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Agriculture, Ecosystems and Environment 78 (2000) 93–106
Review
A review of microbiology in swine manure odor control
Jun Zhu ∗
Biosystems & Agricultural Engineering, University of Minnesota, Southern Experiment Station, 35838-120th Street, Waseca, MN 56093, USA
Received 15 April 1999; received in revised form 16 July 1999; accepted 30 July 1999
Abstract
Generation of odors is a complex process that involves many bacterial species, producing an extensive array of volatile
organic compounds under different manure storage systems currently used. A lack of understanding of the basic microbiology
in manure leads to a poor odor prevention and control from animal wastes. This review covers pertinent available information
about the indigenous bacterial genera in swine manure and their potentials of producing odorous volatile compounds. It
addresses not only the odorous compounds in swine manure but also the inherent relations between the bacterial species
and the related compounds. It also discusses several odor control techniques that have been developed based on microbial
activities and the limitations with these techniques. Two bacterial genera, Eubacterium and Clostridium, are most likely the
major contributors to odorous volatile fatty acids. It appears that anaerobic lagoons may not be an appropriate choice for
treating swine manure for odor control due to the reduced methonogenic activities resulted from the low temperatures in
lagoon liquid. Also, it seems questionable that the microbial-based manure additives will work, without aeration, in a real
storage system for the purpose of odor control. ©2000 Elsevier Science B.V. All rights reserved.
Keywords: Microbiology; Swine manure; Odor control
1. Introduction
The trend toward high-density, confinement rearing of hogs has increased tremendously in recent
years. Associated with this increase is the air pollution problem (odors) which has become a center
of public concern. This is reflected in the increased
frequency of odor-related complaints in areas where
swine production facilities are more intensified. Odor
management is currently impacting many aspects of
the swine industry and there appears a potential that
the sustainability, productivity, and profitability of
swine producers will be dependent upon whether they
∗ Tel.: +1-507-835-3620; fax: +1-507-835-3622.
E-mail address: zhuxx034@tc.umn.edu (J. Zhu).
can reduce the emission of offensive odorants from
operating swine production units to a level which
surrounding communities could tolerate. Therefore,
there exists an acute need for effective methods of
odor control, for if the swine industries are to coexist
with their neighbors, such control measures will have
to be put into operation.
Microbial activities are normally considered to be
responsible for the malodor generation from the stored
swine manure slurry. As a matter of fact, microbes
play a major role in both production and reduction of
malodors. In odor generation, the odorous volatile organic compounds are the normal end products or intermediate products of fermentative degradation of fecal
substances by anaerobic bacteria. In odor reduction,
many odor control techniques that are being developed
0167-8809/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved.
PII: S0167 - 880 9 (99 )00116 -4
94 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
rely on the microbial properties in the swine manure.
Since the malodor originates from microbial activities involving a variety of microbes, understanding the
characteristics of the microflora present in swine manure is essential for developing effective odor control
techniques.
This paper reviews the available information in the
literature related to the types of bacteria in swine manure, the potential odorous compounds associated with
different bacterial genera, and the corresponding techniques used to control odor based on microbiological
principles. Areas that need further research are also
recommended.
2. Microflora in swine manure and odor indicators
2.1. Bacterial genera indigenous to swine manure
Several studies have revealed the types of bacteria that can be isolated from fresh intestinal or fecal material of swine. Rall et al. (1970) reported that
there were six groups of swine fecal bacteria according
to metabolic functions: lactose fermenters; nonlactose
fermenters; Clostridium sp.; Lactobacillus sp.; Enterococci; and Staphylococcus sp.. The population sizes
for the identified bacterial groups in descending order
are lactose fermenters, Lactobacillus sp., Clostridium
sp., nonlactose fermenters, and Staphylococcus sp..
The classifications of bacterial groups based on functions instead of genera or species may not be of much
help in determining the contributions of each single
species to manure odor generation. On the other hand,
it is usually difficult to clearly classify the bacterial
groups only according to their metabolic characteristics. For example, Enterococci in the above discussion
can also be grouped into lactose fermenters (Orvin,
1986).
Nuru et al. (1972) found that the fecal bacteria of
pigs mainly consisted of gram-positive cocci (Streptococcus, Peptostreptococcus, and Staphylococcus),
Lactobacillus, Escherichia, and Bacillus. By using
strictly anaerobic culturing methods, Salanitro et al.
(1977) concluded that the predominant fecal microflora isolated from adult swine comprised several
bacterial groups; namely, fecal streptococci, Eubacterium sp., Clostridium sp., and Propionibacterium
acnes. Similar results were also reported from another
study conducted by Russell (1979) which showed
that the gram-positive cocci were the predominant
organisms identified in swine manure, containing
Streptococcus, Peptococcus, Peptostreptococcus, and
Megasphaera. The reason that Russell (1979) classified Megasphaera as gram-positive was because most
of strains in this group stained gram-positive in his
study.
According to the above researchers, the swine fecal
bacterial genera found can be listed in order of quantity
from high to low as: Gram-positive cocci (ca. 39%),
Eubacterium (ca. 27%), Lactobacillus (ca. 20%),
Gram-negative rods (Escherichia, ca. 8%), Clostridium (ca. 4%), and some other minor groups such as
Propionibacterium acnes and Bacteroides (<2%).
Among these bacterial genera, Clostridium sp., Lactobacillus sp., Peptostreptococcus, Eubacterium, Peptococcus, Propionibacterium acnes, Bacteroides, and
Megasphaera are anaerobes; Streptococcus, Staphylococcus, and Bacillus are facultative anaerobes;
Escherichia are aerobes or facultative anaerobes. Obviously, the anaerobic or facultative anaerobic bacteria
account for the major portion of the bacterial species
found in swine manure due to the anaerobic environment in the intestinal tract of pigs. The level of aerobic bacteria (if Escherichia can be counted as one)
is low.
Identification of the bacterial genera in swine
manure is important to reveal the microbial consortium, but it is not enough to explain the complex
odor generation processes taking place in manure
storage systems. In order to investigate the potential of producing odorous compounds by the bacteria from different groups, a further examination on
each individual genus of the indigenous bacteria is
needed.
2.2. The characteristics of indigenous bacterial
species
2.2.1. Streptococcus
Streptococcus is a group of chemoorganotrophs
with fermentative metabolism (microbes that use
reduced and preformed organic compounds as
sources of energy, hydrogen, electrons, and carbon for biosynthesis). Most of the species are
facultatively anaerobic, but some require addiJ. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106 95
tional CO2 for growth and some may be strictly
anaerobic. Optimum growth temperature is usually 37◦C but maximum and minimum temperatures vary among species. Neutral or near neutral pH will favor the growth and low (<4.0) or
high (>9.6) pH will inhibit the growth. All streptococci ferment carbohydrates, producing predominantly lactic acid; minor amounts of acetic and
formic acids, ethanol, and CO2 may also be produced. Many species in this genus produce ammonia. A total of five species were found in swine
manure (Russell, 1979). However, no information
regarding the identification of these species was
given.
2.2.2. Peptostreptococcus
Peptostreptococcus is a group of anaerobic
chemoorganotrophs that metabolize peptone and
amino acids to acetic, formic, propionic, caproic,
iso-butyric, butyric, iso-valeric, and iso-caproic acids.
Volatile amines and various alcohols may also be
produced. The pH for growth ranges from 6.0 to 8.0
with the optimum being 7.0–7.5, and the temperature
ranges generally from 25 to 45◦C with optimum being
35–37◦C. There is a total of three species identified
in swine manure in this genus (Russell, 1979). They
are P. asaccharolyticus, P. magnus, and P. productus.
2.2.3. Eubacteria
Eubacteria is a group of obligately anaerobic
chemoorganotrophs that produce mixtures of organic
acids from carbohydrates or peptone. Growth usually
is most rapid at 37◦C and pH near 7. Most of them often produce large amounts of butyric, acetic, formic,
and lactic acids (Moore and Holdeman, 1986).
Available literature regarding the number of species
in this genus identified in swine excreta is limited.
According to Russell (1979), a total of five species in
this genus has been identified so far (E. aerofaciens, E.
rectale, E. tenue, E. ventriosum, and E. lentum). There
were another seven species in this genus that could
not be identified in his study. Since many species in
this genus produce volatile fatty acids and indole and
more than half of the species have not been identified,
the effect of this bacterial group in general, and of
individual species in particular, on swine manure odor
generation should receive further research.
2.2.4. Lactobacillus
Lactobacilli are strictly fermentative, aero-tolerant
or anaerobic, and aciduric or acidophilic bacteria. With glucose as a carbon source, lactobacilli
may be either homofermentative, producing >85%
lactic acid, or heterofermentative, producing lactic
acid, CO2, ethanol, and/or acetic acid in equimolar
amounts.
Lactobacilli grow best in slightly acidic media with
pH of 4.5–6.4. Optimal pH for growth usually ranges
from 5.5 to 6.2. Growth ceases when pH 3.6–4.0 is
reached, depending upon the species and strains. The
growth rate is often reduced when the environment
becomes neutral or alkaline. Growth temperature
ranges from 2 to 53◦C with an optimum range of
30–40◦C.
There were nine species in this group found in
swine manure and six of them were identified (Russell,
1979). Since the major product of this genus is lactic acid (only a small amount of acetic acid produced
by some of the species under heterofermentative condition), it could be assumed that the contributions to
odor offensiveness by the biological activities of this
bacterial group is not significant.
2.2.5. Escherichia
The typical species included in this genus is Escherichia coli which is aerobic or facultatively anaerobic, having both respiratory and fermentative types
of metabolism. Glucose and other carbohydrates are
fermented by the bacteria with the production of pyruvate, which is further converted into lactic, acetic,
and formic acids. The optimum growth temperature is
37◦C. Most of the strains in this species (90–100%)
produce indole which is very odorous.
2.2.6. Clostridium
Most species in genus Clostridium are obligately
anaerobic, although tolerance to oxygen varies widely
and some species will grow but not sporulate in the
presence of air at atmospheric pressure. For most
species, growth is most rapid at pH 6.5–7 and at
temperatures 30–37◦C; the range of temperature for
growth is 15–69◦C (Cato et al., 1986).
Clostridium often can ferment amino acids to produce energy by oxidizing one amino acid and using
another as an electron acceptor in a process called
96 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
‘the Stickland reaction’ (Prescott et al., 1996). This
generates ammonia, hydrogen sulfide, fatty acids, and
amines during the anaerobic decomposition of proteins. The volatile fatty acids produced by different
species in this genus in order of quantities from high
to low are acetic, butyric, caproic, lactic, formic, propionic, succinic, valeric, iso-butyric, iso-caproic, and
iso-valeric acids. Some of the species also produce
indoles and phenols. There were four species in this
genus found in the swine excreta (Russell, 1979),
but none of them were identified. The complexity of
the odorous products produced by Clostridium shows
a great potential that the species within this genus
may be major contributors to swine manure odor.
Therefore, to better understand the involvement of the
bacteria in this group in producing different odorous
compounds, further research is needed that should
focus on the identification of the species found in
swine manure.
2.2.7. Propionibacterium
Propionibacterium contains genera which are either obligately anaerobic or aerotolerant. Bacteria
included in this group can produce propionic acid and
acetic acids and lesser amounts of iso-valeric, formic,
succinic, and lactic acids. The optimum growth
temperature is between 30 and 37◦C and pH near
neutral.
There are only two species found in swine manure,
i.e., Propionibacterium acnes and Propionibacterium
granulosum. Both species have the general characters
as discussed above; however, only P. acnes has the
capability of producing indole.
2.2.8. Bacteroides
Bacteroides are obligately anaerobic chemoorganotrophs metabolizing carbohydrates or peptone. Fermentation products include a combination of succinic, lactic, acetic, formic or propionic, and butyric
acids. When n-butyric acid is produced, iso-butyric
and iso-valeric acids are also present. Growth usually
progresses most rapidly at 37◦C and pH near 7.
Two species in this genus have been found in swine
manure and only one of them has been identified (B.
ruminicola). B. ruminicola has an optimum growth
temperature of 37◦C with a growth range between 25
and 45◦C (Holdeman and Moore, 1974).
2.2.9. Megasphaera
There are only two species (M. elsdenii and M.
cerevisiae) in this genus listed in Bergey’s Manual of
Determinative Bacteriology (Holt et al., 1994). Bacteria in this genus are anaerobic chemoheterotrophs
that ferment lactate to produce acetate, propionate,
and volatile fatty acids with carbon numbers from 2
to 6 including 4-carbon straight- and branched-chain
acids. Sulfur containing compounds are also produced
by this genus. The growth temperature ranges from
25 to 40◦C and the optimal pH for growth is slightly
above neutral (pH ≈ 7.4).
The bacterial profile discussed above may not completely cover all the bacterial species in swine manure
(e.g., methanogens were not reported in any of the
above studies, while it is a common bacterial genus
in the gastrointestinal tract of all mammals); however, it does provide information on most of the indigenous genera in the swine manure, especially those
producing odorous compounds. To relate these genera
to malodor production requires a basic knowledge of
the major odorous compounds in swine manure. Thus,
a thorough review of the past research regarding the
odorous compounds in swine manure appears essential to determine the relationship between the bacterial
genera and these compounds.
2.3. Odorous compounds in swine manure
A considerable amount of research has been conducted in determining odorous compounds in swine
manure (Merkel et al., 1969; Barth and Polkowski,
1974; van Gemert and Nettenbreijer, 1977; Schaefer,
1977; Lunn and van De Vyver, 1977; Spoelstra, 1977;
Spoelstra, 1980; Yasuhara and Fuwa, 1980; Williams,
1984; Yasuhara et al., 1984; O’Neill and Phillips,
1992). Generally speaking, the odorous compounds
are produced and accumulated in the storage systems
where the mixture of feces and urine is decomposed
by bacteria under the prevailing anaerobic conditions.
These compounds can be divided into four different
chemical classes (Mackie, 1994).
2.3.1. Volatile fatty acids (VFAs)
Typical acids in this group consist of acetic, propionic, butyric, iso-butyric, valeric, iso-valeric, caproic,
and capric acids. The VFAs can be produced from
J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106 97
Table 1
The indigenous bacterial genera in swine manure and their odorous compounds
Bacterial genera Potential odorous compounds
Streptococcus formic, acetic, propionic, butyric acids, ammonia and volatile amines
Peptostreptococcus formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic,
iso-valeric, ammonia and volatile amines, and iso-caproic acids
Eubacterium formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic,
iso-valeric, iso-caproic acids, indoles and phenols
Lactobacilli formic, acetic, propionic, and butyric acids
Escherichia formic, acetic, propionic, and butyric acids
Clostridium formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic,
iso-valeric, iso-caproic acids, indoles and phenols
Propionibacterium formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic, iso-valeric, iso-caproic acids, indoles
and phenols
Bacteroides formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic, iso-valeric, iso-caproic acids, ammonia
and volatile amines
Megasphaera formic, acetic, propionic, and butyric acids, iso-butyric, valeric, caproic, iso-valeric, iso-caproic acids, volatile
sulfur-containing compounds
the deamination of amino acids that are produced during the process of protein degradation and breakdown
of carbohydrates. In the gastrointestinal tract, a neutral pH (6–7) normally prevails. Under this condition, deamination is the major route for metabolism
of amino acids, which results in the production of
VFAs, CO2, H2, as well as ammonia. Bacterial genera involved in this activity normally include Eubacteria, Peptostreptococcus, Bacteroides, Streptococcus,
Escherichia, Megasphaera, Propionibacterium, Lactobacilli, and Clostridium.
2.3.2. Indoles and phenols
Indole, skatole, cresol, and 4-ethylphenol appear
to be the major components included in this group
of compounds. Phenolic compounds such as phenols
and p-cresols are produced from the microbial degradation of tyrosine and phenylalanine in the intestinal
tract of animals (Ishaque et al., 1985). Metabolism of
tryptophan can result in the production of indoleacetate which is subsequently converted into skatole
(3-methylindole) and indole by a different group of
bacteria (Mackie, 1994). Bacterial genera involved
in these processes include Propionibacterium, Escherichia, Eubacteria, and Clostridia.
2.3.3. Ammonia and volatile amines
Volatile amines include putrescine, cadaverine,
methylamine, and ethylamine. Usually, aliphatic
amines (methyl- and ethyl-amine) are present at low
concentrations. During the storage of fresh manure,
amino acids can most likely undergo decarboxylation
to produce putrescine, cadaverine, and ammonia. Bacterial genera involved in this activity include Streptococcus, Peptostreptococcus, and Bacteroides. Another
big source of ammonia is from urea and nitrates in
addition to amino acid deamination (Spoelstra, 1980).
2.3.4. Volatile sulfur-containing compounds
Included in this group are sulfides as well as
methyl- and ethyl-mercaptans. The sulfur-containing
compounds are produced by bacteria through two
processes, i.e., reduction of sulfate and metabolism
of sulfur-containing amino acids. Sulfate reduction
proceeds via either assimilatory or dissimilatory pathways. In the first process, bacteria produce enough
reduced sulfur for cell biosynthesis, while in the second process sulfate is utilized as terminal electron
acceptor and large quantities of sulfide are produced
(Hao et al., 1996). Bacterial genera involved in this
activity include Megasphaera.
The odorous compounds as well as the bacterial
species associated with these compounds are summarized in Table 1. It appears that all the listed bacterial genera found in swine manure are more or less
related to different types of odorous compounds. For
odor control only, it may not be realistic to deal with
all the genera unless the manure needs to be sterilized. Since one bacterial species may produce one or
98 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
more odorous compounds and different compounds
may contribute differently to the overall odor offensiveness of the manure, it seems helpful and worthwhile to find the major odorous compounds as well as
the bacterial species associated with them. Once the
bacterial species producing the major odorous compounds are determined, effective strategies and techniques for controlling these bacterial activities may be
developed.
2.4. Major odor indicators and the related bacterial
genera
Research on the major indicators for malodors of
swine manure has been carried out for many years.
Merkel et al. (1969) found alcohols were unimportant
in determining the nature of swine confinement manure odors. Barth and Polkowski (1974) reported that
the volatile organic acids correlated best with the odor
intensity. Ammonia was thought to be useful as an indicator for malodor, but in spite of the relatively high
concentrations and the easy determination ammonia
was proved to be a poor parameter in evaluating odor
intensities (Lunn and van De Vyver, 1977). A study
conducted by Spoelstra (1977) showed that indole and
skatole could not be recommended as indicators for
malodor because the concentrations of these two compounds might decline during storage. Later, Spoelstra
(1980) reported in another study that both ammonia
and hydrogen sulfide were not suitable indicators for
the smell. The most pungent and the greatest variety of
obnoxious smelling compounds originate from the decomposition of proteins. Ammonia does not reflect this
degradation kinetics of the manure because the major
part of ammonia in the manure originates from urea
hydrolysis. Moreover, ammonia remains unchanged
by methanogenesis and shows a retarded reaction to
aerobic treatment compared with organic volatiles.
Hydrogen sulfide formation also does not reflect manure degradation kinetics because a relatively large
part is derived from sulfate reduction. He concluded
that the VFAs seemed to be useful indicators to test
whether an effect has occurred in all odor-abatement
methods. The VFAs show typical reactions for the
group of accumulated volatile compounds when environmental changes are made in swine manure to
diminish odor. Williams (1984) found that the most
widely applicable indicator was supernatant biochemical oxygen demand (BOD) both during aerobic treatment and post-treatment storage; VFAs, total organic
acids, indoles and phenols can indicate acceptable
and unacceptable limits of offensiveness during aerobic treatment and post-treatment storage; sulfide is a
misleading indicator during aerobic treatment but is
a useful indicator during post-treatment storage; and
ammonia is of no value as an indicator. A study conducted by Zahn et al. (1997) reported that the volatile
organic acids with carbon numbers from 2 to 9 specifically demonstrated the greatest potential for the decreased air quality. Therefore, according to the above
researchers, it appears that VFAs could be used as a
suitable odor indicator for swine manure.
However, in recent years, it has been shown by
a few studies that different VFAs will have different contribution to the odor generation. Thus, a further classification within this group is needed to determine the potential of producing malodors by different
VFAs so the specific bacterial species involved can be
studied.
The odorous nature of VFAs progresses from pungent odors of formic and acetic acids to the distinctly
unpleasant and offensive odors of valeric and caproic
acids (Morrison, 1987). Although the short chain acids
are present in much higher concentrations and have
higher volatility, the VFAs with higher carbon numbers have lower odor detection threshold thus are more
offensive in nature (Mackie, 1994). Therefore, the high
concentration of VFAs in swine manure may not necessarily cause high intensity of malodor as a large portion of the VFAs could be composed of short chain
acids with less odor potential. A study conducted by
Zhu et al. (1997) appeared to provide evidence supporting this argument. They evaluated five commercial pit additive products and found that some products
could reduce odor threshold without significantly reducing the total amount of VFAs. The offensive odor
potential was not directly associated with the total concentration of VFAs in the manure. It was depending
upon the types and characteristics of certain acids (not
necessarily existing in high concentrations in the manure). Therefore, the purview of VFAs responsible for
odor generation can be narrowed down to those with
long carbon chains ( in this group include iso-butyric, valeric, iso-valeric,
caproic, and iso-caproic acids. The bacterial genera
J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106 99
Table 2
pH and temperature ranges for growth of the related bacteria
Bacterial genera pHa Temperature (◦C)a Oxygen tolerance
Peptostreptococcus 6–8 25–45 (35–37) No
Eubacteria 6.5–7.5 20–45 (37) No
Clostridium 6.5–7 15–69 (30–37) No for most strains
Propionibacterium 6.5–7.5 30–37 (35) No to aerotolerant
Bacterioides 5–8.5 25–45 (37) No
Megasphaera 7.4–8.0 25–40 (30) No
a Numbers in parenthesis are optimum conditions.
producing these compounds include Peptostreptococcus, Clostridium, Bacteroides, Eubacteria, Propionibacterium, and Megasphaera (Table 1).
The bacterial genera in Table 1 are normally active
in the specific environment, e.g., in the gastrointestinal tract of animals, where the bacteria can effectively
perform their metabolic activities for growth. That environment may change or even no longer exist once
the feces are excreted. Since swine manure contains
sufficient nutrients for bacterial growth, the limiting
factors that could affect the growth of these bacterial
genera are most likely pH and temperature. The suitable ranges of these two parameters for the growth of
different bacterial genera are presented in Table 2. Deviations in pH and temperature from the values listed
in Table 2 may not completely stop the bacterial activities in producing volatile fatty acids, but may affect
the productivity of different bacterial genera in varying degrees.
According to Table 2, genus Clostridium has the
widest temperature range for growth among the bacterial genera. Thus, as compared with other bacterial
genera, Clostridium could be more active in producing
odorous acids in the real manure storage environment,
especially at low temperatures. Since little appears to
have been made in systematically studying the microbes at the species level in swine manure under the
storage environment, experimental data that estimate
the contributions of this genus to the VFA production on a quantitative basis are not available. However,
there is plenty of evidence showing that Clostridium,
if the environment favors the growth of this group of
bacteria, is a major genus that is responsible for producing all types of VFAs through amino acids fermentation (Gunsalus and Stanier, 1961; Mead, 1971;
Gottschalk, 1985; Hill, 1986). In operating lagoons
or earthen basins, the storage temperature of wastes
usually ranges from 10 to 20◦C, depending upon the
season (Spoelstra, 1980). Local lagoon waste temperature variation has also been reported by several other
researchers (Ohio, 2–27◦C (White et al., 1977); Oklahoma, 0–30◦C (Rice, 1977); Georgia, 3–25◦C (Smith
and Franco, 1985). The temperature range for manure stored in the pits is between 2 and 18◦C (Donham et al., 1985). The pH range for swine manure is
between 6.5 and 7.5 (Cooper and Cornforth, 1978).
Comparing these situations to the parameters listed in
Table 2, plus the anaerobic environment that always
exists in the liquid manure storage systems where aeration is not available and the availability of nutrients, would suggest that Clostridium very likely is a
genus that can play a major role in producing odorous
VFAs.
Genus Eubacterium could also make significant
contributions to generating odorous acids. Although
it has a narrower temperature range than Clostridium,
it has the largest population among the genera listed
in Table 2 and most of the strains produce long-chain
fatty acids. So it is reasonable to assume that, under
the manure storage environment, the major portion of
the odorous VFAs could be produced by these two
genera. A substantial increase in various VFAs after
manure stored anaerobically for 24 h were observed
by Williams (1981), which could be due mainly to
the active growth of these bacteria. However, this
hypothesis needs further study. It is also reasonable
to assume that controlling the bacterial growth in
these two groups may help reduce malodor generation. Unfortunately, a lack of experimental data to
verify this postulate and the incomplete identification of the species within these two groups make it
difficult to draw specific conclusions in terms of the
odor-related acids production with regard to different
bacterial species. Therefore, further research on these
100 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
genera seems of significance in determining the types
and quantities of odorous compounds produced by
different species in these two groups.
As mentioned above, pH could be a factor that affects bacterial growth. It can be seen from Table 2 that
all the bacterial genera have a neutral or near neutral
pH for their growth. This offers an opportunity to regulate bacterial growth by adjusting the pH in manure
liquid. This can be achieved more easily than controlling temperature that is neither practical nor effective
at the farm level. There have been several studies in
which alkaline materials were added into manure to
increase the manure pH (Hammond and Day, 1968;
Veenhuizen and Qi, 1993; Vincini et al., 1994; Bundy
and Greene, 1995). These studies demonstrated odor
reductions in varying degrees when manure pH was
raised to a range of 8–11. However, none of these
studies presented an explanation for the mechanisms.
Based on previous discussions, it could be concluded
that one major reason that the raised pH could reduce
odor is that it inhibits the growth of those odor-causing
bacteria indigenous to swine manure. Another mechanism of reducing odor by alkaline materials is due
to the precipitation of volatile fatty acids by formation of salts. At high levels of pH, the formed salts
will not be converted back to acids; thus, both the levels and volatility of the odorous acids will be reduced
(Rainville and Morin, 1985; Morrison, 1987).
One problem associated with the pH adjustment is
the emission of large quantities of either ammonia (at
the raised pH) or hydrogen sulfide (at the lowered
pH) from the treated swine manure. The emission of
these two gases may cause severe problems to the
environment and losses of animals and human lives
under certain conditions. Therefore, to avoid the potential damage caused by the emission of these two
gases during the pH adjustment, it would be better to
treat fresh manure instead of aged manure. In fresh
manure, the bacterial activity of decomposing organic
substances to form ammonia and hydrogen sulfide has
not fully developed, so the volatile portion of the gases
is relatively low. Accordingly, these two gases may not
reach a threatening level on both the environment and
the properties in a short time period. The problem with
this treatment is that continuous adjustment of pH has
to be conducted to maintain the adjusted pH. Otherwise, due to the biological activities, pH will change
and odor may return during the manure storage time.
3. Odor control techniques
In this chapter, only the major odor control techniques closely relevant to the bacterial properties will
be discussed. Other techniques that are less related to
the biological treatment in essence, such as storage
tank covers, solids–liquid separation, and chemical deodorants are not addressed here.
3.1. Aeration
The value of aeration in reducing offensive odors
has been demonstrated by a number of workers using olfactometric evaluation methods (Williams et al.,
1984; Williams et al., 1989; Pain et al., 1990; Sneath
et al., 1992). The basic principle of this treatment is to
provide, by whatever means, enough dissolved oxygen to aerobic bacteria so they can actively decompose
the odorous compounds; hence achieving odor reduction. There have been some research efforts made to
link aeration with specific microorganisms in terms of
reducing odor (Evans et al., 1983; Evans and Baines,
1985; Evans et al., 1986; Munch et al., 1987). According to these studies, a group of microorganisms
called ‘heterotrophs’ are commonly assumed to be the
most numerous and important in this biological treatment process. However, a complete profile of the bacterial genera within this group seems not available.
Past studies only investigated the overall performance
of the aerobic bacteria, with the characteristics of each
individual bacterial genera being untouched.
The importance of bacteria in aeration has not received specific attention since most of the papers related to aeration were focused on the development and
improvement of all kinds of aerators mechanically.
However, even when these papers are reviewed, the
inherent relation between bacteria and the aeration efficiency of aerators can still be perceived. One study
showed that in general, aerator performance was better
at raised temperatures (Cumby, 1987a). Another study
showed that if the liquid temperature was kept at 15◦C
or above, low dissolved oxygen content could still
achieve the removal of carbonaceous material from
pig slurry (Smith and Evans, 1982). No explanations
were presented by the authors for these observations.
But if examined from the standpoint of microbiology,
these results might be explainable. There have been
J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106 101
reports, although limited, showing that several aerobic bacterial species could effectively degrade VFAs
at raised temperatures (Bourque et al., 1987; Jolicoeur
and Morin, 1987). Therefore, it may not be the aerator that worked better at raised temperatures. It could
be the microbes that enhanced their metabolic processes in decomposing organic materials at high temperatures. The role of microbes in improving aeration
efficiency is evidently important and requires further
study. While aeration alone does not destroy odors.
Since the gastrointestinal tract of pigs is strictly
anaerobic, the levels of the aerobic bacteria, if any,
cannot be high. Thus, under aeration, whether the existing aerobic bacteria are able to compete for nutrients
actively, to establish their growth firmly, and to reach
dominant levels rapidly becomes critical. And the assumption of ‘a group of aerobic heterotrophs’ playing
a major role in aeration may not hold unless dominant
population levels of these bacteria have been reached.
This depends largely on the bacterial species. In general, the microbial species having the fastest growth
rate and the ability to utilize most of the available organic matter will be the predominant species (Loehr,
1974). Since the tolerance of different bacterial genera or species to the living environment and the ability
to effectively digest the odorous organic compounds
varies, the identification of the aerobes indigenous to
swine manure will be of profound significance to help
find or develop good aerobic bacterial species that can
be used in assisting aeration.
To date, ample research has been conducted in either
improving the aeration efficiency of different aerators
(Cumby, 1987b) or reducing the extent of aeration
(Ginnivan, 1983; Zhang et al., 1997). However, research attention that has been paid to studying the
other half of the story, i.e., microbes, appears meager.
Due to the diversities of not only the bacterial genera but also their functions, it is not unreasonable to
suggest that more fundamental research in completely
determining the microbiological activities of different
bacterial genera in aeration be needed.
3.2. Anaerobic lagoons
Anaerobic lagoons are a process in which microorganisms are used under anaerobic conditions to
convert biodegradable organic materials to odorless
gases, such as methane and carbon dioxide, and nonbiodegradable solids. There are basically three steps
involved in the process, i.e., hydrolysis, acidogenesis, and methanogenesis. The key to preventing odor
production is that the balance between the second
and third step has to be maintained. In other words,
the production of acids by the indigenous bacteria
and the consumption of acids by the methanogens to
produce methane and carbon dioxide have to be in
equilibrium. Otherwise, malodor may result.
Methanogens are a group of bacteria mainly responsible for methane production (Wolfe, 1971).
Methanogens thrive in anaerobic environments rich
in organic matter: the rumen and intestinal system of
animals, fresh water and marine sediments, swamps
and marshes, hot springs, and anaerobic sludge digesters (Prescott et al., 1996). Methanogens are very
strictly anaerobic bacteria and all grow by oxidizing
hydrogen. They can grow well in either mesophilic
(20–45◦C) or thermophilic (40–75◦C) temperature
ranges depending upon genera. For most genera, the
minimum pH for growth is ca. 6; some genera (e.g.,
Methanococcus) can grow at pH as high as 9.2. Since
the methanogens are the working force in the anaerobic decomposition process, whether an anaerobic
treatment process can function well depends largely
on the performance of the methanogens.
Anaerobic lagoons are designed to employ the
methanogens to decompose the organic substances
in swine manure under anaerobic environments. Unfortunately, many anaerobic lagoons do not function
as properly as designed due to overloading and bad
management and complaints about the odor generated
from these lagoons have risen widely. As discussed
early, the final products of microbial degradation of
carbonaceous material in an anaerobic natural ecosystem are methane and carbon dioxide. However, little
or a relatively low methane formation was observed
in the anaerobic storage system (Stevens and Cornforth, 1974). This may deserve an explanation from
the microbiological point of view.
The major factor that influences the methanogenic
process for methane production is the low temperature in lagoons. In operating lagoons, the storage
temperature of wastes usually ranges from 10 to
20◦C, depending upon the season (Spoelstra, 1980).
Local lagoon temperature variations have also been
reported by several other researchers (2–27◦C for
102 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
Ohio; 0–30◦C for Oklahoma; 3–25◦C for Georgia). These temperature ranges generally are lower
than the optimum mesophilic temperature (35◦C)
for most of the methanogens to function properly.
There have been three orders of methanogens found
so far (Methanobacteriales, Methanococcales, and
Methanomicrobiales), consisting of 18 genera and 39
species. Genera included in Order I will not grow
below 60◦C (Boone and Mah, 1989a). The growth
temperature range for genera in Order II is between
25 and 86◦C depending upon species (Whitman,
1989). In Order III, most genera have optimum
growth temperatures higher than 20◦C, only three
species start growth at 15◦C (Methanogenium cariaci,
Methanococcoides methylutens, and Methanogenium
marisnigri) and one genera (Methanothrix) with three
species start growth at 3◦C (Boone and Mah, 1989b).
Obviously, the number of species that can grow well
at the psychrophilic temperature range appears limited
so the methane fermentation can not be high in this
temperature range. Although methane fermentation in
nature occurs below 10◦C (Svensson, 1975) and was
observed as low as 4◦C (Stevens and Schulte, 1979),
methanogens produce methane at a much lower rate
and grow much slower at lower temperatures (Zeikus
and Winfrey, 1976; Van den Berg, 1977). Allen
and Lowery (1976) reported that the mean biogas
production rate from a full-scale swine lagoon was
0.006 m3/m2-day for a mean lagoon temperature of
14◦C and 0.55 m3/m2-day for a 3-day period when
the lagoon temperature was 27.5◦C. Surprisingly, a
difference of 13.5◦C in temperature would cause a
reduction in methane production by ca. 92-fold due
to the low activity of methanogens, indicating how
important the temperature is in the methanogenesis.
This low activity of methanogens finally has resulted
in the accumulation of odorous fatty acids and the
generation of odor.
The low activity of methanogens in methanogenesis
due to low temperature has also caused other problems
associated with this process. First, the solids retention
time has increased and lagoons are liable to overloading. Stevens and Schulte (1979) found that low temperature digestion (<25◦C) required a solids retention
time approximately twice as long to achieve the same
volatile solids reduction as in the mesophilic digestion. Safley and Westerman (1992) showed that at low
temperatures (>10◦C), not only has the retention time
to be increased but the loading rates of organic wastes
have to be decreased. It could be inferred from these
studies that the capability of treating swine manure
by anaerobic lagoons could be limited due to the low
temperatures, and more critical management appears
needed to avoid overloading. As a matter of fact, overloading has become a major problem for the anaerobic
lagoon systems currently used in the middle and southern areas in the United States due to the fast-growing
swine industry producing a huge volume of manure in
a short time period. Therefore, the balance between the
acids produced by the indigenous bacterial groups and
the acids consumed by the methanogens for methane
formation can hardly be achieved. This is why there
is little methane formed in, and there is strong offensive odor generated from, the waste storage lagoons.
According to the above analysis, if no restrictions are
expected to be placed on the growth of the swine
industry, it might be worthwhile to reexamine the use
of anaerobic lagoons for storing and treating swine
manure from the standpoint of odor control.
3.3. Microbial manure additives
The idea of using manure additives to control odors
was proposed ca. 20 years ago and a considerable
amount of research effort has been spent in this field.
Past researchers rarely found any of the pit additive
products to be effective in reducing odor levels of
swine manure (Cole et al., 1975; Ulich and Ford, 1975;
Sweeten et al., 1977; Warburton et al., 1980; Ritter
and Eastburn, 1980). Although Al-Kanani et al. (1992)
did show some effect on odor control using peat moss,
the usage is excessive (8%). The inefficiency of manure additives for odor control partially could be due
to the complexity of odorous components in swine
manure; however, the key hindrance to the development of effective manure additive products rests with
a lack of understanding of the biological activities occurring in the stored swine manure. The wildly used,
trial-and-error based, methods to evaluate manure additive products are not only time consuming but also,
in most cases, provide little information on the mechanisms involved. Thus, in order to develop effective additive products, there exists a necessity to understand
both the basic working principles of the additives and
the environmental characteristics in the manure that
J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106 103
may affect the chemical, physiological, and biological
processes of the additives.
According to Liao and Bundy (1994) and Barrington (1994), microbial digestive additives contain
bacteria or enzymes that eliminate odors and suppress
gaseous pollutants by their biochemical digestive
processes. There have been only a few efforts made
to investigate the bacterial decomposition of odorous
compounds in swine manure by some specific bacterial species. Ohta and Ikeda (1978) conducted a laboratory study regarding the possibility of deodorizing
pig feces by Streptomyces, which is a genera belonging to a group of microbes encompassing a wide
range of bacteria called Actinomycetes. They found
that the optimum conditions for deodorization were as
follows: pH, 8.6–10; temperature, 35–40◦C; moisture
content, 42–63%; and minimum amount of inoculum,
2 g of seed culture per 10 g of fresh feces. No aeration
was introduced to the testing manure but the inoculated manure was incubated aerobically. Under these
conditions, they reported that two bacterial genera
(Streptomyces griseus and Streptomyces antibioticus)
demonstrated strong ability of deodorization. Volatile
fatty acids with a carbon number up to six were
greatly reduced after 48-h treatment and the reduction
of specific malodors of the feces was observed.
Bourque et al. (1987) conducted research on microbiological degradation of odorous substances of
swine manure on a laboratory scale under aerobic
conditions. The bacterial culture under study was inoculated into sterilized swine manure and incubated
for a maximum of six days at 29◦C. They found that
three bacterial species (Acinetobacter calcoaceticus,
Alcaligenes faecalis, and Arthrobacter flavescens)
could completely degrade all types of VFAs in swine
manure while Corynebacterium glutamicum and Micrococcus sp. could only degrade acetic and propionic acids. Another laboratory experiment done by
Jolicoeur and Morin (1987) also reported that Acinetobacter calcoaceticus could degrade VFAs in both
sterilized and non-sterilized swine slurry incubated at
22◦C within pH 6.2–8.6 for 21 days.
According to Grubbs (1979), the key in using bacterial cultures for deodorization of manure is to have the
added bacteria become the predominant strain in the
manure. For the added bacteria to flourish, the real environment should not deviate tremendously from the
optimum growth range for the bacteria. Past work was
mainly focused on determining the bacterial functions
in digesting odorous compounds under optimum conditions. This usually does not guarantee that bacteria
growing well under optimum conditions will also grow
well in the field. Bourque et al. (1987) showed that
none of the inoculated microorganisms became dominant in the non-sterilized swine manure samples. The
indigenous flora (not necessarily those reducing odors)
of the wastes always grew better than the inoculated
microorganisms. In addition, the selected microorganisms may even use other organic compounds in preference to the malodorous substances when inoculated
in wastes. This impairs the values of the additives accordingly. Goldstein et al. (1985) explained possible
failure of inoculation to enhance biodegradation.
The temperature and pH of the stored manure may
not favor the growth of the added bacteria. The mean
temperature of stored slurry ranged between 3 and
22◦C (Patni and Jui, 1985) while the temperatures used
in laboratory studies ranged from 22 to 40◦C. In addition, most of the tests were run under pH condition
higher than that of manure (6.3–7.7). Although bacteria can adapt to environmental changes, large deviations from their optimum growth conditions undoubtedly interfere with normal metabolic activities, this
results in a slow growth. The evaluation of a commercial product containing enzymes and selected bacteria
showed no acceleration of degradation of the malodorous substances even at 15◦C (Bourque et al., 1987).
Since predominance of the added bacteria is critical to the treatment, the quantity of bacterial material
is questionable. Usually, the indigenous microorganisms are present in high concentration and are able to
grow rapidly. Therefore, massive inoculation has to be
exercised to accelerate the development of the added
bacteria. Such massive inoculation can be achieved
only on a laboratory scale, not at the farm level where
the volumes of manure to be treated are considerable.
According to Ohta and Ikeda (1978), 2 g of bacterial
culture seed was needed to treat 10 g of fresh swine
feces. Another study (Zhu et al., 1996) also showed
that a dose of ca. 4.5 kg of bacterial material was consumed for odor control for each pig marketed. Obviously, these numbers are not realistic in dealing with
odor problems at the farm level.
One point that needs to be mentioned here is the feasibility of using microbial additives for odor control.
As can be seen, the majority of the bacterial genera
104 J. Zhu / Agriculture, Ecosystems and Environment 78 (2000) 93–106
discussed above are obligate aerobes while most of the
storage lagoons or earthen basins (despite that some
of them are claimed as aerobic) are actually anaerobic.
As a result, the supplemental bacteria culture in such
manure handling systems will die shortly after inoculation and will never achieve dominant level because
of the lack of oxygen. This may explain the reason
that the success of using microbial additives to control
odor has been relatively limited as indicated by Ritter
(1981).
It appears that the available techniques for controlling odors are either costly (aeration) or ineffective
(anaerobic lagoon and biological manure additives).
The combination of aeration and microbial additives
is usually more expensive than aeration alone unless
the added bacteria are able to significantly reduce the
aeration time to reach dominant levels. Without aeration, the possibility of controlling odor by any of
the microbial-based manure additives that have been
developed so far is questionable.
4. Summary and conclusion
1. To quantify the microbial production of odors
by the bacterial genera indigenous to swine manure, a complete profile of bacterial species for
all the genera found in the manure is needed.
According to the discussions in the paper, the
odorous volatile fatty acids are mainly produced
under anaerobic manure storage conditions by
bacterial genera Peptostreptococcus, Propionibacterium, Bacteroides, Eubacterium, Clostridium, and Megasphaera, with genera Clostridium
and Eubacterium being most likely the major
contributors. More research is necessary to determine the species within each genus as well as the
capability of producing odorous compounds by
each individual species.
2. Raising manure pH can attenuate the growth of the
odor-causing bacteria, thus reducing odor emission. However, caution has to be exercised in treating aged manure to avoid any potential losses in
lives and properties due to the emission of large
quantities of either ammonia or hydrogen sulfide.
The adjustment of pH to fresh manure is therefore
recommended.
3. Raising temperature can enhance methanogenic
process such that odor can be reduced; however,
as compared with the adjustment of pH, raising
temperature is less feasible in the real world.
4. Anaerobic lagoons may not be an appropriate
treatment for odor control because the low temperature makes methanogens unable to function
properly, resulting in malodors due to the accumulation of volatile fatty acids.
5. Controlling odors by microbial manure additives
alone needs to be restudied. At this stage, it is actually questionable for any of the microbial-based
manure additives to control odors without aeration
in the manure storage systems currently in use.
6. Due to the complex nature of bacterial involvement in swine manure odor production, research
regarding how to control malodors microbiologically is still in its infancy. Since the source of the
odorous compounds is mainly microbial in origin,
a sustained, rational research initiative is required
using well-developed classical anaerobic microbiology technology, combined with modern molecular techniques and the latest analytical/sensory
methodology, to determine the fundamentals controlling the production of malodor.
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