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 af-
fects 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 reg- ulate bacterial growth by adjusting the pH in manure
liquid. This can be achieved more easily than control- ling 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 mech-
anism of reducing odor by alkaline materials is due to the precipitation of volatile fatty acids by forma-
tion of salts. At high levels of pH, the formed salts will not be converted back to acids; thus, both the lev-
els 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 po- tential 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. Other-
wise, 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 tech- niques 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 de- odorants are not addressed here.
3.1. Aeration The value of aeration in reducing offensive odors
has been demonstrated by a number of workers us- ing 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 oxy- gen to aerobic bacteria so they can actively decompose
the odorous compounds; hence achieving odor reduc- tion. 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. Ac- cording to these studies, a group of microorganisms
called ‘heterotrophs’ are commonly assumed to be the most numerous and important in this biological treat-
ment process. However, a complete profile of the bac- terial 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 re- ceived specific attention since most of the papers re-
lated 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 ef-
ficiency 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 aero- bic bacterial species could effectively degrade VFAs
at raised temperatures Bourque et al., 1987; Jolicoeur and Morin, 1987. Therefore, it may not be the aera-
tor that worked better at raised temperatures. It could be the microbes that enhanced their metabolic pro-
cesses in decomposing organic materials at high tem- peratures. 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 ex- isting aerobic bacteria are able to compete for nutrients
actively, to establish their growth firmly, and to reach dominant levels rapidly becomes critical. And the as-
sumption 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 gen-
eral, the microbial species having the fastest growth rate and the ability to utilize most of the available or-
ganic matter will be the predominant species Loehr, 1974. Since the tolerance of different bacterial gen-
era 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, re-
search 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 gen- era 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 mi-
croorganisms are used under anaerobic conditions to convert biodegradable organic materials to odorless
gases, such as methane and carbon dioxide, and non- biodegradable solids. There are basically three steps
involved in the process, i.e., hydrolysis, acidogene- sis, 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 re- sponsible 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 di-
gesters 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 anaer- obic 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. Un- fortunately, 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 ecosys- tem are methane and carbon dioxide. However, little
or a relatively low methane formation was observed in the anaerobic storage system Stevens and Corn-
forth, 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 temper-
ature 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 Geor- gia. 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 m
3
m
2
-day for a mean lagoon temperature of 14
◦
C and 0.55 m
3
m
2
-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 overload-
ing. Stevens and Schulte 1979 found that low tem- perature digestion 25
◦
C required a solids retention time approximately twice as long to achieve the same
volatile solids reduction as in the mesophilic diges- tion. 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, over- loading has become a major problem for the anaerobic
lagoon systems currently used in the middle and south- ern 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 offen-
sive 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 ma- nure additives for odor control partially could be due
to the complexity of odorous components in swine manure; however, the key hindrance to the develop-
ment of effective manure additive products rests with a lack of understanding of the biological activities oc-
curring in the stored swine manure. The wildly used, trial-and-error based, methods to evaluate manure ad-
ditive products are not only time consuming but also, in most cases, provide little information on the mecha-
nisms involved. Thus, in order to develop effective ad- ditive 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 Bar- rington 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 bacte- rial species. Ohta and Ikeda 1978 conducted a lab-
oratory study regarding the possibility of deodorizing pig feces by Streptomyces, which is a genera be-
longing 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 inocu-
lated 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 mi- crobiological degradation of odorous substances of
swine manure on a laboratory scale under aerobic conditions. The bacterial culture under study was in-
oculated 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 Mi- crococcus sp. could only degrade acetic and propi-
onic acids. Another laboratory experiment done by Jolicoeur and Morin 1987 also reported that Acine-
tobacter 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 bacte-
rial 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 en- vironment 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 con- ditions. 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 domi- nant 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 microorgan- isms may even use other organic compounds in pref-
erence to the malodorous substances when inoculated in wastes. This impairs the values of the additives ac-
cordingly. 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 ad- dition, most of the tests were run under pH condition
higher than that of manure 6.3–7.7. Although bacte- ria can adapt to environmental changes, large devia-
tions from their optimum growth conditions undoubt- edly interfere with normal metabolic activities, this
results in a slow growth. The evaluation of a commer- cial product containing enzymes and selected bacteria
showed no acceleration of degradation of the malodor- ous substances even at 15
◦
C Bourque et al., 1987. Since predominance of the added bacteria is criti-
cal to the treatment, the quantity of bacterial material is questionable. Usually, the indigenous microorgan-
isms 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 con-
sumed for odor control for each pig marketed. Obvi- ously, these numbers are not realistic in dealing with
odor problems at the farm level.
One point that needs to be mentioned here is the fea- sibility 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 inocu- lation 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 control- ling 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 aer- ation, 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
