefore, it is possible that hormones may persist for longer periods of time during colder, winter temperatures when microbial activity tends to be slower than during warmer months (Zhao et al., 2008).
Hormones are a difficult class of compounds to generalize in manure application studies because the amounts and types of hormones in manure varies with the type, age, and reproductive state of the herd or flock, as well as the storage technique of the manure (Lange et al., 2002; Bartelt-Hunt et al., 2013). However, new developments in manure land application methods have shown promise in pollution reduction from manure-applied fields. No-till and reduced tillage cropping systems restrict the movement of sediments and their related pollutants from agricultural fields, however, they require surface application of manure, so as not to disturb the soil (Maguire et al., 2011). Subsurface application of animal manure is becoming an increasingly popular technique to avoid the pollution associated with surface application while still maintaining no-till character. Due to the relatively low water solubility and high octanol water partition coefficients of steroid hormones, these molecules are more likely to remain in the soil by sorption with soil components and less likely to leach with water through the soil profile (Lee et al, 2003; Ying and Kookana, 2005).
Manure storage and treatment
Storing manure allows livestock and poultry producers with confined operations to better utilize their nutrient management plans and apply manure to address crop needs most efficiently. Adequate storage capacity enables operators to store manure during times of the year when no crops are growing and avoid applying manure on frozen or snow-covered ground, immediately before, during, and after rainfall events, or when the land may be water-logged or saturated (Zhao et al., 2008). Storing manure for extended periods may also minimize pathogen loads and promote degradation or adsorption of antibiotics and hormones (Lee et al., 2007). Technologies are now available to treat manure nutrients such that other disposal options become available. However, although many of these options are proven from an engineering standpoint, the costs are often too prohibitive for most producers to utilize. Livestock and poultry producers should weigh the economic viability of such technologies for their operations and consider all possibilities. For example, in some cases, nutrients from manure, such as phosphorus byproducts, can be recovered, sold and transported to locations low in phosphorus. Given that phosphorus is a nonrenewable resource, these byproducts could become an increasingly valuable source of income (Chesapeake Bay Commission, 2012).
Physical and chemical treatments are designed to separate the solids and liquids in manure slurry to make the manure easier to handle and transport. Physical treatment involves separating the solids from liquid manure through settling, filtration, screening or drying. Chemical treatment involves the addition of coagulants, such as lime, alum, and organic polymers to manure. Composting and anaerobic digestion are also treatment options. Composting is the time-proven process of aerobic biological decomposition of manure in a controlled environment. Research suggests that composting may promote antimicrobial degradation (Zhao et al., 2008). Anaerobic digesters are an emerging technology using oxygen-free environments in which bacteria break down manure, generating gases that may be captured for energy use.
Historically, the focus of manure management has been to utilize nutrients in manure for crop production. More recently, livestock and poultry producers, land grant universities, and government agencies have worked together to develop practices and systems to minimize the impact of manure production and utilization on the environment. Widespread implementation of appropriate practices will help reduce agricultural runoff and minimize potential environmental problems associated with emerging contaminants from livestock and poultry manure while improving soil health through judicious nutrient and organic matter application.
Soil health is the capacity of the soil to provide an environment for optimum growth and development of plants, while also ensuring the health of animals and humans. Humans have used animal manure for centuries as a nutrient source for soils. However, manure application affects many other soil properties such as water holding capacity, infiltration, bulk density, aggregate stability, fertility, and biological properties. The soil is a complex ecosystem and manure application affects this ecosystem by supplying nutrients and improving various soil properties. However, the extent to which it does can be extremely variable and depends on multiple factors including the chemical and physical properties of the manure itself and external factors including climate and soil characteristics. In addition, while the benefits of manure on various soil properties are clear, conclusions about the effect of manure on some soil properties must be approached cautiously (Rayne and Aula, 2020). The high variability in manure characteristics and the unpredictability of the response to the environment pose a challenge to sustainable management of manure. The benefits to the soil must also result in improved future plant and/or animal productivity while reducing the threat to the environment.
In reaction to the potential risk to the environment if manure is mishandled, the U.S. and other countries have developed regulations and restrictions related to the storage and spreading of manure. The importance of this resource and its benefit to agricultural production and sustainability of the environment are well recognized. The benefits of manure application to overall soil quality are numerous and its application to land is a viable option to improve and perhaps restore the health of degraded acreage (Rayne and Aula, 2020). However, manure must be utilized and managed properly and there are aspects of manure application in relationship to soils that should be further explored in future research. Nutrient use efficiency from manure is one area in need of additional investigation; finding ways to improve nutrient uptake from manure may reduce the loss of nutrients from the land and the subsequent pollution of the environment. Methods to increase the degradation and breakdown of antibiotics and hormones in manure is another area where research is lacking. There remains a need to better understand manure decomposition and the transformation and degradation of antibiotics and hormones in manure and how these processes affect soil health over time. Monitoring nutrients as well as different types of antibiotics and hormones throughout an environmental system will provide additional information on the fate, accumulation, and movement of these animal manure components from manure amended soils.
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