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Weed seed survival during anaerobic digestion in biogas plants.

Introduction

General

Anaerobic digestion of animal manure, organic waste and crop biomass is used for biogas production as a sustainable alternative to fossil fuels, as a more efficient way of disposing of waste products, as a sludge reducing procedure, and as an odour-less alternative to composting. Various European governments provide financial and legislative incentives to biogas production. This has resulted in Germany, for example, in some 7,000 biogas plants, processing tons of manure, and some five mega tons of maize biomass per year (http://www.biogasportal.info/). The biogas produced is sufficient to satisfy 5.5 % of the current demand for electricity in Germany (http:// www.erneuerbare-energien.de/). These numbers are expected to rise in the future.

The sludge or digestate, the semi-solid leftover after anaerobic digestion, has several advantages as a crop fertilizer compared to animal slurry; a lower C/N ratio, higher concentrations of K, P and N, and a better availability of the latter, as N[H.sub.4], increased pH, improved fluidity, and reduced odour emissions (Arthurson, 2009). However, the ingredients for biogas production, namely manure, organic wastes and crop biomass, can be contaminated with pests and diseases, and, if they survive the process of anaerobic digestion, the use of contaminated sludge as a crop fertilizer could constitute a threat to the health of humans, animals and plants alike. Known human and veterinary pathogens and parasites commonly found in animal manures, biological and household wastes, and sewage and sewage sludge are listed, for example, in Bendixen (1994); Deportes et al. (1995); Colleran (2000), or Martens and Bohm (2001). Little is known with regard to the phytosanitary risks associated with the presence and survival of weed seeds.

In Germany, most anaerobic digesters are located on-farm and operated by the same farmers that produce the manure or biomass. In contrast, in Denmark, centralised anaerobic digesters exist, which process manure and other feedstocks from 60 to 80 farms per plant (Colleran, 2000). The digestate can be used either on-farm or sold and used elsewhere. In the latter case, the sludge can serve as a vehicle for the spread of pests and diseases. The likelihood of spread will be highest for common organisms, as these have the highest probability to enter the anaerobic digestion cycle, and organisms resistant to the adverse conditions in anaerobic digesters.

Because it is impossible to test the fate of all (micro-)organisms in anaerobic digesters, testing is usually restricted to a limited sets of organisms, the so-called indicator organisms (Colleran, 2000; Sahlstrom, 2003). These include organisms that are prescribed by national authorities for the sanitation of biosolids or biowaste, e.g., Ascaris suum and poliovirus 1 (PVS-1)(USA; U.S. Environmental Protection Agency, 2003), tobacco mosaic virus, Plasmodiophora brassicae, and tomato seeds (Germany; Bundesministerium fur Umwelt, Naturschutz und Reaktorsicherheit, 1998, BioAbfV), Streptococcus feacalis (Denmark; Bendixen, 1994), Clostridium perfringens, Salmonella spp., and a member of the Enterobacteriaceae, e.g., Escherichia coli (EU; The European parliament and council, 2002. Regulation (EC) No. 1774/2002 and supplement No. 208/2006). The emphasis in legislation is on limiting veterinary and human health risks; phytosanitary risks have been less of a priority, except in Germany, where indicators for plant pathogens are explicitly included in the BioAbfV regulation. The use of an indicator species is based on the assumption that "it can be reliably used to evaluate the hygienisation efficiency of the anaerobic treatment process" (Colleran, 2000), meaning that other organisms will be inactivated as efficiently as or more efficiently than the indicator species. The advantage is that the hygienisation efficiency of installations and processes can be compared. A disadvantage is that organisms that are more resistant to anaerobic digestion than the indicator species may survive and spread.

The speed of reduction in biogas reactors is usually expressed as the decimal reduction time, [D.sub.x] (Lewis, 1956), which is the time required at temperature x to kill 90 % (one log-unit) of the organisms being studied. In general, bacterial spores (e.g., [D.sub.35]=[D.sub.53][greater than or equal to]28 day, Olsen & Larsen, 1987) tend to be more resistant to anaerobic digestion than fungi (e.g., [D.sub.37]=0.8-10 day, [D.sub.55]=0.02->30 day, Schniirer & Schniirer, 2006), which, in turn, tend to be more resistant than viruses (e.g., [D.sub.35]=0.2-2.3 day, [D.sub.55]=0.01-1.5 day; Lund et al., 1996), vegetative bacteria (e.g., [D.sub.35]=0.9-7.1 day, [D.sub.53]=0.3-1.2 h; Olsen & Larsen, 1987), helminth cysts ([D.sub.35]=0.4 day; Turner et al., 1983), ova and larvae (e.g., full inactivation at 35[degrees]C in <1 day and at 53[degrees]C in 0.04-0.2 day, Olsen et al., 1985). However, there are always some that are more resistant than others, such as, for example, thermoresistant fungi (Schnurer & Schnurer, 2006). Decimal reduction times for weed seeds tend to be comparable to those of fungi (e.g., [D.sub.41]=0.8-19.7; Westerman et al., 2012b).

Risks Associated with Sludge Contaminated with Weed Seeds

In the case of weeds, no indicator species are routinely included in sanitation procedures, except tomato seeds, which are prescribed in the BioAbfV regulation as a proxy for weed seeds (Germany; Bundesministerium fur Umwelt, Naturschutz und Reaktorsicherheit, 1998, BioAbfV). Seeds are a logical choice, because they are the most likely structure to survive anaerobic digestion. Seeds tend to be well-protected by seed coat and other protective structures, they usually have a low metabolic rate and dormancy mechanisms that prevent germination, and they are known to be able to endure and survive adverse environmental conditions. However, weed species differ considerably in seed characteristics, and are, therefore, expected to differ in survival probability during anaerobic digestion. Systematic research on the ability of weeds from different taxonomic and functional groups to survive anaerobic digestion is lacking, and it is, therefore, difficult to say how well tomato represents weeds.

Weed seeds can enter the biogas chain either via crop biomass or via animal manure. In maize, the most common feedstock in Germany, 180 species of weeds have been recorded (Mehrtens et al., 2005). The most frequently encountered weed species were: Chenopodium spp. (79.7 % of the fields), Stellaria media (61.0 %), Fallopia convolvulus (55.7 %), Echinochloa crus-galli (53.0 %), Matricaria spp. (50.3 %), Viola arvensis (47.8 %), Polygonum aviculare (45.8 %), Lamium spp. (41.6 %), Galium aparine (39.7 %), Elytrigia repens (39.4 %), Solanum nigrum (36.3 %), Thlaspi arvense (34.3 %), Capsella bursa-pastoris (33.8 %), Veronica spp. (31.1%), Poa spp (27.7 %), Cirsium arvense (25.9 %), Polygonum persicaria (24.8 %), Atriplex patula (21.6 %), and Polygonum lapathifolium (20.8 %). The above percentages were related to incidences, not weed abundances. Figures for weed identity and intensity in other energy crops are lacking.

The presence of weeds in a field does not necessarily mean that the harvested biomass will contain their seeds. For example, the density of a weed could be so low that the risk of contamination of biomass during harvest is negligible. Some weed plants are physically so small that they escape the combine-harvester, such as for example S. media, Veronica spp, Vi. arvensis, Myosotis arvensis, Anagallis arvensis, or Argentina anserine (Westerman & Gerowitt, 2012). Most farmers cut maize at a height of 10 to 30 cm (Wu & Roth, 2004). Many weeds remain vegetative (e.g., Mertens, 1998) due to competition for light. Some weeds produce seeds either so early that they are all shed prior to harvest, or so late that most seeds will be immature and non-viable at harvest (e.g., Harker et al., 2003). Compared to maize grown for grain, maize for silage and biogas production is usually harvested early, giving few weeds the possibility to reproduce. In maize, the number of weed seeds in flower heads above the cutting height varied between fields from 0 to 157 000 seed [m.sup.-2] (Westerman & Gerowitt, 2012).

With regard to the probability that manure is contaminated with seeds, research on cattle and sheep manure shows that large numbers of viable seeds from different weed species can survive and be present in the manure, but density and identity vary with farm, depending on what animals had been fed (e.g., Dastgheib, 1987; Cudney et al., 1992; Mt. Pleasant & Schlather, 1994).

Risks associated with spread and infestation of weeds will be highest for invasive, quarantine and troublesome weeds that do not have a widespread distribution yet. In addition to the infestation risk associated with the use of contaminated sludge, low levels of weed survival could select for 'anaerobic-digestion-resistant' biotypes, provided that the sludge is repeatedly recycled on-farm and provided that seed survival has a genetic basis.

Scope and Aim of this Review

The purpose of this review was 1) to provide an overview of what is known with regard to weed seed survival after anaerobic digestion in biogas plants (Chapters III and IV) and 2) identify high-risk weed species, i.e., species that have a particularly high probability of surviving the conditions encountered in biogas plants.

Unfortunately, literature on these subjects was scarce and fragmentary. The literature search was furthermore hampered by a large amount of 'grey' literature, i.e., papers that are not peer-reviewed, not easily accessible, and often published in a language other than English. Despite an extensive search, the only literature describing empirical data on seed survival in anaerobic digesters consists of seven peer-reviewed publications (Jeyanayagam & Collins, 1984; Engeli et al., 1993; Sarapatka et al., 1993; Ryckeboer et al., 2002; Strauss et al., 2012 (in German); Westerman et al., 2012a, b), one article in a popular scientific journal (Schrade et al., 2003 (in German)), and six project reports (Hansen & Hansen, 1983 (in Danish); Bohm et al., 2000 (in German); Lorenz et al., 2001 (in German); Katovich et al., 2004; Marcinisyn et al., 2004 (in German); Westerik & Kleizen, 2006 (in Dutch); Leonhardt et al., 2010 (in German)). Three of these only report on the survival of tomato seeds (Bohm et al., 2000; Lorenz et al., 2001; Ryckeboer et al., 2002), and one only on the survival of crop seeds (Strauss et al., 2012).

To achieve the second goal, i.e., identify high-risk weed species, survival probabilities for a large range of weed species, involving different taxonomic or functional groups or contrasting seed characteristics, would be required, such that generalizations are possible. However, systematic research on weed seeds is lacking and most studies included no more than 5-6 weed species, which is insufficient for the purposes of this review. Mechanisms of seed inactivation can be classified as thermal, biological or chemical. However, evidence of chemical inactivation is completely lacking and is, therefore, excluded from this review. We here provided a brief background on the conditions that seeds are likely to encounter in biogas plants (Chapter III) and summarized what is known with regard to the effect of these conditions, in particular temperature and duration of exposure (Chapter V), and microbial activity (Chapter VI), on seed viability. We borrowed knowledge from related fields, such as endozoochory, weed seed banks and survival of microorganisms in biogas reactors, to complement the deficient literature. In addition, we tried to identify seed waits that might be linked to seed survival in biogas reactors (Chapter VII), such that in the future extensive testing of seeds in biogas reactors can be omitted and replaced by simple, predictive tests, based on specific seed traits.

Anaerobic Digestion

Reactor Types

Continuous Flow-Through, Stirred Tank Reactor. The conditions to which pathogens, pests and weed seeds are exposed depend on the type of reactor used and the operational settings chosen. The most commonly used type of anaerobic digester for biogas production in Germany, the country with the highest number of biogas plants in the world, is the so called single-stage, continuous flow-through, stirred tank reactor (CSTR) that uses high solids as a feedstock in wet fermentation and is operated at the mesophilic temperature range. 'Single-stage' refers to the fact that all four microbiological steps involved in digestion, namely hydrolysis, acidogenesis, acetogonesis and methanogenesis, occur simultaneously in the same reactor. Each process is conducted by a specific group of microorganisms, with its own set of requirements with regard to pH, temperature, etc. The fact that all four processes take place in the same reactor means that the prevailing conditions are a compromise that is suboptimal for all groups involved. 'Continuous flow-through' refers to the fact that the reactor is fed at the inlet with new biomass and slurry, and relieved from sludge at the outlet, continuously and simultaneously. The content of the tank is stirred continuously, using various designs of agitators (e.g., Deublein & Steinhauser, 2011), such that new feedstock is mixed in with the partially digested feedstock already present. 'Mesophilic' refers to the temperature range at which anaerobic digestion takes place, namely 20-45[degrees]C (92 % of the biogas plants in Germany), as opposed to psychrophylic (< 20[degrees]C) or thermophilic (>45[degrees]C). 'High solid, wet fermentation' refers to the fact that the concentration of total suspended solids in the liquid is >15 %; the slurry in the reactor is thick and viscous, but can still be pumped around. This type of reactor is typically fed a mixture of agricultural waste, such as animal slurry or mist (swine or cattle), in combination with agricultural raw products, such as maize, small-grain cereals, or potato- or sugar beet residues (codigestion), but the exact composition of the feed varies from reactor to reactor.

The residence time, i.e., the time that the substrate, including weed seeds, is exposed to the conditions inside anaerobic digesters, is variable. The average residence time, or hydraulic retention time (HRT), is calculated as the volume of the tank divided by the flow rate. Depending on the operational temperature, the HRT of mesophilic CSTRs is usually between 20 and 40 days, that of thermophilic CSTRs between 8 and 15 days (Deublein & Steinhauser, 2011). However, there is considerable variation in the actual residence time inside a reactor, which can be studied with the help of tracers (e.g., Monteith & Stephenson, 1981; Smith et al., 1993; Teefy, 1996). In an ideal CSTR, where mixing is perfect and instantaneous, a sudden pulse of a tracer at the inlet would cause an immediate peak followed by an exponential decline of the tracer material at the outlet. An important consequence is that a certain proportion of the tracer material will be exposed for (much) shorter or (much) longer periods of time than the HRT. However, no CSTR is perfect because of short-circuiting in the reactor, imperfect mixing, or dead space in the vessel. Deviations from the ideal CSTR affect the shape and width of the tracer curve, causing higher or lower variance around the HRT. Tracer studies, assisted by modelling, can help to characterize real reactors to optimize biogas production (e.g., Capela et al., 2009) and to predict the level of disinfection that can be achieved in water treatment facilities (e.g., Teefy, 1996). The shape and width of the tracer curve will be variable between reactors used in biogas production, as most are custom-build and unique to some degree.

Batch Reactor. Another type of reactor is the so-called 'batch' reactor. The difference with the CSTR is that it is fully loaded with organic materials, sealed, the contents are digested and the reactor unloaded. The reason that this type of reactor is mentioned here is not because it is important in commercial biogas production (e.g., approx. 5 % of the biogas plants in Germany), but because it is often used in controlled laboratory conditions as a substitute for CSTRs and easier to handle. Batch reactors differ from CSTRs in that the four steps in the microbiological conversion of organic material to biogas occur sequential, not simultaneously, causing fluctuations in pH and the concentration of intermediate substances, and that the residence time is fixed and without variance. The relationships between results obtained under laboratory conditions vs. full-scale commercial conditions, or batch vs. continuous conditions are ambiguous. For example, pathogenic bacteria were more easily reduced under laboratory conditions than in full-scale, continuous digesters (Carrington et al., 1982). Similarly, batch reactors were more effective at destroying seeds and pathogenic bacteria than CSTRs, operated at the same temperature and HRT (Jeyanayagam & Collins, 1984; Kearney et al., 1993). In contrast, Olsen and Larsen (1987) found that batch and continuous digesters were equally effective at reducing bacterial pathogens, and Westerman et al. (2012a, b) found that the ranking of weed species differed between experimental batch reactors and commercial CSTRs.

Plug-Flow Reactor. Three publications on seed survival in biogas reactors (Ryckeboer et al., 2002; Katovich et al., 2004; Mareinisyn et al., 2004) deal with a plug-flow reactor (PFR), which is a horizontal pipe or tunnel, to which substrate is added at one end and digestate is removed from the other end. A main difference with the above-mentioned types of reactors is that the substrate is stackable (dry fermentation), not liquid, and that the substrate is pushed through the PFR and not mixed. The retention time is, therefore, fixed and without variance. In this sense, processing is as in a batch loaded reactor, although the actual loading and unloading is continuous.

Gastrointestinal Tract of Animals. Because of interest in plant dispersal by animals (endozoochory), a large amount of literature is available on seed survival in the alimentary tract of animals, in particular ruminants (for overview see, for example; Bonn & Poschlod, 1998; Hogan & Phillips, 2011). The processes that take place in the gastrointestinal tract of animals bear resemblance to those in anaerobic reactors, although temperature is fixed, dependent on the body temperature of the animal species. Insights gained in one system could be used in the other. However, there are a number of differences in process characteristics and research methodology.

1) The digestion of lignocellulosics in the digestive tract of ruminants is much more effective than in anaerobic digesters (Bayane & Guiot, 2011). Lignocellulosics are the plant's main structural components, they occur in cell walls, and they are one of the main energy carriers in biomass. The biodegradability of cellulose and hemicellulose is affected by the degree of lignification (Van Soest, 1982, 1988). Lignin cannot be cleaved by hydrolytic enzymes, and thus protects cellulose and hemicellulose from hydrolysis (Hofrichter, 2002). Only a few specialized fungi and bacteria can effectively digest lignin via lignin-modifying enzymes, such as peroxidises and phenol-oxidases. Some of these occur in the digestive tract of ruminants (Trinci et al., 1994) and some other animals. Because the degradation of lignocellulose in bioreactors is slow and limited, lignin degrading enzymes and microorganisms have attracted attention because of their potential to improve biogas and biofuel production (e.g., Bayane & Guiot, 2011; Jin et al., 2011; Sanderson, 2011).

2) The residence time in ruminants is much shorter than in commercial reactor vessels. The mean retention time (MRT) ranges from 25 h in deer (Mouissie et al., 2005) to 50-63 h in cattle and sheep (Glendening & Paulsen, 1950; Simao Neto et al., 1987; Cosyns et al., 2005).

3) Anaerobic digestion in the reticulorumen (1st and 2nd chamber of the stomach) and intestine of ruminants is interrupted by acidic hydrolysis in the abomasum (4th chamber or tree stomach) with a pH of around 2. In cattle, normally only 2-4 h are spent in the strongly acidic abomasums and duodenum (first section of the small intestine) (Gardener et al., 1993b). Some found that the duration of stay and the conditions encountered in the rumen were decisive for seed survival (Simao Neto & Jones, 1987; Carpanelli et al., 2005) and that additional passage through the true stomach and intestines had little effect on seed degradation and germination. However, using a simulated (in vitro) digestive process, others found that both the rumen and the stomach negatively affected seed survival (e.g., Edwards & Younger, 2006). Pepsin incubation, as in the stomach, was very damaging to seeds and made prior rumen incubation largely irrelevant.

4) The residence time in the alimentary tract of ruminants is influenced by particle size and density. The reasons for this are a) selective filtering by the mat, a thick mass of partially degraded, fibrous material that is formed in the rumen, in combination with ruminal contractions, and b) smaller particles are better able to pass through the orifice, the opening between the reticulorumen and the abomasums, than larger particles (Poppi et al., 1985). For example, the mean retention time (MRT) was found to be approx. 20 h longer for 10 mm particles than for 1 mm particles (Kaske & van Engelhardt, 1990). The MRT was minimal for particles of 6.4 mm and longer for particles that were either shorter (3.2 mm) or longer (12.7 mm) (Ehle & Stem, 1986). The MRT in the reticulorumen was longest for particles with a density around 1.2-1.4 g.[ml.sup.-1], and shorter for both lighter and heavier particles (DesBordes & Welch, 1984; Ehle & Stem, 1986; Kaske & van Engelhardt, 1990). Differences in the fate of ingested seeds can, therefore, be caused by differences in sensitivity of weed species to anaerobic digestion as such, or by differences in the duration that particles remain in the digestive tract. Often, it is impossible to distinguish between the two causes. In CSTRs, the residence time cannot be influenced by the size, shape or density of the particles that inhabit them, because solids are carried along with liquids and the retention time of solids (SRT) is equal to that of liquids (HRT). In some type of CSTRs, however, the solid fraction is separated from the liquid fraction after outflow and re-circulated into the reactor, resulting in SRT > HRT. In that case, seeds could be processed either as the liquid or as the solid fraction. We are not aware of any literature investigating the fate of differently sized particles in such reactors.

5) Usually, only germination after passage through the gastrointestinal tract was scored and not seed viability. This means that in many studies on zoochory mortality is confounded with dormancy. Seeds that were fully digested were often ignored, making it impossible to get a pure estimate of seed mortality. In the most extreme cases, the number of seeds recovered of a particular species was not expressed as a proportion of the number of seeds that entered the animal, but as a proportion of the total number of seeds recovered from the faeces (e.g., Pakeman et al., 2002). As a consequence, differences in the availability of seeds to grazers and the probability of ingestion are ignored (for discussion see Bruun & Poschlod, 2006). The latter category of papers was, therefore, omitted from the review.

Despite the differences and recognized problems, literature on seed survival after passage through animals was included in this review, to supplement the scarce information available on seed survival in anaerobic digesters. It is clear that the outcome of animal feeding experiments should be interpreted cautiously.

Conditions During Anaerobic Digestion

In mesophilic CSTRs, weed seeds will be exposed to dark, moist, anaerobic conditions, constant temperatures that can differ between reactors from approx. 20 to 40[degrees]C, and a pH that is ideally between 6.8 and 8. Most environmental conditions will be kept within tight bounds, because deviations could disrupt biogas production. In addition to water, methane and C[O.sub.2], a wide range of substances can occur in bioreactors, including hydrolases, lipases, proteases, and other enzymes involved in decomposition, amino and organic acids, including long chain fatty acids, [H.sub.2]S, H[S.sup.-], [S.sup.-], alcohols, N[H.sub.4.sup.+]/N[H.sub.3], and cyanides. Particularly when sewage and organic household waste are used as biogas feedstock, light and heavy metal ions may be present as well as a large range of organic (micro) pollutants, including polycyclic aromatic hydrocarbons, N-substituted aromatics (e.g., nitrobenzenes, nitrophenols), chlorophenols, halogenated carbohydrates (e.g., chloroform), phytohormones and analogues, and their degradation products (e.g., Deportes et al., 1995; McGrath, 1999; Langenkamp et al., 2001). These substances have been studied because they are important intermediates in the process of biogas production, because of negative side-effects, such as disruption of biogas production (Chen et al., 2008) and odour nuisance (Hansen et al., 2004), or because of a reduction in the quality of the digestate as a crop fertilizer (Lukehurst et al., 2010).

As soon as seeds and other biomass enter the liquid medium of CSTRs, their surfaces will be colonized by microorganisms, such as bacteria, archaea, and protists. They form a biofilm, a coordinated functional community that is much more efficient than a mixed population of floating organisms (Costerton et al., 1995). Biofilm microorganisms produce and maintain spatial and temporal gradients of pH, metabolites, etc., which allow the coexistence with specialized and fastidious species, such as methanogenic bacteria (Costerton et al., 1995 and references therein). Once established, associations between microorganisms and surfaces are often difficult to disrupt physically or chemically.

The conversion of biomass to biogas develops via four microbiological steps, each involving a specific group of microorganisms. During hydrolysis, microorganisms break down the insoluble organic polymers, such as proteins, lipids and carbohydrates, into amino acids, fatty acids and sugars. The acidogenics, in particular members of the genera Clostridium, Paenibacillus, and Ruminococcus, convert the amino acids, fatty acids and sugars into carbonic acids, alcohols, hydrogen, carbon dioxide and ammonia (acidogenesis). Next, acetogenics and sulphate-reducing bacteria convert the organic acids into acetic acid, hydrogen, and carbon dioxide (acetogenesis), and, finally, methanogenics, in particular those belonging to the Methanosaeta, the genera Methanobacterium and Methanosarcina, and the species Methanospirillum hungatii convert the hydrogen, acetic acid and carbon dioxide into methane and carbon dioxide. For a short overview of the chemical pathways and the microorganisms involved the various steps in anaerobic digestion, we refer to Deublein and Steinhauser (2011).

Up- and Downstream Processes

Anaerobic digestion is not a stand-alone process. Biomass, including weed seeds, will run through a series of events before (upstream processes) and after (downstream processes) anaerobic digestion. These processes will affect weed seeds as well.

Upstream. Weed seeds will enter biogas plants either via animal manure or via biomass. In the former case, seeds must pass through the gastrointestinal tract of animals, usually pigs or cattle. At one time, these seeds had been fed to the animals either as fresh (grazing), dried (hay), or ensiled material. In the latter case, seeds were freshly harvested together with maize or other feedstock, or they had been stored in silage. Both the alimentary tract of animals and silage are hostile environments to seeds (Blackshaw & Rode, 1991; Westerman et al., 2012a). Anaerobic digesters are often preceded by grinders or cutters for reducing the size of biomass particles and mixers for homogenizing water, manure and biomass. Mechanical damage to seeds prior to exposure to anaerobic digestion is possible. In several countries, anaerobic digestion has to be preceded by a pasteurization step, which usually involves treatment of animal manure and other organic wastes in a (aerobic) sanitation tank at 70[degrees]C for at least 1 h (Bendixen, 1994; Colleran, 2000; Sahlstrom, 2003). Chemical sanitation is also possible and involves enhancing the pH to above 8 by the addition of large quantities of calcium hydroxide (lime) (Haas et al., 1995; Deublein & Steinhauser, 2011). High pH and the presence of ammonia (N[H.sub.3]), which is made available at pH>8, are effective biocides, particularly against viruses. High temperatures, high pH and ammonia are likely to influence seed viability. Consequently, the probability that undamaged, highly vital and vigorous weed seeds will enter the biogas reactors directly is low. Most experiments in anaerobic digesters, however, use newly produced or laboratory stored seeds and single out anaerobic digestion as such. This is likely to cause overestimation of seed survival over the entire chain.

Downstream. Usually, the output from anaerobic digesters is stored in a basin until further use. Either aerobic or anaerobic digestion will continue, causing additional seed mortality (Strauss et al., 2012). In addition, post-sanitation may take place, as an alternative to pre-sanitation, involving thermal hygienisation, exposing seeds to the same kind of stress as described for upstream hygienisation (Strauss et al., 2012).

Seed Viability as Affected by Anaerobic Digestion

In Biogas Plants

In anaerobic digesters, the viability of seed declines exponentially over time (Jeyanayagam & Collins, 1984; Schrade et al., 2003; Westerik & Kleizen, 2006; Leonhardt et al., 2010; Strauss et al., 2012; Westerman et al., 2012b), in a similar way as the exponential inactivation of bacterial, fungal and viral pathogens. The exponential inactivation of seeds tends to be preceded by a lag phase, indicating that seeds are initially unaffected by anaerobic digestion. Temperature was found to be the most important factor influencing seed survival; lag phase was shorter and decline faster with increasing temperatures. For example, in experimental CSTRs at approximately 54[degrees]C, eight species of seeds were killed within 24 h, while 3 days were required to inactive four out of eight species at 36[degrees]C (Schrade et al., 2003; Table 1). Similarly, ten species of weed seeds were inactivated within 1 day in a batch loaded reactor at 50[degrees]C, whereas at least 3 day were required to inactivate seven out often weed species at 35[degrees]C (Leonhardt et al., 2010; Table 1). Temperature was also found to be the most important factor influencing survival of pathogenic bacteria (Olsen & Larsen, 1987; Dumontet et al., 1999), fungi (Schnurer & Schnurer, 2006), and viruses (Lund et al., 1996). Not only seed viability was affected, but also seed vigour. The speed of germination of surviving seeds decreased with increasing exposure time to anaerobic digestion in experimental batch loaded reactors (Westerik & Kleizen, 2006). By physically separating hydrolysis from the other three steps in the anaerobic digestion process (two stage digester), Engeli et al. (1993) showed that most seeds were inactivated during hydrolysis, the first step in anaerobic digestion.

Some species survived for appreciably longer periods inside biogas reactors than others, in particular under mesophilic conditions (Table 1). For example, tomato seeds proved to be more resistant to mesophilic digestion than most other species (Westerik & Kleizen, 2006; Strauss et al., 2012; Table 1), leading to the opinion that tomato would make an appropriate indicator for sanitation. However, Schrade et al. (2003) and Westerman et al. (2012a, b) found that some species survived much better than did tomato. Frequently, the same species were included in studies and, therefore, the same species tend to surface as being resistant to mesophilic anaerobic digestion; Abutilon theophrasti, C. album and Amaranthus retroflexus at approximately 37[degrees]C (Katovich et al., 2004); C. album, A. retroflexus, At. patula, E. crus-galli, P. lapathifolium, and Rumex obtusifolius at 35[degrees]C (Leonhardt et al., 2010); Amaranthus retroflexus, C. album, E. crus-galli and R. obtusifolius at approximately 30[degrees]C (Sarapatka et al., 1993); C. album and R. obtusifolius at approximately 36[degrees]C (Schrade et al., 2003); flax; mustard and oilseed rape at 38[degrees]C (Strauss et al., 2012), and A. theophrasti, Datura stramonium, Erodium cicuratium, Malva neglecta and Vicia tetrasperma at 37[degrees]C (Westerman et al., 2012a).

Differences between species were also found under thermophilic conditions. Polygonum lapathifolium (59 %), C. album (57 %), Amaranthus sp. (23 %) and E. crus-galli (1%) survived 3 day at 45[degrees]C, in contrast to six other species (Leonhardt et al., 2010). Tomato and Urtica urens required 24 h at 51[degrees]C to be fully inactivated, in contrast to four other species that were inactivate much faster (Westerik & Kleizen, 2006; Table 1).

Ranking of species differed between studies. For example, survival of P. lapathifolium was lowest in the study by Sarapatka et al. (1993) and one of the highest in the study by Leonhardt et al. (2010); survival of E. crus-galli was higher than that of C. album in the study by Sarapatka et al. (1993), but lower in the study by Leonhardt et al. (2010). Either the initial seed quality or the conditions inside reactors must have varied between studies. Furthermore, ranking of species may change with exposure time due to differences in the shape of the seed survival curves (Jeyanayagam & Collins, 1984; Leonhardt et al., 2010; Strauss et al., 2012; Westerman et al., 2012b).

In the Digestive Tract of Animals

As in biogas reactors, seed viability decreased exponentially over time after an initial lag phase, in the digestive tract of ruminants (Alomar et al., 1994; Alomar & Ulloa, 1994; Fredrickson et al., 1997; Gokbulak, 2002). The same was observed when seeds were exposed to the (simulated) rumen alone (Simao Neto & Jones, 1987; Blackshaw & Rode, 1991; Alomar et al., 1992; Fredrickson et al., 1997; Edwards & Younger, 2006), or (simulated) stomach alone (Edwards & Younger, 2006). Both the length of the lag phase and the rate of decrease differ between species (Blackshaw & Rode, 1991). For example, Bromus tectorum remained fully viable for up to approx. 10 h in the rumen of cattle, after which viability decreased rapidly to almost zero. In contrast, viability of F. convolvulus decreased gradually over time, with no noticeable lag time (Blackshaw & Rode, 1991). Ranking of species, therefore, depends on the exposure time, similar to the situation in biogas reactors. Seed vigour, estimated as the speed of germination, is also affected by (simulated) digestion in animals (e.g., Peco et al., 2006), as in anaerobic digesters.

D'hondt and Hoffmann (2011) compared the germination success of seeds of 48 grassland species after passage through cattle. Included were 12 species that may occur as weeds in maize in Germany (Mehrtens et al., 2005). The best germinating weeds were Trifolium pratense (100 %), Juncus bufonis (83 %), Agrostis stolonifera (35 %), Plantago lanceolata (32 %), Poa annua (25 %), R. obtusifolius and C. album (both 21%). Similarly, Cosyns et al. (2005) compared the germination success of seeds of 19 grassland species after passage through rabbit, cattle, sheep, donkey and horse. Included were six species that may occur as weeds in maize in Germany. Ranking of species in order of decreasing germination success was as follows; Trifolium arvensis, P lanceolata, Prunella vulgaris, V. arvensis, T. repens, and T. pratense.

Studies in which seeds were exposed to ruminal conditions under more controlled conditions and for known periods of time, i.e., via fistulated animals or an artificial rumen (e.g., Rusitec; Czerkawski & Breckenridge, 1977), may yield relationships that are more valuable for predicting seed survival in biogas reactors. Although such studies do exist, they tend to investigate the process of ruminal digestion, such as speed of inactivation and mortality curves of individual species (e.g., Fredrickson et al., 1997; Alomar et al., 1992), and do not compare the survival probabilities of a range of weed species, with one exception. In a study with 12 weed species, seeds that survived exposure to fistulated cows for 24 h particularly included; T. arvense (68 %), Malva pusilla (57 %), E convolvulus (56 %), C. album (52 %) and A. retroflexus (45 %) (Blackshaw & Rode, 1991).

Thermoresistanee

Temperature was found to be the most important factor influencing seed survival in biogas reactors. With increasing temperatures, the lag phase of the survival curve decreased and the rate of decline increased. Thermoresistance depends very much on the moisture contents (mc) of the seeds. First, the available knowledge with regard to the response of seeds to temperature as a function of moisture contents will be summarized, before proceeding to thermoresistance in biogas reactors. Knowledge on this subject is fundamental in understanding the mechanism of inactivation of seeds in the hot and moist environments of biogas reactors, and in understanding deviations from the expected patterns.

Response to Temperature Depending on Seed Moisture Content

The thermoresistance of seeds can be divided into four categories, based on the survival characteristics as influenced by seed moisture contents and temperature; 1) low seed mc, low and medium T, 2) medium seed mc, high T, 3) high seed mc, medium T, and 4) high seed me, high T.

Ad I. Dry Seeds at Low and Medium Temperatures. There is a lot of knowledge available regarding the longevity of very dry (mc [much less than] 15 %), orthodox seeds, at low and medium temperatures (T<30[degrees]C). Almost all arable weed species belong to the category of orthodox (=desiccation tolerant) seeds. Seed mortality decreases exponentially with decreasing temperatures and moisture contents. This means that seeds can survive for extended periods of time at low T and low me. Research on the survival of dry seeds has been motivated by the need to define optimal conditions for maintaining seed viability for a long period of time for seeding purposes and storage of genetic material in gene banks. This knowledge has culminated in the development of the so-called seed viability equation (Ellis & Roberts, 1980; Pritchard & Dickie, 2003), whose parameters are constant for a given seed species at a given temperature and moisture content, making seed longevity predictable. The seed viability equation fails completely in fully imbibed (me>20 %), but not in partially imbibed seeds (mc=15-20 %, see ad 2).

Ad 2. Moist Seeds at High Temperatures. Seeds with medium seed moisture contents (mc=15-20 %) age very quickly when exposed to high temperatures (T=40-45[degrees]C). This fact has found application in three areas, namely procedures to estimate the parameters of the seed viability equation to predict storage behaviour at low mc and low temperatures (accelerated ageing test), procedures to predict and compare 'vigour' or 'quality' of seed lots (controlled deterioration test (CDT)(Powell & Matthews, 1981) or controlled ageing test (CAT)(Delouche & Baskin, 1973)), and research with regard to mechanisms involved in the deterioration of seeds, i.e., the loss of membrane integrity, impairment of RNA and protein synthesis and DNA degradation, caused by the accumulation of reactive oxygen species (ROS) and lipid peroxidation (e.g., Walters, 1998; Bailly et al., 2008; Lehner et al., 2008).

Ad 3. Fully Imbibed Seeds at Medium Temperatures. In contrast to partially imbibed seeds, fully imbibed seeds (mc>20 %) can survive for extended periods of time as long as temperatures are not too high (T=20-35[degrees]C), and provided that they do not germinate or rot (e.g., Villiers, 1974; Murdoch & Ellis, 2000). Under anaerobic conditions, the deterioration of seeds is merely halted (Ibrahim & Roberts, 1983), but under aerobic conditions, the process of seed deterioration is reversed and longevity is restored to some extent (Ibrahim et al., 1983). This improvement seems to be caused by metabolic repair of previously sustained damage (Powell et al., 2000). It is not necessary for seeds to be continuously imbibed; even a short period of imbibition can improve seed longevity (Villiers & Edgecumbe, 1975). This principle has found application in seed priming and other seed invigoration treatments to improve, synchronize and speed up germination and emergence (e.g., Powell et al., 2000).

Ad 4. Fully Imbibed Seeds at High Temperatures. At higher temperatures (T>35[degrees]C) the viability of fully imbibed seeds declines exponentially over time (Economou et al., 1998, Dahlquist et al., 2007). Thermal death models have been fitted, using exponential or other non-linear models, to describe mortality of imbibed seeds over time. These models allow the prediction of the duration of exposure at a given temperature to cause 100 % mortality, or, alternatively, the temperature required to cause 100 % mortality at a given exposure time (thermal death point), and are used to assist weed control via soil solarisation and steaming (Horowitz & Taylorson, 1983; Egley, 1990; Economou et al., 1998; Thompson et al., 1997a; Dahlquist et al., 2007). In general, the higher the temperature the shorter the period of time required to reach the thermal death point.

At the thermophilie range, loss of viability of imbibed seeds is quick. Depending on the species, 15-312 h at 46[degrees]C, 4-113 h at 50[degrees]C, 0.25-3 h at 60[degrees]C and 0.17-0.67 h at 70[degrees]C were sufficient to kill 100 % (Dahlquist et al., 2007). About 800 h were required to inactivate Avena sterilis at 38[degrees]C, 450 h at 39[degrees]C, 300 h at 40[degrees]C and less than 50 h at 45[degrees]C (Eeonomou et al., 1998). One day at 55 or 65[degrees]C was sufficient to kill all seeds of six weed species; 2 day were required to inactivate two out of six species at 45[degrees]C and 5 day at 45[degrees]C for another species; three species were not inactivated within 9 day at 45[degrees]C (Nishida et al., 2002). Loss of viability is slower at the mesophilic range. Seed viability was unaffected at 39[degrees]C, and that of three of the six species tested was unaffected at 42[degrees]C (up to 28 day exposure). For the remaining three species, 4-16 day was required to cause 100 % mortality (Dahlquist et al., 2007). Similarly, seed viability was unaffected for five out of six species at 35[degrees]C (Nishida et al., 2002).

Differences in Thermoresistance between Weed Species

The imbibed seeds of some species are more sensitive to exposure to hot water or hot moist soil than others. Thermal death models indicate that both the lag phase and the speed of decline may vary between species (Economou et al., 1998; Dahlquist et al., 2007). Summarizing seven studies on the effects of soil solarisation, Elmore (1991) concluded that, in general, summer annuals tended to be more thermoresistant than winter annuals. Senecio vulgaris was among the least, and Melilotus sp. and Medicago sp. among the most thermoresistant species (Elmore, 1991).

Ranking of six weed species in order of decreasing thermoresistance in the study by Nishida et al. (2002) was as follows; Amaranthus spinosus, Solanum carolinense, A. patula, S. americanum, Phytolacca americana, A. theophrasti. Based on the period required to kill 100 % of the seeds at 50[degrees]C ranking of six species was as follows; Amaranthus albus (113 h), S. nigrum (71 h), Portulaca oleracea (56 h), E. crus-galli (9 h), Sisymbrium irio (6 h), Sonchus oleraceus (4 h) (Dahlquist et al., 2007). All seeds of R. obtusifolius were inactivated by ten minutes in water at 70[degrees]C, but 15 % of the seeds of A. fatue were still viable at this temperature; tomato and P persicaria were inactivated by 10 min at 65[degrees]C; T. maritima and Anthemis arvensis were inactivated by 10 min at 60[degrees]C (Lorenz et al., 2001). Xanthium strumarium seeds were fully inactivated after 6 h in moist soil at 60[degrees]C, or 3 day at 50[degrees]C, Sida spinosa required 1 day to be inactivated at 60[degrees]C and 6 h at 70 h, A. theophrasti required 1 day at 70[degrees]C, Sorghum halepense 2 day, Anoda cristata 5 day and P. oleracea 7 day at 70[degrees]C to be fully inactivated (Egley, 1990). Seeds of A. retroflexus needed either temperatures >70[degrees]C or exposure periods >7 day to be fully inactivated. Seven days exposure to moist soil at 40[degrees]C had no effect on any of the eight species (Egley, 1990).

In anaerobic digesters, the temperature is 20[degrees]C or higher and seeds should be fully imbibed, corresponding to the situation as described under ad 4. Exposure of seeds to hot water baths could, therefore, be used as a first screen to determine the minimum percentage of mortality that can be expected and to identify potentially thermoresistant weed species, i.e., species whose seeds might be able to withstand the thermal conditions in anaerobic digestion for a longer period of time. This method was employed by Lorenz et al. (2001) and Bohm et al. (2000), but unfortunately not verified in biogas reactors. Results by Dahlquist et al. (2007) and others make clear that, at least within the mesophilic temperature range, the inactivation of seeds in biogas reactors cannot solely be due to high temperatures. This means that exposure of seeds to hot water or moist soil could (strongly) underestimate seed mortality in biogas reactors. For example, seed viability was unaffected by exposure to 39[degrees]C in water baths (Dahlquist et al., 2007), while most seeds in anaerobic digesters died within 3 day at 35[degrees]C. The fact that high temperatures alone cannot fully explain the demise of seeds during anaerobic digestion also means that additional mortality factors have to be involved.

Mechanisms and Compounds that modify the Effects of High Temperatures

Similar as with seeds, high temperatures could not fully explain the demise of pathogenic bacteria, viruses or helminths during anaerobic digestion (Berg & Berman, 1980; Olsen & Larsen, 1987; Sahlstrom, 2003; Popat et al., 2010). As an explanation for the higher than expected decimation rates, the involvement of substances with bactericidal or virucidal activity, such as ammonia (Ward, 1978) or long chain fatty acids, was put forward (for review see: Sahlstrom, 2003). In the case of bacteria, competition for limiting supplies of nutrients could be involved.

Interestingly, certain substances and mechanisms occurring in biogas reactors seem to be able to protect bacteria and viruses from thermal inactivation. The resulting decimation rates are then lower than expected on the basis of thermal inactivation alone. Substances and mechanisms involved include, for example, certain anionic detergents, food additives and amino acids (Popat et al., 2010), adhesion to suspended solids (Bar-Or, 1990) or embedding of virus particles and clumps of bacterial cells in viscous envelops (Rollins & Colwell, 1986; Lund et al., 1996).

It is unknown if substances with herbicidal activity or seed protective properties could occur in biogas reactors, and if these could be responsible for the higher or lower than expected decimation rates based on thermal inactivation alone. Certain amounts of chemical herbicides may enter via the biomass feedstock, allelochemicals may be present in crop residues, such as in wheat straw, bacterial phytotoxins may be present in anaerobic digesters, as well as phytohormones, such as ethylene, auxines and cytokinin analogues (e.g., Belay & Daniels, 1987; Marchaim et al., 1997). Furthermore, a wide range of 'other' substances may be present or produced in biogas plants. Whether the concentrations in biogas reactors are high enough to affect seed viability is unknown.

Seed damaging or seed protecting mechanisms may exist in biogas reactors too. For example, if seeds in biogas reactors would not fully imbibe (mc<20 %), they would respond as if exposed to the accelerated ageing test and die much more rapidly. Imbibition is a strictly physical process, and depends on the difference in water potential between the seed and its environment, the protein, lipid and starch composition of the seed, and the permeability of the seed coat (Nelson, 2004). Water will be absorbed regardless of whether seeds are dormant (except physically dormant) or non-dormant seeds, viable or nonviable (Bewley & Black, 1994). The water potential in seeds may range from -350 MPa to -50 MPa (Nelson, 2004; Bewley & Black, 1994). However, the water potential of mixtures inside biogas reactors is unknown. If the difference is insufficient, seeds will not or only partially imbibe. Furthermore, heavy metals are known to block water uptake in seeds (Kranner & Colville, 2011). If seeds are indeed only partially imbibed in biogas reactors, the accelerated aging test could be used to predict seed resistance to anaerobic digestion. A special case involves seeds with a water-impermeable layer (see VII.A.) that do not imbibe at all when exposed to water, rendering them much more thermoresistant than partially or fully imbibed seeds. This situation will be discussed in more detail in section VII.A.

Seed Defence Mechanisms

Because thermosensitivity can explain only part of the inactivation of seeds in biogas reactors, in particular under mesophilic conditions, chemical and biological processes occurring during anaerobic digestion have to play a role as well. Understanding the various ways that seeds defend themselves against microbial attack and toxins may help to identify weak spots in the defence, and, identify groups of seed species that might be either unusually susceptible or unusually resistant to inactivation during anaerobic digestion.

The seed coat is an effective barrier against microbial attack and toxic compounds (Mohamed-Yasseen et al., 1994). Halloin (1983) described it as the most important component of resistance against microbial attack. Seeds with deliberately damaged seed coats have a much lower survival probability both in the soil (Davis et al., 2008) and in the rumen (e.g., Michael et al., 2006), and reduced longevity during storage (Mohamed-Yasseen et al., 1994 and references therein). To gain access to the embryo, microorganisms have to breach the protection offered by the seed coat and other protective layers. Various reviews summarize the available knowledge with regard to the structure and functioning of the seed coat and other layers in seeds in the defence against microbial infections (e.g., Halloin, 1983; Mohamed-Yasseen et al., 1994; Dalling et al., 2011). Here, the most important findings will be summarized with an emphasis on those aspects that are most relevant to the issue at hand.

Halloin (1983) eloquently summarized the functioning of seed coat as; 'a chemical barrier of inhibitory polyphenolic compounds, as a mechanical barrier, and as a barrier to the availability of nutrients to fungi'. This division will be used to structure the following sub-sections.

Seed Coat Composition, Thickness and Weak Spots

The first barrier is a physical one. The seed coat is presumed to be the initial point of access for microorganisms (e.g., Chee-Sanford et al., 2006). Seed coat composition and thickness may determine to a large extent the sensitivity to microbial degradation.

Unfortunately, very little research has focussed on the composition of seed coats (Graven et al., 1996). Consequently, it is largely unknown if and how seeds of various weed species differ in seed coat composition. The general assumption is that the seed coat consists mainly of the usual cell wall components, including cellulose, hemicellulose, pectin and lignin. Because hydrolytic bacteria produce cellulases and hemicellulases profusely, seed coats could be digested. There is only a limited amount of direct evidence for this to happen. Observations by scanning electron microscope (Simao Neto et al., 1987) and light microscope (Michael et al., 2006) indicate that a thin outer layer of the seed coat of legume and Malva parviflora seeds was partly or wholly removed during passage through the digestive tract of ruminants. Legume seeds that survived passage through animals were often blackened and partially swollen, indicating that they had been acted upon by the digestive processes (Glendening & Paulsen, 1950). Fermentation in the rumen was accompanied by loss of dry matter, which increased with MRT (Alomar et al., 1992; Fredrickson et al., 1997). The weight of C. album and oilseed rape seeds decreased when exposed to selected bacteria (Streptomyces spp.) and fungi (Phanerochaete chrysosprium) in liquid medium or soil (Einhom & Brandau, 2006). The weight loss suggests that either part of the seed coat or entire seeds were digested. Weight loss was also observed when only the seed coats of oilseed rape seed were exposed, despite the fact that these contained a large percentage of lignin (Einhom & Brandau, 2006). Lignin cannot easily be digested by hydrolytic bacteria (Hofrichter, 2002). However, the bacteria and fungi used in the study by Einhom and Brandau (2006) had been selected on the basis of known or suspected production of high amounts of cellulase or lignin-modifying enzymes.

Chemical Defence

A second function of the seed coat as a defence against microbial attack, as defined by Halloin (1983), is a chemical barrier. In addition to lignin, the seed coat may contain all kinds of alkaloids, terpenoids, biogenic silica, peptides, suberin, protease inhibitors, lectins and (poly)phenolic compounds, such as flavanols, catechins, tannins and other pigments, etc. (Rolston, 1978, Halloin, 1983; Broekaert et al., 1995). These substances can have multiple functions, such as waterproofing the seed coat, inhibit germination, maintain dormancy, inhibit or kill microbes and deter granivores (e.g., Rolston, 1978; Mohamed-Yasseen et al., 1994; Dalling et al., 2011). An indication of the involvement of biogenic silica in seed resistance against anaerobic digestion was found in Jeyanayagam and Collins (1984), who claimed that the higher ash content of S. halepense (9.4 %) in comparison to Panicum dichotomoflora (2.6 %) was responsible for the lower digestibility of S. halepense in anaerobic digesters. Unfortunately, the conclusion was based on only two species and requires confirmation.

With the exception of A. theophrasti (Kremer, 1993 and references therein), almost nothing is known with regard to the identity or effectiveness of the chemical compounds involved in chemical defence in weed seeds. It is, therefore, unknown how and how much species of weed seeds differ in this respect. Tests to determine the identity and concentrations of antimicrobial compounds require specialized laboratories and cannot be determined quickly and easily. However, there is no doubt that secondary plant metabolites affect microorganisms. Some secondary plant metabolites affect digestibility of plant materials in both ruminants and biogas reactors (Van Soest, 1982, 1988; Deublein & Steinhauser, 2011). Digestibility is sometimes more limited by substances such as tannins and silica than by lignin (Jackson, 1977; Van Soest, 1988). Biogenic silica, for example, reduces the digestibility of cellulose and hemicellulose in a manner that is additive to lignin (Van Soest & Jones, 1968).

Nutrient Availability and Microorganisms

The third function of the seed coat is described by Halloin (1983) as 'a barrier to the availability of nutrients to fungi'. Based on insights gained over the last four decades, the third function needs to be slightly revised, because the seed coat naturally harbours and nurtures microorganisms that are generally considered beneficial to the seed (Nelson, 2004; Chee-Sanford et al., 2006). These mutualistically associated microorganisms provide protection against pathogenic microorganisms, via competition for nutrients and space, the production of inhibitors and antimicrobial compounds (Broekaert et al., 1995), and the decomposition of chemical cues that could attract deleterious microorganisms in the spermophere (Nelson, 2004; and references therein). In turn, the seed coat functions a source of carbon and nitrogen, and it provides structure, binding sites for microbial attachment, and protection from predators and adverse environmental conditions. It seems that if microorganisms cannot be kept at bay, it is better to team up with the beneficial ones, rather than to be exposed to the pathogenic ones.

Beneficial seed-microbial associations can be formed during seed set, or after seed dispersal in the soil. In the latter case, community composition depends to a large extent on the microorganisms present in the substrate surrounding the seed (Nelson, 2004; Chee-Sanford et al., 2006). Seeds influence their relationship with microorganisms; different weed species and different genotypes harbour different microbial assemblages (Nelson, 2004; Chee-Sanford et al., 2006). Also, the number of microorganisms that colonize a seed and their spatial distribution on the seed surface differs between species and genotypes (Nelson, 2004 and references therein). The selectivity may be based on nutritional selection, selection by antimicrobial compounds, or by providing distinctive opportunities for nutrition and surface attachment (Chee-Sanford et al., 2006).

Initially, biofilm formation will not be extensive, given the relatively dry and oligotrophic conditions on seed surface and in the spermosphere. However, when the conditions are right for germination, in particular with regard to water availability and temperature, seeds will start to imbibe water; a process that is immediately accompanied by the leaking of cellular and vacuolar constituents from the seed (Nelson, 2004). The substances released are usually low-molecular-weight molecules and include carbohydrates and amino acids. Leaking stops after approximately 12 h when cellular membranes are fully hydrated and functional (Nelson, 2004 and references therein). During this short period of time, the attached microorganisms will grow, such that a more extensive biofilm is present when some time later the radicle extends and protrudes through the seed coat; the most vulnerable stage in the life of a seed.

The interaction with microorganisms is a double-edged sword. Exogenous soil microorganisms will be stimulated to germinate or attracted by the exudates, and compete with the resident microorganism for the available resources. Pathogenic microorganisms can outcompete the beneficial ones, colonize the seed coat, and induce seed coat decomposition. Studies that search for microorganisms that can either provide protection against plant diseases to crop seeds (Nelson, 2004 and references therein, Dalling et al., 2011) or help to control weeds by decomposing seeds in the weed seed bank (Kremer, 1993, Kennedy, 1999; Chee-Sanford et al., 2006) reflect this dualism. Compared to the conditions in the soil, conditions in biogas reactors may be favourable for prolific growth of microorganisms (moist, warm, anaerobic and eutrophic). It is uncertain how much protection the associated, beneficial microorganisms, if any, may provide under these conditions, but most likely they will be outcompeted by the active hydrolytic assembly in the slurry.

Seeds can also harbour microorganisms that have colonized internal tissues (endophytes). These microorganisms may confer various benefits to seedling and plant, including enhanced nutrient uptake, greater stress tolerance, and protection from herbivory, plant pathogens and pests (Clay & Schardl, 2002 and references therein). However, it is unknown if and how they help protect the seed itself. Furthermore, the fate of endophytes in anaerobic digesters is unexplored.

Species Resistant to Anaerobic Digestion

Based on the previous sections, four groups of plant species could be identified that might have a higher than usual probability of surviving anaerobic digestion, namely weed species with hard seeds (see VII.A.), thermoresistance not based on a water-impermeable layer in the seed coat (see VII.B.), seeds with a thick seed coat (see VII.C.), and seeds adapted to endozoochory (see VII.D.).

Seed with a Water-Impermeable Layer (Hard Seeds)

Mechanism and Occurrence

Seeds with water-impermeable layers in the seed coat or fruit form a special category, because they do not imbibe water. Seeds that do not imbibe water are less sensitive to heat stress than partially or fully imbibed seeds (see V.A. Ad 1). Ergo, seeds with a water-impermeable seed coat are expected to be able to survive high temperatures, such as in anaerobic digesters or the intestinal tract of animals, much better than imbibed seeds. They are termed 'hardseeded' or 'hard seed', because they remain hard compared to imbibed seeds, which swell and soften during imbibition (Rolston, 1978). Hardseededness is one of the mechanisms responsible for keeping seeds in a state of dormancy (called 'physical dormant' by Baskin & Baskin, 1998 or 'intrinsically quiescent' by Murdoch & Ellis, 2000). This term is not to be confused with the thickness or hardness of the material of the seed coat itself.

Usually, the water-impermeable barrier consists of one or more palisade layers of lignified cells in the seed coat, waterproofed by wax, lignin, tannin, suberin, pectin, quinine derivates, or phenolic compounds (e.g., Rolston, 1978; Baskin et al., 2000; Ma et al., 2004). Impermeability develops during seed dehydration, meaning that newly formed seeds are not immediately water-impermeable. Initially, water is lost via the seed coat, but once water impermeability develops, the hilum (the mark on the seed coat indicating the former attachment site to the ovary wall) acts as a hygroscopic valve that prevents water uptake but allows water loss (Rolston, 1978). The percentage of water-impermeable seeds in a seed lot increases with decreasing moisture content of the seeds and is influenced by genetics and by environmental factors during maturation. If dehydration is insufficient (> 10 % me), water impermeability can be reversed. The status of a seed lot can, therefore, be described in terms of both degree and percentage of water impermeability (Rolston, 1978).

Hardseededness is usually associated with members of the Fabaceae, but can also be found in members of many other families, including Convolvulacea, Geraniaceae, Malvaceae, and Solanaceae (Rolston, 1978; Baskin et al., 2000; Murdoch & Ellis, 2000). Not all members of these families exhibit hardseededness. For many species it is unknown if they have a water-impermeable layer. Arable weed species with known hardseededness include A. theophrasti, An. cristata, M. parviflora, M. pusilla, Sida hermaphrodita and S. spinosa (Malvaceae), Datura ferox (Solanaceae), Erodium botrys, E. cicutarium, Geranium carolinianum, G. dissectum, G. molle, G. pusillum and G. robertianum (Geraniaceae), Convolvulus arvensis, C. sepium, Ipomoea purpurea, I. hederaceae and Cuscuta campestri's (Convolvulaceae), Lespedeza capitata, Melilotus alba, M. officinalis and Vicia sp. (Fabaceae), (Horowitz & Taylorson, 1984, Marowski & Morrison, 1989, Baskin & Baskin, 1998; and references therein, Meisert, 2002, Michael et al., 2006, Dorado et al., 2009). A large number of legume crop species are hardseeded, including lucerne, clovers, fetch, lupin, soybean, and pea, although for several crops varieties have been bred without hardseededness.

Survival of Hard Seeds during Anaerobic Digestion

There is little information on the survival of water-impermeable seeds in biogas reactors. Red clover (Fabaceae) was among the best survival species in simulated batch reactors (Leonhardt et al., 2010) and A. theophrasti (Malvacaea) survived best in a PFR (Katovich et al., 2004). A. theophrasti and M. neglecta (Malvacaea), D. stramonium (Solanaceae), E. cicuratium (Geraniaceae), and V. tetrasperma (Fabaceae) were the best surviving out of 21 species in simulated batch reactors (Westerman et al., 2012a); M. neglecta was also the best surviving species in commercial biogas plants, but A. theophrasti was not (Westerman et al., 2012b). Soyabean (Fabaceae) was among the worst surviving species in simulated batch reactors (Strauss et al., 2012; but see also VII.A.3.). In soil solarisation studies, Melilotus sp. and Medicago sp. (Fabaceae; Elmore, 1991), and A. theophrasti and An. cristata (Malvaceae; Egley, 1990) were among the more thermoresistant species.

More information is available on the survival of water-impermeable seeds in the digestive tract of animals. Legumes and other species with physical dormancy invariable stand out as being among the most resistant to anaerobic digestion in the alimentary tract of animals. For example, of the four most resistant species in the study by D'hondt and Hoffmann (2011), one belonged to the Malvaceae (Helianthemum nummularum), two to the Fabaceae (T. campestre, T. pratense), and one to the Juncaceae (J. bufonius), whereby the latter species was recognized for having highly water-impermeable seeds (Peco et al., 2006). Of the five most resistant species in the study by Cosyns et al. (2005), one belonged to the Malvaceae (H. nummularum), two to the Fabaceae (T. arvense, T. pratense), one to the Cyperaceae (Carex arenaria), and one to the Poaceae (Agrostis capillaries). Of the five most resistant species in the study by Peco et al. (2006), two belonged to the Fabaceae (=Leguminosae) (Astragalus pelecinus, Ornithopus compressus), one to the Campanulaceae (Jasione montana), one to the Lamiaceae (Lavandula stoechas), and one to the Plantaginaceae (P. lanceolata).

For a range of legume species, the percentage of seed survival in the rumen was directly related to the percentage of hard seeds in the original material (Gardener et al., 1993a, b). Soft seeds die, while most of the remaining hard seeds survive passage through the tract (Gardener et al., 1993a, Glendening & Paulsen, 1950). Similar results were obtained for M. parviflora; seeds that were made water permeable through mechanical scarification were completely digested within 24 h in the rumen, while hard seeds remained largely intact until the end of the experiment (48 h; Michael et al., 2006).

Controlled and prolonged exposure to the rumen via fistulas suggest the existence of two seed survival curves; one for water-permeable soft seed with a short lag time is short and a rapid rate of decline, and one for water-impermeable hard seeds with a long lag time and slow rate of decline. In several legume species, the time required to kill hard seeds exceeded the natural MRT in the digestive tract of cattle (35-51 h; Gardener et al., 1993a, b).

Restoring Water Permeability

When water permeability is restored, seeds will imbibe water and thermoresistance will be lost. It is unknown how well conditions inside biogas reactors fulfil the requirements for restoring water permeability. Water permeability can naturally be restored by high temperatures, low winter temperatures, temperature fluctuations, fire, passage through the digestive tract of animals, and, possibly, by microbial activity (Rolston, 1978, Baskin & Baskin., 1998). Methods of artificially restoring water permeability include acid scarification (concentrated sulphuric acid), mechanical scarification, organic solvents (ethanol, acetone), wet heat (60-100[degrees]C), dry heat (50-150[degrees]C), prolonged storage, soaking, high pressure, percussion, freezing, heating, and radiation or ultrasound treatments (Rolston, 1978, Baskin & Baskin, 1998). Conditions in biogas reactors are such that dormancy is likely to be broken in at least some hardseeded species.

All treatments act via one of the build-in areas of weakness in the seed coat, i.e., hilum, strophiole (a crestlike excrescence about the hilum), micropyle (opening through which the pollen tube enters), or chalaza (the region opposite the micropyle, where the integuments and nucellus (central part in which the embryo sac develops) are joined) that either softens, cracks, ruptures, or collapses during treatment (Rolston, 1978, Baskin et al., 2000). However, in soybean cultivars that have been bred for reduced hardseededness, cracks develop outside these pre-designed areas (Ma et al., 2004), which may have been the reason for the low survival of soyabean in the study by StrauB et al. (2012). Not all mechanisms work for all species. For example, Gardener et al. (1993b) found large differences between legume species in resistance to breakdown in the digestive system of ruminants.

Once water permeability is restored, seeds respond to anaerobic digestion as any other species without a water-impermeable layer. However, water uptake can cause a doubling in seed size or weight (Leopold, 1983, Mullin & Xu, 2001, Geneve et al., 2007), which results in an increase in the pressure within the seed coat. The strain causes a decrease in thickness and hardness of the seed coat, making it more vulnerable to mechanical damage and infection (Fraczek et al., 2005). When the difference in water potential between seed and environment is large, water uptake is fast and both seed coat and embryonic tissues can weaken or rupture (soaking injury; Yasue & Hibino, 1984, Bewley & Black, 1994, Fraczek et al., 2005).

Other Thermoresistant Species

Based on studies comparing the thermoresistance of seeds in hot water or hot, moist soil, seeds of, for example, Melilotus sp., Medicago sp., S. spinosa, A. theophrasti, An. cristata, A. retroflexus, A. spinosus, A. albus, S. nigrum, S. carolinense, tomato, R. obtusifolius, P oleracea, Po. persicaria, A. fatue, and S. halepense would qualify as relatively thermoresistant. The first five are hardseeded but the other species are not. The mechanism involved in thermoresistance of the latter 11 species is unknown and, therefore, testing in hot water baths will be needed to identify such species.

Seeds with a Thick Seed Coat

It is reasonable to assume that the thicker the seed coat, the longer it will take to be digested. There is very little direct evidence that the thickness of the seed coat is related to seed survival in anaerobic digesters. Only a few species of weed seeds have been tested in biogas plants and for most of these the thickness of the seed coat is unknown (but see: Davis et al., 2008, Gardarin et al., 2010). Nevertheless, differences in seed coat thickness were consistent with the longer period required to inactivate A. artemisiifolia (159 [micro]m; Gardarin et al., 2010) than C. bursa-pastoris (18 [micro]m) or S. media (27 [micro]m) in simulated batch reactors (Leonhardt et al., 2010).

There is indirect evidence that the thickness of the seed coat may aid in seed survival during anaerobic digestion. A significant relationship was found between seed coat thickness and seed persistence in the soil (Davis et al., 2008, Gardarin et al., 2010). This relationship was not linear, but seed mortality declined exponentially with increasing thickness (Gardarin et al., 2010), meaning that for thin-coated seeds an increase in thickness causes a relatively large reduction in seed mortality, while for thick-coated species a similar increase causes only a small reduction in seed mortality. Seed longevity in the soil, in turn, has been related to seed survival during anaerobic digestion in ruminants, suggesting that factors responsible for seed survival in the seed bank also protect seeds during anaerobic digestion (Cosyns et al., 2005, Mouissie et al., 2005). The latter relationships tend to be significant, but weak (slope of the regression line=0.15, Cosyns et al., 2005; R=0.4, Mouissie et al., 2005), suggesting the involvement of modifying factors. Further research is required on this subject. Techniques for measuring the thickness of the seed coat, based on light or electron microscopy or X-rays in combination with image analysis, are available (e.g., Fraczek et al., 2005, Davis et al., 2008, Gardarin et al., 2010).

Microbes could bypass the tedious process of decomposing the seed coat if they could gain access directly via pre-designed weak spots, such as hilum, strophiole, chalaza, or micropyle, or via entrances created by cracks, nicks or wrinkles in the seed coat. There is some evidence that suggest that this may be happening. For example, Halloin (1975) observed that certain fungi entered cotton seeds predominantly via the chalaza. Decomposed seeds with entirely intact seed coats were found by Chee-Sanford et al. (2006). It is unknown how common this phenomenon is. Most seed lots contain at least some seeds with cracked or damaged seed coats. The degree of cracking, in terms of the percentage of the population affected and severity of cracking, is largely influenced by the conditions during seed filling and imbibition. It can also have a hereditary basis, for instance, via genes that code for seed coat composition (e.g., Moise et al., 2005; and references therein). The same applies to wrinkling and shrinking of seeds (Halloin, 1983 and Mohamed-Yasseen et al., 1994 and references therein). Consequently, analysing seed coat thickness as a predictor for resistance against anaerobic digestion is only useful for a certain category of seed species.

If seeds would actually germinate during anaerobic digestion they would most likely be doomed. There are some indications for this to happen. Janzen (1981) found partly digested, newly germinated seed of Enterolobium cyclocarpum in the dung of horses. Some species of seeds can germinate under anaerobic conditions, i.e., weeds in rice (Kennedy et al., 1980, Yamasue, 2001). The presence of phytohormones in biogas plants, such as ethylene, auxines and cytokinin analogues (e.g., Belay & Daniels, 1987, Marchaim et al., 1997) may help breaking dormancy and initiate germination. It is completely unknown if germination of seeds inside anaerobic digesters occurs or not.

Openings in the seed coat, due to germination, cracking, or other causes do not always have to lead to seed mortality. Resistance mechanisms exist within the embryo and other tissues inside the seed coat (Halloin, 1983 and reference therein). For example, when seeds of the grass Pennisetum clandestinum were deliberately damaged by clipping the tip of the seed, mortality in the ruminal fluid was enhanced (48 % vs. 37 %), but not 100 %, as expected. A similar result was obtained with damaged grass seeds in comparison with damaged legume seeds (Simao Neto et al., 1987). The need for additional protective layers may be higher in seeds that normally germinate hypogeally vs. epigeally. Monocotyledons germinate hypogeally, while dicotyledons germinate predominantly epigeally. In the case of epigeal germination, the cotyledons and seed coat are pushed out of the soil during germination, such that further colonization by soil microorganisms is prevented (Nelson, 2004). In the case of hypogeal germination, only the epicotyl with the meristematic tissue or the coleoptile that covers the shoot reach the soil surface, while all other structures, such as endosperm and cotyledons, remain underground requiring further protection.

Seeds Selected for Endozoochory

Usually, seed defence mechanisms have developed in response to adverse conditions and microbial pressure associated with the soil environment. However, Janzen (1984) suggested that seed attributes could have developed in response to selection exerted by grazers. In analogy with selection of specific seed traits that accommodate dispersal by ants, birds or wind, Janzen (1984) proposed that grazers could exert a selective force to accommodate endozoochory by herbivorous mammals, such that seeds would become more resistant to anaerobic digestion. The ideal zoochorical seed as anticipated by Janzen would be small, tough, hard and inconspicuous, and its seed coat would have to be able to resist digestion for a period of days or months, and would have to contain toxins to protect against seed predators, without affecting the large herbivores that eat them. Unfortunately, there is little empirical evidence to support Janzen's theory. Nevertheless, the idea that grazers can at least in some cases exert selection has been accepted (e.g., D'hondt & Hoffmann, 2011). This would suggest that seed species whose mode of dispersal is mainly through endozoochory could prove to be more resistant to anaerobic digestion in biogas reactors. The identification of seeds predominantly dispersed via endozoochory will be difficult, because seed traits associated with this means of dispersal are very general. Besides, most could have originated through selection by other forces as well.

Several studies compared the survival (or germination) of a range of seed species after passage through the digestive tract of ruminants and other animals. All studies indicated clear differences in survival probability between seed species. Attempts were made to correlate seed survival to certain seed characteristics, such as seed size, weight, and shape (ecological correlates); if successful, dispersal distance and spatial distribution patterns of species due to endozoochory could be simulated (e.g., Will & Tackenberg, 2008). However, results were inconsistent. For example, some found that round seeds survived or germinated better than elongated seeds (Simao Neto et al., 1987, Mouissie et al., 2005). In contrast, others found that ovate-lanceolate seeds survived or germinated better than round seeds (Cosyns et al., 2005). Some found that seed survival and germination were positively influenced by seed mass (Cosyns et al., 2005, Peco et al., 2006); others that seed survival was negatively influenced by seed mass (Mouissie et al., 2005).

The only seed characteristic that was more or less consistently positively related to seed survival after passage through the alimentary tract of animals was the seed longevity index (LI), i.e., the proportion of records in a database that report a species as having a persistent seed bank (Thompson et al., 1997b). This suggests that the same factors responsible for seed persistence in the seed bank also protect seeds in the gastrointestinal tract. Because seed persistence is strongly correlated with seed coat thickness (Davis et al., 2008, Gardarin et al., 2010), it would be worthwhile to include seed coat thickness in future studies searching for ecological correlates.

Various explanations for the observed inconsistencies have been put forward, such as a) the fact that large-seeded species are more prone to mechanical damage by chewing (e.g., Mouissie et al., 2005), b) the residence time in the alimentary tract of ruminants is influenced by particle size and density, and c) statistical problems related to small sample size and taxonomic interdependencies (D'hondt & Hoffmann, 2011).

The latter authors pointed out that the high survival rate of seeds with water-impermeable seed coats (physical dormancy), which do not imbibe water, overruled simple seed traits, such as size, weight and shape. Omission of seeds with physical dormancy from the data sets may elicit correlations with other seed traits. They furthermore suggested that the water-impermeable seed coat itself could be the most important ecological correlate and that it may have evolved through frequent ingestion by grazers. This is corroborated by data by Gardener et al. (1993a, b).

Gardener et al. (1993b) furthermore found that the seeds of dense, low-growing, rhizomatous or stoloniferous grasses have a higher survival probability during passage through the gastrointestinal tract of cattle than seeds of tall, tussock grasses. The former category of seeds has a higher probability of being ingested during cattle grazing than the latter. It would also mean that the selection of 'anaerobic-digestion-resistant' biotypes in repeatedly recycled sludge from biomass to crop field and vice versa is likely.

Prospects

Potential Test Procedures

In summary, the available, scarce information gathered in this review suggests that seeds die during anaerobic digestion due to a combination of thermal inactivation and inactivation due to microbial activity. Evidence for inactivation by toxic compounds is lacking, but may exist too. Given these mechanisms, tests could be selected to help to screen a large range of seed species for tentative resistance to anaerobic digestion in biogas reactors.

Sensitivity to thermal inactivation could be determined relatively easily using exposure of seeds to hot water baths (e.g., Dahlquist et al., 2007). Such tests would estimate minimum seed mortality to be expected inside biogas reactors; the actual mortality will be higher, in particular in reactors operated in the mesophilic temperature range.

Procedures to screen seed resistance to microbial inactivation are much more speculative, because the mechanisms and processes involved are not well understood and may differ between seed species. Systematic empirical data is lacking. There are some indications that seed coat thickness may be related to sensitivity to microbial inactivation; the thicker the seed coat, the longer it will take to decompose. Various methods are available for estimating seed coat thickness. However, the relationship may be disrupted by seeds that have cracks, wrinkles, or pre-designed 'weak spots' in the seed coat that microorganisms could use as an easy point of entry. It is not clear how to identify these.

There is a positive correlation between the degree of persistence of seeds in the soil seed bank and seed survival during anaerobic digestion. This would make sense, given that microbial processes are involved in the degradation of seeds in both systems, although the one proceeds much faster than the other. The seed longevity index, which is usually used to quantify seed persistence and which is defined as the proportion of records in a database that report a species as having a persistent seed bank (Thompson et al., 1997b), may not necessarily be the most appropriate measure for seed persistence (e.g., Bekker et al., 1998). Seed persistence, in turn, is positively correlated with seed coat thickness, and it is possible that the two are based on the same principle.

It is likely that the seed coat composition, in particular the degree of lignification and the presence and concentration of secondary metabolites with antimicrobial activity, influences the speed of decomposition by microorganisms. However, empirical evidence is largely lacking. Methods to determine and compare the chemical composition are generally complicated and expensive, and the routine use of these is unlikely. One exception involves ash content as an estimate of biogenic silica, which strongly limits digestibility.

Testing of seeds via ingestion by animals, in particular ruminants, could help to determine the sensitivity of seed species to anaerobic digestion in biogas reactors, because the two systems bear close resemblance. However, interpretation of the data sets derived from such studies is obscured by several factors that are irrelevant to the situation in biogas plants, such as species-specific residence times and damage due to chewing. Studies in which seeds are exposed to ruminal conditions under more controlled conditions and for known periods of time, i.e., via fistulated animals or in artificial rumen (e.g., Rusitec), may yield relationships that are much more valuable for predicting seed survival in biogas reactors.

Groups of Seed Species Resistant to Anaerobic Digestion

Two groups of seeds stood out with regard to their tentative potential to withstand anaerobic digestion; those with a water-impermeable seed coat and those adapted to dispersal via endozoochory. The two groups may partially overlap.

Seeds with a water-impermeable layer in the seed coat (hardseededness or physically dormant) do not absorb water when imbibed, and are, therefore, protected from thermal inactivation. However, once the water-impermeable layer is breached, the seeds imbibe water and thermoresistance is lost. Several physical cues necessary for breaking physical dormancy are present in biogas reactors. Hardseeded species and biotypes within species may differ, genetically or phenotypically, in the percentage of hardseededness within a population.

Seeds adapted to dispersal via ingestion by grazers (endozoochory) are expected to be more resistant to anaerobic digestion than those that rely on other modes of dispersal. Unfortunately, the anticipated physical characteristics of endozoochorically dispersed seeds, i.e., small, tough, hard, and inconspicuous (Janzen, 1984), cannot be distinguished from other seeds, and such seeds will, therefore, be hard to identify. It has been proposed that hardseededness has evolved in response to frequent ingestion by grazers (D'hondt & Hoffmann, 2011), meaning that hard seeded species are both thermoresistant and resistant to anaerobic digestion. Other groups of seed species prone to frequent ingestion by grazers, in particular small grasses, may have developed resistance to anaerobic digestion, which is neither based on hardseededness nor on seed coat thickness.

DOI 10.1007/s12229-013-9118-7

Acknowledgment This study was made possible with the financial support of the German Agency for Renewable Resources (Fachagentur fur Nachwachsende Rohrstoffc c.V.; Bundcsministerium fur Emahrung, Landwirtschatt und Verbrauehcrschutz (= German Federal Ministry of Food, Agriculture and Consumer Protection)), project No. 22028408, 'Untersuchungcn zum phytosanitfircn Risiko durch die anaerobe Vergarung von pflanzlichen Biomassen in Biogasanlagen; Teilvorhaben 2.'

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Paula R. Westerman (1,2) Barbel Gerowitt (1)

(1) Group Crop Health, Faculty of Agricultural and Environmental Sciences, University of Rostock, Satower Str. 48, 18059 Rostock, Germany

(2) Author for Correspondence; e-mail: paula.westerman@uni-rostock.de

Published online: 7 August 2013

Table 1 Inactivation of seeds during anaerobic digestion, either
expressed as survival (%) given a certain exposure time, or as the
length of time required until full inactivation, given specific
reactor types and operational temperatures

Reference            Species            Reactor       Temperature
                                        type          [[degrees]C]

Bohm et al.,         tomato             Exp. CSTR     33
  2000
Engeli et al.,       Rumex              Exp. batch    35
  1993                 obtusifolius
Engeli et al.,       tomato             Exp. batch    35
  1993
Jeyanayagam &        Panicum            Exp. CSTR     35
  Collins, 1984        dichotomoflora
Jeyanayagam &        Sorghum            Exp. CSTR     35
  Collins, 1984        halepense
Katovich et al.,     Abutilon           PFR           37
  2004                 theophrasti
Katovich et al.,     Amaranthus         PFR           37
  2004                 retrojlexus
Katovich et al.,     Chenopodium        PFR           37
  2004                 album
Katovich et al.,     Panicum            PFR           37
  2004                 miliaceum
Katovich et al.,     Polygonum          PFR           37
  2004                 persicaria
Katovich et al.,     Setaria faberi     PFR           37
  2004
Leonhardt            Amaranthus sp.     Exp. batch    35/50
  et al., 2010
Leonhardt            Atriplex patula    Exp. batch    35/50
  et al., 2010
Leonhardt            Avena fatua        Exp. batch    35/50
  et al., 2010
Leonhardt            Bromus sp.         Exp. batch    35/50
  et al., 2010
Leonhardt            Chenopodium        Exp. batch    35/50
  et al., 2010         album
Leonhardt            Echinocloa         Exp. batch    35/50
  et al., 2010         crus-galli
Leonhardt            Elytrigia repens   Exp. batch    35/50
  et al., 2010
Leonhardt            Galium aparine     Exp. batch    35/50
  et al., 2010
Leonhardt            Polygonum          Exp. batch    35/50
  et al., 2010         lapathifolium
Leonhardt            Rumex              Exp. batch    35/50
  et al., 20I0         obtusifolius
Leonhardt            Amaranthus sp.     Comm. CSTR    42/45/45
  et al., 2010
Leonhardt            A triplex pa       Comm. CSTR    42/45/45
  et al., 2010         tula
Leonhardt            Avena fatua        Comm. CSTR    42/45/45
  et al., 2010
Leonhardt            Bromus sp.         Comm. CSTR    42/45/45
  et al., 2010
Leonhardt            Chenopodium        Comm. CSTR    42/45/45
  et al., 2010         album
Leonhardt            Echinocloa crus-   Comm. CSTR    42/45/45
  et al., 2010         galli
Leonhardt            Elytrigia repens   Comm. CSTR    42/45/45
  et al., 2010

Leonhardt            Galium aparine     Comm. CSTR    42/45/45
  et al., 2010
Leonhardt            Rumex              Comm. CSTR    42/45/45
  et al., 2010         obtusifolius
Leonhardt            Polygonum          Comm. CSTR    42/45/45
  et al., 2010         lapathifolium
Leonhardt            Ambrosia           Exp. batch    35
  et al., 2010         artemesiifolia
Leonhardt            Capsella bursa-    Exp. batch    35
  et al., 2010         pastoris
Leonhardt            maize              Exp. batch    35
  et al., 2010
Leonhardt            red clover         Exp. batch    35
  et al., 2010
Leonhardt            Stellaria media    Exp, batch    35
  et al., 2010
Leonhardt            Trifolium          Exp. batch    35
  et al. 2010          aestivum
Lorenz               tomato             Exp. CSTR     34
  et al., 2001
Lorenz               tomato             Exp. CSTR     55
  et al., 2001
Marcinisyn           Rumex              Comm. CSTR    39-47
  et al., 2004         obtusifolius
Marcinisyn           tomato             Comm. CSTR    38-48
  et al., 2004
Marcinisyn           tomato             Comm. PFR     49
  et al., 2004
Marcinisyn           tomato             Comm. CSTR    55
  et al., 2004
Ryckeboer            tomato             Exp. PFR      52
  et al., 2002
Sarapatka            Agropyron repens   Comm. batch   50[right arrow]30
  et al., 1993                                          (c)
Sarapatka            Amaranthus         Comm. batch   50[right arrow]30
  et al., 1993         retroflexus                      (c)
Sarapatka            Avena fatua        Comm. batch   50[right arrow]30
  et al., 1993                                          (c)
Sarapatka            Chenopodium        Comm. batch   50[right arrow]30
  et al., 1993         album                            (c)
Sarapatka            Chenopodium        Comm. batch   50[right arrow]30
  et al., 1993         strictum                         (c)
Sarapatka            Echinochloa        Comm. batch   50[right arrow]30
  et al., 1993         crus-galli                       (c)
Sarapatka            Plantago major     Comm. batch   50[right arrow]30
  et al., 1993                                          (c)
Sarapatka            Polygonum          Comm. batch   50[right arrow]30
  et al., 1993         lapathifolium                    (c)
Sarapatka            Rumex              Comm. batch   50[right arrow]30
  et al., 1993         obtusifolius                     (c)
Sarapatka            Thlaspi arvense    Comm. batch   50[right arrow]30
  et al., 1993                                          (c)
Sarapatka            Tripleurospermum   Comm. batch   50[right arrow]30
  et al., 1993         maritimum                        (c)
Schrade et al.,      Alopecurus         Exp. CSTR     36/54
  2003                 myosuroides
Schrade et al.,      Chenopodium        Exp. CSTR     36/54
  2003                 album
Schrade et al.,      oilseed rape       Exp. CSTR     36/54
  2003
Schrade et al.,      Rumex              Exp. CSTR     36/54
  2003                 obtusifolius
Schrade et al.,      Sinapis arvensis   Exp. CSTR     36/54
  2003
Schrade et al.,      Thlaspi arvense    Exp. CSTR     36/54
  2003
Schrade et al.,      tomato             Exp. CSTR     36/54
  2003
Schrade et al.,      wheat              Exp. CSTR     36/54
  2003
Strauss et al.,      flax               Exp. batch    38
  2012
Strauss et al.,      maize              Exp. batch    38
  2012
Strauss et al.,      mustard            Exp. batch    38
  2012
Strauss et al.,      oilseed rape       Exp. batch    38
  2012
Strauss et al.,      soyabean           Exp. batch    38
  2012
Strauss et al.,      tomato             Exp. batch    38
  2012
Strauss et al.,      wheat              Exp. batch    38
  2012
Westerik &           Agrostemma         Exp. batch    38/51
  Kleizen, 2006        githago
Westerik &           Jacobaea           Exp. batch    38/51
  Kleizen, 2006        vulgaris
Westerik &           Rumex acetosella   Exp. batch    38/51
  Kleizen, 2006
Westerik &           Taraxacum          Exp. batch    38/51
  Kleizen, 2006        officinale
Westerik &           tomato             Exp. batch    38/51
  Kleizen, 2006
Westerik &           Urtica urens       Exp. batch    38/51
  Kleizen, 2006
Westerman            Abutilon           Exp. batch    37
  et al., 2012 (a)     theophrasti
Westerman            Amaranthus         Exp. batch    37
  et al., 2012 (a)     retrofexus
Westerman            Anchusa arvensis   Exp. batch    37
  et al., 2012 (a)
Westerman            Bromus secalinus   Exp. batch    37
  et al., 2012 (a)
Westerman            Capsella           Exp. batch    37
  et al., 2012 (a)     bursa-pastoris
Westerman            Chenopodium        Exp. batch    37
  et al., 2012 (a)     album
Westerman            Datura             Exp. batch    37
  et al., 2012 (a)     stramonium
Westerman            Echinochloa        Exp. batch    37
  et al., 2012 (a)     crusrgalli
Westerman            Erodium            Exp. batch    37
  et al., 2012 (a)     cicuratium
Westerman            Fallopia           Exp. batch    37
  et al., 2012 (a)     concolvulus
Westerman            Galium aparine     Exp. batch    37
  et al., 2012 (a)
Westerman            Geranium           Exp. batch    37
  et al., 2012 (a)     pusillum
Westerman            Lithospermum       Exp. batch    37
  et al., 2012 (a)     arvense
Westerman            Malva neglecta     Exp. batch    37
  et al., 2012 (a)
Westerman            Rumex              Exp. batch    37
  et al., 2012 (a)     obtusifolius
Westerman            Solanum nigrum     Exp. batch    37
  et al., 2012 (a)
Westerman            Stachus arvensis   Exp. batch    37
  et al., 2012 (a)
Westerman            Stellaria media    Exp. batch    37
  et al., 2012 (a)
Westerman            tomato             Exp. batch    37
  et al., 2012 (a)
Westerman            Tripleurospermum   Exp. batch    37
  et al., 2012 (a)     maritimum
Westerman            Vicia              Exp. batch    37
  et al., 2012 (a)     tetrasperma
Westerman            Abutilon           Comm. CSTR    41
  et al., 2012 (b)     theophrasti
Westerman            Chenopodium        Comm. CSTR    41
  et al., 2012 (b)     album
Westerman            Fallopia           Comm. CSTR    41
  et al., 2012 (b)     convolvulus
Westerman            Malva neglecta     Comm. CSTR    41
  et al., 2012 (b)
Westerman            tomato             Comm. CSTR    41
  et al., 2012 (b)

Reference            Exposure   Survival    Inactivation
                     [d]        (%)         [d]

Bohm et al.,                                21
  2000
Engeli et al.,       14         0
  1993
Engeli et al.,       14         56 (a)
  1993
Jeyanayagam &        28         55-63 (b)
  Collins, 1984
Jeyanayagam &        28         75-80 (b)
  Collins, 1984
Katovich et al.,     20         16
  2004
Katovich et al.,     20         1
  2004
Katovich et al.,     20         12
  2004
Katovich et al.,     20         0
  2004
Katovich et al.,     20         0
  2004
Katovich et al.,     20         0
  2004
Leonhardt                                   7/1
  et al., 2010
Leonhardt                                   7/1
  et al., 2010
Leonhardt                                   3/1
  et al., 2010
Leonhardt                                   1/1
  et al., 2010
Leonhardt                                   21/1
  et al., 2010
Leonhardt                                   7/1
  et al., 2010
Leonhardt                                   1/1
  et al., 2010
Leonhardt                                   1/1
  et al., 2010
Leonhardt                                   7/1
  et al., 2010
Leonhardt                                   7/1
  et al., 20I0
Leonhardt                                   3/7/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   7/7/3
  et al., 2010
Leonhardt                                   3/7/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   3/3/3
  et al., 2010
Leonhardt                                   3/7/3
  et al., 2010
Leonhardt                                   3
  et al., 2010
Leonhardt                                   0.42
  et al., 2010
Leonhardt                                   3
  et al., 2010
Leonhardt                                   3
  et al., 2010
Leonhardt                                   0.42
  et al., 2010
Leonhardt                                   1
  et al. 2010
Lorenz                                      21
  et al., 2001
Lorenz                                      1
  et al., 2001
Marcinisyn           20         0.09
  et al., 2004
Marcinisyn           21/42      0/0
  et al., 2004
Marcinisyn           14         0
  et al., 2004
Marcinisyn           14/28      0/0
  et al., 2004
Ryckeboer                                   0.8-1.0
  et al., 2002
Sarapatka            30         0
  et al., 1993
Sarapatka            30         4
  et al., 1993
Sarapatka            30         0
  et al., 1993
Sarapatka            30         9
  et al., 1993
Sarapatka            30         0
  et al., 1993
Sarapatka            30         36
  et al., 1993
Sarapatka            30         0
  et al., 1993
Sarapatka            30         0
  et al., 1993
Sarapatka            30         19
  et al., 1993
Sarapatka            30         0
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Sarapatka            30         0
  et al., 1993
Schrade et al.,                             1/1
  2003
Schrade et al.,                             21/1
  2003
Schrade et al.,                             1/1
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Schrade et al.,                             7/1
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Schrade et al.,                             1/1
  2003
Schrade et al.,                             3/1
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Schrade et al.,                             7/1
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Schrade et al.,                             1/1
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Strauss et al.,                             6
  2012
Strauss et al.,                             2
  2012
Strauss et al.,                             6
  2012
Strauss et al.,                             6
  2012
Strauss et al.,                             2
  2012
Strauss et al.,                             30
  2012
Strauss et al.,                             3
  2012
Westerik &                                  0.25/0.25
  Kleizen, 2006
Westerik &                                  1/0.1
  Kleizen, 2006
Westerik &                                  1/0.1
  Kleizen, 2006
Westerik &                                  0.25/0.04
  Kleizen, 2006
Westerik &                                  5/1
  Kleizen, 2006
Westerik &                                  2/1
  Kleizen, 2006
Westerman            30         36.5
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         <1
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         <1
  et al., 2012 (a)
Westerman            30         6.7
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         21.1
  et al., 2012 (a)
Westerman            30         <1
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         30.4
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         0
  et al., 2012 (a)
Westerman            30         2.8
  et al., 2012 (a)
Westerman            30         <1
  et al., 2012 (a)
Westerman            30         12.6
  et al., 2012 (a)
Westerman                                   1.5-2.0 (d)
  et al., 2012 (b)
Westerman                                   4.7-19.7 (d)
  et al., 2012 (b)
Westerman                                   1.2-9.1 (d)
  et al., 2012 (b)
Westerman                                   17-23.6 (d)
  et al., 2012 (b)
Westerman                                   0.8-8.1 (d)
  et al., 2012 (b)

(a) Nylon bags not in close contact with digestate

(b) Seeds first subjected to simulated rumen treatment

(c) Cooling from 50 to 30[degrees]C during operation

(d) Estimate of decimal reduction time
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Author:Westerman, Paula R.; Gerowitt, Barbel
Publication:The Botanical Review
Article Type:Report
Geographic Code:4EUGE
Date:Sep 1, 2013
Words:19410
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