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Seed germination test for toxicity evaluation of compost: Its roles, problems
and prospects
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                                                                                       Waste Management
                                                             journal homepage: www.elsevier.com/locate/wasman
a r t i c l e i n f o a b s t r a c t
Article history:                                                         Compost is commonly used for the growth of plants and the remediation of environmental pollution. It is
Received 6 April 2017                                                    important to evaluate the quality of compost and seed germination test is a powerful tool to examine the
Revised 18 September 2017                                                toxicity of compost, which is the most important aspect of the quality. Now the test is widely adopted,
Accepted 19 September 2017
                                                                         but the main problem is that the test results vary with different methods and seed species, which limits
Available online xxxx
                                                                         the development and application of it. The standardization of methods and the modelization of seeds can
                                                                         contribute to solving the problem. Additionally, according to the probabilistic theory of seed germination,
Keywords:
                                                                         the error caused by the analysis and judgment methods of the test results can be reduced. Here, we
Compost
Toxicity
                                                                         reviewed the roles, problems and prospects of the seed germination test in the studies of compost.
Germination                                                                                                                                     Ó 2017 Published by Elsevier Ltd.
Model seed
Contents
    1.   The roles of the seed germination test for the toxicity evaluation of compost . . . . . . . . . . . . . . . . . . . . . . . .                                            .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
    2.   Could there be a widely accepted procedure of the seed germination test? . . . . . . . . . . . . . . . . . . . . . . . . . .                                             .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
    3.   Is it necessary to improve analysis and judgment methods of the results of the seed germination test? . . .                                                              .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
    4.   Could there be a species of plant seed to be used as a model seed for the toxicity evaluation of compost?                                                                .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
    5.   Conclusions and prospects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .             .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
         Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .           .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
         References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   .   00
1. The roles of the seed germination test for the toxicity                                                               agro-industrial residues (Aviani et al., 2010), municipal organic
evaluation of compost                                                                                                    solid wastes (Kelessidis and Stasinakis (2012); Anand and Apul,
                                                                                                                         2014), etc. Compost is often used as the growth media (Boldrin
   Composting, an effective and economical biotechnology, is                                                             et al., 2010), the organic fertilizer (Feng et al., 2016), the soil
widely used in the sanitization and recycling of biowastes includ-                                                       amendment (D Hose et al., 2014; Alvarenga et al., 2015) and the
ing animal manures (Ge et al., 2016; Liang et al., 2017a) and car-                                                       suppressive substance of soil-borne plant diseases (Mehta et al.,
casses (Gwyther et al., 2011), crop straws (Zhang et al., 2016),                                                         2014; Yu et al., 2015) for agricultural production and landscaping.
                                                                                                                         In recent years composting has been studied for the bioremedia-
 ⇑ Corresponding authors at: College of Environmental Science and Engineering,                                           tion of soils contaminated with heavy metal(loid)s (Park et al.,
Hunan University, Changsha 410082, China.                                                                                2011; Wu et al., 2016; Liang et al., 2017 b) and organic
   E-mail addresses: liangjie@hnu.edu.cn, liangjie82@163.com (J. Liang),
zgming@hnu.edu.cn (G. Zeng).
https://doi.org/10.1016/j.wasman.2017.09.023
0956-053X/Ó 2017 Published by Elsevier Ltd.
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
2                                                       Y. Luo et al. / Waste Management xxx (2017) xxx–xxx
contaminants (Chen et al., 2015; Huang et al., 2016; Kastner and                            Number of germinated seedsðsampleÞ
                                                                                    RSG ¼                                        100%                       ð2Þ
Miltner, 2016).                                                                             Number of germinated seedsðcontrolÞ
    Compost quality, such as stability and maturity, should be
checked before the application of compost on land. The unstable                              Total radicle length of germinated seedsðsampleÞ
and/or immature compost can have adverse effects on seed germi-                     RRG ¼                                                       100%
                                                                                             Total radicle length of germinated seedsðcontrolÞ
nation, plant growth and soil environment due to the decreased
                                                                                                                                                             ð3Þ
supply of oxygen and/or available nitrogen or the presence of phy-
totoxic compounds (Bernal et al., 2009). Stability is the resistance
                                                                                    GI ¼ RSG  RRG  100%                                                    ð4Þ
of the organic matter in compost against further microbial decom-
position as long as there is no inhibition on the microbes by other
                                                                                           GI50% þ GI75%
factors not relevant to the organic matter, while maturity is an                    GI ¼                  100%                                              ð5Þ
agronomic parameter that is clearly associated to the effect of com-                             2
post on plant growth (Komilis, 2015). The indices of respiration
                                                                                           GI25% þ GI50% þ GI75%
and humification of compost are used to evaluate the stability                      GI ¼                          100%                                      ð6Þ
                                                                                                     3
and maturity of compost (Komilis and Kanellos, 2012; Hill et al.
(2013); Nikaeen et al., 2015), respectively. The substances, includ-                where GI25%, GI50% and GI75% were GI values of the samples that were
ing low molecular weight organic acids (e.g. phenolic acids                         25%, 50% and 75% of the raw aqueous extract of compost diluted
(Marambe et al., 1992)), ammonium nitrogen (NH+4-N) (Ramírez                        with deionized or distilled water (v/v), respectively.
et al., 2008), salinity (Hase and Kawamura, 2012), heavy metals                         At present, the major problem in the studies of the seed germi-
(Fuentes et al., 2004), xenobiotics (e.g. antibiotics (Liu et al.,                  nation test is that there is no universally adopted procedure, which
2009) and agrochemicals (Cayuela et al., 2008; Tang et al.,                         is reflected at the incompleteness of the test procedure and the dif-
2008)), can cause damage to plants when they are in high levels.                    ferences of the corresponding methods (Table 1). In the first step, it
In general, many of these substances need to be gauged via time-                    is essential to determine the extraction ratio because the toxicity of
consuming and expensive detection processes to determine                            compost extract is related to its concentration (Emino and
whether their levels are beyond or within acceptable ranges. How-                   Warman, 2004; Said-pullicino et al., 2007; Young et al., 2016).
ever, there exists the possibility for the unexpected factors that are              Although the extraction ratio of 1:10 (w/v) is one of the most used
not taken for analysis. Furthermore, there is a lack of analytical                  ratios in studies (Table 1), the test samples are fresh samples and
procedure to evaluate the joint effect of the toxic substances in                   have different moisture content. Owing to the large change in
compost. Consequently, as a bioassay, seed germination test has                     the moisture content of the raw material during composting, the
attracted a lot of attention to overcome these concerns. The seed                   moisture content of the samples collected from different compost-
germination index (GI) was firstly proposed by Zucconi et al.                       ing stages is different (Chikae et al., 2006). In order to accurately
(1981) who used cress seeds in the germination test for evaluating                  evaluate the change of the toxicity of samples during composting
the toxicity of compost. GI is calculated by the radicle length and                 and increase the comparability of the toxicity of samples with dif-
germination percentage of the seeds in the sample (compost                          ferent moisture content, it is necessary to eliminate the interfer-
extract) compared to that in the control (e.g. deionized water). GI                 ence of moisture content on test results. So far, there are two
is correlated with some other biological and chemical indices for                   methods to address this problem. One method (Chikae et al.,
evaluating compost quality. The study of El Fels et al. (2016)                      2006; Khan et al., 2014) is to prepare the extract according to a cer-
showed that GI was positively correlated with the biological index                  tain extraction ratio of water and dry weight of fresh sample, but
of the Artemia salina cytotoxicity test for evaluating the toxicity of              how to select a suitable value of the extraction ratio remains unset-
compost. In addition, GI is positively correlated with humification                 tled. Another method (Pampuro et al., 2010) is to adjust the mois-
parameters (Gavilanes-Terán et al., 2016) while negatively corre-                   ture content of fresh sample to 85% to prepare the extract or its
lated with the content of NH+4 (Tiquia et al., 1996; Guo et al.,                    dilutions for the seed germination test (Said-pullicino et al.,
2012). Therefore, the seed germination test has been broadly                        2007; Cesaro et al., 2015). Centrifugation and membrane filtration
accepted for evaluating compost quality. In Italy, GI is listed in                  can quickly and effectively remove the particulates in the extract.
the quality assessment regulation of compost for commercializa-                     They are essential steps to reduce the interference of particulates
tion (Cesaro et al., 2015). However, there are large variations in                  on test results. In the second step, the major differences are
the aspects of method and seed species of the test among previous                   reflected at the species of seed and the definition of seed germina-
studies (see Section 2). The problems and prospects of studies in                   tion (Table 1). There is no recognized seed species that can be used
the seed germination test will be comprehensively reviewed in                       to evaluate the toxicity of compost and the seed is often obtained
the following parts.                                                                locally. The definition of seed germination can be divided into
                                                                                    three groups by radicle length: only visible, at least 2 mm and at
2. Could there be a widely accepted procedure of the seed                           least 5 mm. It is not difficult to observe, even the incubation time
germination test?                                                                   is prolonged, the initial radicles of the germinated seeds inhibited
                                                                                    in test are no longer to elongate, so a certain length that the radicle
   The seed germination test procedure consists of three major                      reached is used as the operational definition of germination. In fact,
steps. Firstly, prepare an aqueous extract of compost; secondly,                    the process of germination is completed by visible radicle protru-
incubate seeds with the extract; thirdly, measure and calculate                     sion through the testa (seed coat), and radicle elongation belongs
the indicators related to the test results by Eqs. (1–6), including                 to post-germination (Weitbrecht et al., 2011). Moreover, if the
the seed germination (SG), the relative seed germination (RSG),                     incubation time is too long, the secondary root will begin to grow
the relative radicle growth (RRG) and the seed germination index                    and the cotyledon will have strong phototaxis, and the length of
(GI). More details of the typical test procedures in studies are sum-               radicle cannot exactly reflect the toxicity. The incubation time
marized in Table 1.                                                                 depends on specific environmental conditions and seed species.
                                                                                    After the incubation time is over, seeds can be frozen at -10 °C
       Number of germinated seeds
SG ¼                               100%                                  ð1Þ       for 24 h or added with ethanol equivalent to the sample (aqueous
         Number of total seeds                                                      extract) to end their growth (Macias et al., 2000; Gómez-Brandón
                                                                                    et al., 2008). These methods are effective in the handling of seeds,
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
                                                                                                                                                                   Table 1
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
The essential steps of the seed germination test for evaluating the toxicity of compost.
                                                                                                                                                                                                                                                                                                                                                                                                          3
4                                                       Y. Luo et al. / Waste Management xxx (2017) xxx–xxx
especially in measuring the radicle length of germinated seeds                      principle of the small probability event (a = 0.05), the case that
accurately. The third step is mainly about the calculation of GI                    the number of germinated seeds is less than seven in ten seeds
(see Eqs. (2–4) for more details). The GI value, not less than 80%,                 does not occur in one test (P < 0.05). If it does in the Petri dish of
usually means that compost has no phytotoxicity (Tiquia et al.,                     the sample, which means that the seed germination is inhibited;
1996). However, the toxicity of compost is also affected by the                     if it does in the Petri dish of the control, which means that the seed
extraction ratio. One way to eliminate the effect of the extraction                 selected is undesirable for the test. Usually, plump and shiny seeds
ratio is preparing high concentration of compost extract and using                  are sieved to ensure the germination under suitable conditions, but
its dilution with water (v/v) for the test, so the actual toxicity of it            there may be some special ones, such as the deep dormant seeds
could be reflected by GI. Said-pullicino et al. (2007) enhanced the                 (Derek Bewley, 1997), which still cannot germinate. Therefore,
moisture content of the fresh compost samples to 85% (wet                           the principle of probability and statistics to judge the number of
weight) with deionized water and made aqueous extracts by con-                      germinated seeds in test can reduce the error caused by the special
taction, centrifugation and filtration (see Table 1 for more details).              seeds.
The results showed that the values of GI increased from 12.8% (day                       There are currently three viewpoints on analysis and judgment
0) to 74.7% (day 250). However, the electrical conductivity values                  of the results of the seed germination test. First, GI is widely
of the composting mixture samples were from 5.0 to 7.8 mS cm1,                     adopted because it combines RSG with RRG, both of which can
which implied that the concentrations of soluble salts were in the                  reflect the toxicity of compost (Zucconi et al. (1981); Emino and
level considered being inhibitory for seed germination (Hoekstra                    Warman, 2004). Second, RRG is more sensitive indicator than RSG
et al., 2002). In addition, as seen from Eqs. (4–6), the accuracy of                to the toxicity (Tiquia et al., 1996; Fuentes et al., 2004), so RRG is
GI to evaluate the toxicity of compost could be improved by                         used alone. Third, the toxic level of the compost that inhibits seed
increasing the weight of GI values of different dilutions. Mitelut                  germination is higher than that inhibits radicle elongation, thus
and Popa (2011) prepared compost extract with the fresh sample                      RSG and RRG are used to evaluate the toxicity separately. In other
and distilled water at the ratio of 1:2 (w/v), then it was diluted                  words, if compost inhibits seed germination, it is not necessary
with distilled water to yield 0%, 25%, 50%, 75% and 100% of the ini-                to evaluate the effect of it on radicle elongation; if not, the effect
tial extract (v/v). The global germination index (Eq. (5)), i.e. the                on the radicle needs to be evaluated. Luo et al. (2016) used the
average of GI values of the 50% and 75% of the extracts, was                        indices of SG (Eq. (1)), RRG and GI to determine the profile of the
adopted in their study. The results showed that the index values                    toxicity of pig manure during composting. The results showed that
of the samples were below 80% and the germination percentages                       the RRG values of two species of seeds (radish and cabbage) were
of the extracts (beyond 25% of the initial extract) were almost zero,               significantly and positively correlated, and the SG values of all
which proved to be a high phytotoxicity of the samples. Further-                    seeds were more than 70% (seven germinated seeds of ten seeds
more, the study revealed that the samples significantly inhibited                   per Petri dish), which indicated that compost had no effect on ger-
seed germination (radicle emergence), and let alone radicle elonga-                 mination of the seeds. The third viewpoint on the test is worth
tion. Similarly, according to the test procedure listed in Table 1 and              studying in compost derived from other biowastes.
Eq. (6), the results of Qian et al. (2014) showed that the GI values                     Moreover, time courses of seed germination are usually several
varied from 68% (day 30) to 129% (day 90) in swine manure com-                      days under suitable conditions, which can be morphologically
posting and from 88% (day 30) to 119% (day 90) in dairy manure                      divided into three phases (Fig. 1) that consist of phase I (imbibi-
composting. In addition, the GI values of commercial compost of                     tion), phase II (radicle emergence) and phase III (radicle elonga-
swine manure and dairy manure reached 145% and 126%, respec-                        tion). The uptake of water is the major process of seed
tively. Recently, Young et al. (2016) made the extract concentra-                   germination during the phase I, which could be negatively affected
tions used in the test range from 0.5% to 100% (i.e. 0.5%, 1%, 5%,                  by high salinity of compost. During the phase II, the low molecular
10%, 20%, 40%, 60%, 80% and 100%, v/v) of the raw extract that                      weight organic acids of compost could be the primary inhibitor of
was prepared by mixing a dry sample with deionized water                            radicle emergence after testa rupture. Radicle elongation could be
(1:10, dw/v). They proposed that the two concentrations of com-                     inhibited by NH+4 during the phase III. This speculation partly sup-
post extract (RRG=80% and GI=80%) were both over 100%, which                        ports a viewpoint that seed germination can be used to examine
indicated non-inhibitory effect of compost. This is a new idea to                   the compost with high toxicity and radicle growth can be used to
study the phytotoxicity of compost from the perspective of dose-                    examine the compost with low toxicity (Zucconi et al. (1981);
effect relationships, and it has important guiding significance for                 Tiquia et al., 1996). Further studies are needed to validate the effec-
the comparison between samples with different toxicity degrees.                     tiveness and applicability of this conception in the seed germina-
                                                                                    tion test.
                                                                                    Table 2
3. Is it necessary to improve analysis and judgment methods of                      Binomial probability distribution of the number of germinated seeds with ten seeds
the results of the seed germination test?                                           per Petri dish.a
(P) that represents the viability of the whole selected seeds. Gener- 8 C810 p8 ð1 pÞ2 0.1937
ally, the germination frequency or percentage of one thousand 7 C710 p7 ð1 pÞ3 0.0574
seeds is adopted as P. Assuming a commercial seed lot with the 6 C610 p6 ð1 pÞ4 0.0112
germination percentage of 90% is used to carry out the test with                       5                                   C510 p5 ð1  pÞ5         0.0015
                                                                                       4                                   C410 p4 ð1  pÞ6         0.0001
ten seeds per Petri dish. It is well known that the probability of
                                                                                       3                                   C310 p3 ð1  pÞ7         8.75  10-6
the number of the germinated seeds are subject to binomial distri-
                                                                                       2                                   C210 p2 ð1    pÞ   8    3.64  10-7
bution (Boyle, 2003). Thus, solving for the binomial distribution of
                                                                                       1                                   C110 p1 ð1    pÞ9       9.00  10-9
ten seeds per Petri dish (see Table 2 for more details), results indi-
                                                                                       0                                   C010 p0 ð1    pÞ   10   1.00  10-10
cate that nearly 99% of Petri dishes would contain seven to ten ger-
minated seeds, and there is low probability (<0.0001) of the                          a
                                                                                        Assuming an infinitely large population of seeds where 90% are capable of
germinated seeds less than five in a Petri dish. According to the                   germinating (p = 0.9).
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
                                                              Y. Luo et al. / Waste Management xxx (2017) xxx–xxx                                                               5
Fig. 1. Morphological key processes during the seed germination and seedling growth of Chinese cabbage, a non-endospermic eudicot. The yellow and white fonts represent
the stage where light is and is not required, respectively. The dotted line indicates the top of the dish for placing seeds. The diagram is based on the theories of Derek Bewley
(1997) and Weitbrecht et al. (2011) and the study of Luo et al. (2016).
4. Could there be a species of plant seed to be used as a model                            tivity to environmental pollution and the short-period course
seed for the toxicity evaluation of compost?                                               without photosynthesis. The seed germination test is an effective
                                                                                           and economical bioassay to evaluate the potential toxicity of com-
    The result of the seed germination test is a seed species-                             post before it can be used. Further studies of the determination of
dependent parameter, and cress seed is the most adopted species                            the extraction ratio (e.g. sample to water, dw/v), the application of
in previous studies (Said-pullicino et al., 2007; Zeng et al., 2007;                       the probabilistic theory (e.g. binomial probability), the correlation
Aslam et al., 2008; Pampuro et al., 2010; Khan et al., 2014). How-                         between affecting factors (e.g. salinity, low molecular weight
ever, the range of application of cress seed is proved to be limited,                      organic acids and NH+4) and different stages of seed germination
and there has been a few works to determine whether there exists                           process (imbibition, radicle emergence and radicle elongation),
a species of plant seed that is more sensitive than cress seed to the                      and the selection of model seeds (e.g. Chinese cabbage) in the seed
toxicity of compost. Emino and Warman (2004) compared the GI                               germination test of the compost made from different kinds of feed-
values of mature and immature municipal solid waste compost                                stocks are still required. Moreover, future investigations are
with three groups of the seeds that included the large size (green                         needed to evaluate and correlate the different procedures of the
bean, sweet corn, hybrid cucumber and sunflower), the medium                               seed germination test. Overall, the standardization and improve-
size (broccoli, Chinese cabbage, radish, tomato, amaranthus and                            ment of the test procedure and the modelization of the test seeds
shasta daisy) and the small size (cress, carrot, lettuce and petunia)                      are beneficial to enhancing the validity and reproducibility of the
seeds. They concluded that most of the species, including cress                            seed germination test for evaluating the toxicity of compost.
seed, were not sensitive enough to discriminate between the
mature and the immature compost, while Chinese cabbage seed
was the most sensitive one of these seeds to that. Most impor-                             Acknowledgements
tantly, they firstly proposed a criterion that the model seed would
germinate and grow well in mature compost, whereas the seed                                   This work was supported by the National Natural Science Foun-
would germinate less and grow slowly in immature compost. Ear-                             dation of China [51479072, 51679082, 51521006, 51579094,
lier studies of Chinese cabbage seed in pig manure composting                              51579098, 51508177] and the New Century Excellent Researcher
(Tiquia et al., 1996) and three types of mature compost                                    Award Program [NCET-08-0181] from the Ministry of Education
(Warman, 1999) indicated that Chinese cabbage seed was sensitive                           of China.
to the low level of the toxicity of compost, which confirmed the
conclusion that Chinese cabbage seed met the criterion. Recently,
                                                                                           References
Zhang and Sun (2016) used the germination test of Chinese cab-
bage seed to evaluate the toxicity of compost made from lignocel-                          Alvarenga, P., Mourinha, C., Farto, M., Santos, T., Palma, P., Sengo, J., Morais, M.C.,
lulosic waste. In addition, Chinese cabbage is a subspecies of                                 Cunha-Queda, C., 2015. Sewage sludge, compost and other representative
Brassica rapa (Saeki et al., 2016), and Komatsuna, a variety of Bras-                          organic wastes as agricultural soil amendments: Benefits versus limiting
                                                                                               factors. Waste Manage. 40, 44–52.
sica rapa, is related to Chinese cabbage. The germination test of                          Anand, C.K., Apul, D.S., 2014. Composting toilets as a sustainable alternative to
Komatsuna seed had been widely used in compost (Hase and                                       urban sanitation – a review. Waste Manage. 34, 329–343.
Kawamura, 2012). Chinese cabbage seed has its own advantages                               Aslam, D.N., Horwath, W., VanderGheynst, J.S., 2008. Comparison of several
                                                                                               maturity indicators for estimating phytotoxicity in compost-amended soil.
in terms of the response to toxic substances (sensitive), the germi-                           Waste Manage. 28, 2070–2076.
nation cycle ( 48 h) and the seed size (medium), so it could be                           Aviani, I., Laor, Y., Medina, S., Krassnovsky, A., Raviv, M., 2010. Co-composting of
used as a model organism to investigate the toxicity of compost.                               solid and liquid olive mill wastes: Management aspects and the horticultural
                                                                                               value of the resulting composts. Bioresour. Technol. 101, 6699–6706.
                                                                                           Bernal, M.P., Alburquerque, J.A., Moral, R., 2009. Composting of animal manures and
5. Conclusions and prospects                                                                   chemical criteria for compost maturity assessment. A review. Bioresour.
                                                                                               Technol. 100, 5444–5453.
                                                                                           Boldrin, A., Hartling, K.R., Laugen, M., Christensen, T.H., 2010. Environmental
    Seed germination as the critical initial stage of plant growth has                         inventory modelling of the use of compost and peat in growth media
its own performances against seedling growth, such as the sensi-                               preparation. Resour. Conserv. Recy. 54, 1250–1260.
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
6                                                                   Y. Luo et al. / Waste Management xxx (2017) xxx–xxx
Boyle, T.H., 2003. Influence of seed germination percentage and number of seeds                  Liu, F., Ying, G.G., Tao, R., Zhao, J.L., Yang, J.F., Zhao, L.F., 2009. Effects of six selected
     sown per cell on expected numbers of seedlings in plug trays. Horttechnology                     antibiotics on plant growth and soil microbial and enzymatic activities. Environ.
     13, 689–693.                                                                                     Pollut. 157, 1636–1642.
Cayuela, M.L., Millner, P.D., Meyer, S.L.F., Roig, A., 2008. Potential of olive mill waste       Luo, Y., Yuan, J., Li, G., Li, S., Jiang, T., Tan, J., Xing, W., 2016. Applicability of seed
     and compost as biobased pesticides against weeds, fungi, and nematodes. Sci.                     germination test to evaluation of low C/N compost maturity. J. Agro-Environ.
     Total Environ. 399, 11–18.                                                                       Sci. (in Chinese) 35, 179–185.
Cesaro, A., Belgiorno, V., Guida, M., 2015. Compost from organic solid waste: Quality            Macias, F.A., Castellano, D., Molinillo, J., 2000. Search for a standard phytotoxic
     assessment and European regulations for its sustainable use. Resour. Conserv.                    bioassay for allelochemicals. Selection of standard target species. J. Agr. Food
     Recy. 94, 72–79.                                                                                 Chem. 48, 2512–2521.
Chen, M., Xu, P., Zeng, G., Yang, C., Huang, D., Zhang, J., 2015. Bioremediation of soils        Marambe, B., Ando, T., 1992. Phenolic acids as potential seed germination inhibitors
     contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides,                       inanimal-waste compost. Soil Sci. Plant Nutr. 38, 727–733.
     chlorophenols and heavy metals by composting: applications, microbes and                    Mehta, C.M., Palni, U., Franke-Whittle, I.H., Sharma, A.K., 2014. Compost: Its role,
     future research needs. Biotechnol. Adv. 33, 745–755.                                             mechanism and impact on reducing soil-borne plant diseases. Waste Manage.
Chikae, M., Ikeda, R., Kerman, K., Morita, Y., Tamiya, E., 2006. Estimation of maturity               34, 607–622.
     of compost from food wastes and agro-residues by multiple regression analysis.              Mitelut, A.C., Popa, M.E., 2011. Seed germination bioassay for toxicity evaluation of
     Bioresour. Technol. 97, 1979–1985.                                                               different composting biodegradable materials. Rom. Biotech. Lett. 16, 121–129.
D Hose, T., Cougnon, M., De Vliegher, A., Vandecasteele, B., Viaene, N., Cornelis, W.,           Nikaeen, M., Nafez, A.H., Bina, B., Nabavi, B.F., Hassanzadeh, A., 2015. Respiration
     Van Bockstaele, E., Reheul, D., 2014. The positive relationship between soil                     and enzymatic activities as indicators of stabilization of sewage sludge
     quality and crop production: A case study on the effect of farm compost                          composting. Waste Manage. 39, 104–110.
     application. Appl. Soil Ecol. 75, 189–198.                                                  Pampuro, N., Santoro, E., Cavallo, E., 2010. Evaluation of maturity and fertilizer
Derek Bewley, J., 1997. Seed germination and dormancy. Plant Cell 9, 1055–1066.                       capacity of compost derived from swine solid fraction International Conference
El Fels, L., Hafidi, M., Ouhdouch, Y., 2016. Artemia salina as a new index for                        on Agricultural Engineering-ageng: Towards Environmental Technologies, pp.
     assessment of acute cytotoxicity during co-composting of sewage sludge and                       28.
     lignocellulose waste. Waste Manage. 50, 194–200.                                            Park, J.H., Lamb, D., Paneerselvam, P., Choppala, G., Bolan, N., Chung, J., 2011. Role of
Emino, E.R., Warman, P.R., 2004. Biological assay for compost quality. Compost Sci.                   organic amendments on enhanced bioremediation of heavy metal(loid)
     Util. 12, 342–348.                                                                               contaminated soils. J. Hazard. Mater. 185, 549–574.
Feng, X., Ling, N., Chen, H., Zhu, C., Duan, Y., Peng, C., Yu, G., Ran, W., Shen, Q., Guo, S.,   Qian, X., Shen, G., Wang, Z., Guo, C., Liu, Y., Lei, Z., Zhang, Z., 2014. Co-composting of
     2016. Soil ionomic and enzymatic responses and correlations to fertilizations                    livestock manure with rice straw: Characterization and establishment of
     amended with and without organic fertilizer in long-term experiments. Sci.                       maturity evaluation system. Waste Manage. 34, 530–535.
     Rep. 6, 24559.                                                                              Ramírez, W.A., Domene, X., Andrés, P., Alcañiz, J.M., 2008. Phytotoxic effects of
Fuentes, A., Llorens, M., Saez, J., Aguilar, M.I., Ortuno, J.F., Meseguer, V.F., 2004.                sewage sludge extracts on the germination of three plant species. Ecotoxicology
     Phytotoxicity and heavy metals speciation of stabilised sewage sludges. J.                       17, 834–844.
     Hazard. Mater. 108, 161–169.                                                                Saeki, N., Kawanabe, T., Ying, H., Shimizu, M., Kojima, M., Abe, H., et al., 2016.
Gavilanes-Terán, I., Jara-Samaniego, J., Idrovo-Novillo, J., Bustamante, M.A., Moral,                 Molecular and cellular characteristics of hybrid vigour in a commercial hybrid
     R., Paredes, C., 2016. Windrow composting as horticultural waste management                      of Chinese cabbage. BMC Plant Biol. 16, 1–15.
     strategy – a case study in Ecuador. Waste Manage. 48, 127–134.                              Said-pullicino, D., Erriquens, F., Gigliotti, G.A., 2007. Changes in the chemical
Ge, J., Huang, G., Huang, J., Zeng, J., Han, L., 2016. Particle-scale modeling of methane             characteristics of water-extractable organic matter during composting and
     emission during pig manure/wheat straw aerobic composting. Environ. Sci.                         their influence on compost stability and maturity. Bioresour. Technol. 98, 1822–
     Technol. 50, 4374–4383.                                                                          1831.
Gómez-Brandón, M., Lazcano, C., Domínguez, J., 2008. The evaluation of stability                 Tang, L., Zeng, G., Shen, G., Li, Y., Zhang, Y., Huang, D., 2008. Rapid detection of
     and maturity during the composting of cattle manure. Chemosphere 70, 436–                        picloram in agricultural field samples using a disposable immunomembrane-
     444.                                                                                             based electrochemical sensor. Environ. Sci. Technol. 42, 1207–1212.
Guo, R., Li, G., Jiang, T., Schuchardt, F., Chen, T., Zhao, Y., Shen, Y., 2012. Effect of        Tiquia, S.M., Tam, N.F., Hodgkiss, I.J., 1996. Effects of composting on phytotoxicity of
     aeration rate, C/N ratio and moisture content on the stability and maturity of                   spent pig-manure sawdust litter. Environ. Pollut. 93, 249–256.
     compost. Bioresour. Technol. 112, 171–178.                                                  Warman, P.R., 1999. Evaluation of seed germination and growth tests for assessing
Gwyther, C.L., Williams, A.P., Golyshin, P.N., Edwards-Jones, G., Jones, D.L., 2011. The              compost maturity. Compost Sci. Util. 7, 33–37.
     environmental and biosecurity characteristics of livestock carcass disposal                 Weitbrecht, K., Muller, K., Leubner-Metzger, G., 2011. First off the mark: early seed
     methods: A review. Waste Manage. 31, 767–778.                                                    germination. J. Exp. Bot. 62, 3289–3309.
Hase, T., Kawamura, K., 2012. Evaluating compost maturity with a newly proposed                  Wu, H., Lai, C., Zeng, G., Liang, J., Chen, J., Xu, J., et al., 2016. The interactions of
     index based on a germination test using Komatsuna (Brassica rapa var.                            composting and biochar and their implications for soil amendment and
     peruviridis) seeds. J. Mater. Cycles Waste Manage. 14, 220–227.                                  pollution remediation: a review. Crit. Rev. Biotechnol., 1–11
Hill, G.B., Baldwin, S.A., Vinnerås, B., 2013. Evaluation of Solvita compost stability           Yang, F., Li, G.X., Yang, Q.Y., Luo, W.H., 2013. Effect of bulking agents on maturity
     and maturity tests for assessment of quality of end-products from mixed latrine                  and gaseous emissions during kitchen waste composting. Chemosphere 93,
     style compost toilets. Waste Manage. 33, 1602–1606.                                              1393–1399.
Hoekstra, N.J., Bosker, T., Lantinga, E.A., 2002. Effects of cattle dung from farms with         Young, B.J., Rizzo, P.F., Riera, N.I., Torre, V.D., López, V.A., Molina, C.D., Fernández, F.
     different feeding strategies on germination and initial root growth of cress                     E., Crespo, D.C., Barrena, R., Komilis, D., Sánchez, A., 2016. Development of
     (Lepidium sativum L.). Agr. Ecosyst. Environ. 93, 189–196.                                       phytotoxicity indexes and their correlation with ecotoxicological, stability and
Huang, D., Qin, X., Xu, P., Zeng, G., Peng, Z., Wang, R., Wan, J., Gong, X., Xue, W., 2016.           physicochemical parameters during passive composting of poultry manure.
     Composting of 4-nonylphenol-contaminated river sediment with inocula of                          Waste Manage. 54, 101–109.
     Phanerochaete chrysosporium. Bioresour. Technol. 221, 47–54.                                Yu, D., Sinkkonen, A., Hui, N., Kurola, J.M., Kukkonen, S., Parikka, P., Vestberg, M.,
Kastner, M., Miltner, A., 2016. Application of compost for effective bioremediation                   Romantschuk, M., 2015. Molecular profile of microbiota of Finnish commercial
     of organic contaminants and pollutants in soil. Appl. Microbiol. Biotechnol. 100,                compost suppressive against Pythium disease on cucumber plants. Appl. Soil
     3433–3449.                                                                                       Ecol. 92, 47–53.
Kelessidis, A., Stasinakis, A.S., 2012. Comparative study of the methods used for                Zang, B., Li, S., Michel, F.J., Li, G., Luo, Y., Zhang, D., Li, Y., 2016. Effects of mix ratio,
     treatment and final disposal of sewage sludge in European countries. Waste                       moisture content and aeration rate on sulfur odor emissions during pig manure
     Manage. 32, 1186–1195.                                                                           composting. Waste Manage. 56, 498–505.
Khan, N., Clark, I., Sánchez-Monedero, M.A., Shea, S., Meier, S., Bolan, N., 2014.               Zeng, G., Huang, D., Huang, G., Hu, T., Jiang, X., Feng, C., Chen, Y., Tang, L., Liu, H.,
     Maturity indices in co-composting of chicken manure and sawdust with                             2007. Composting of lead-contaminated solid waste with inocula of white-rot
     biochar. Bioresour. Technol. 168, 245–251.                                                       fungus. Bioresour. Technol. 98, 320–326.
Ko, H.J., Kim, K.Y., Kim, H.T., Kim, C.N., Umeda, M., 2008. Evaluation of maturity               Zhang, L., Jia, Y., Zhang, X., Feng, X., Wu, J., Wang, L., Chen, G., 2016. Wheat straw: An
     parameters and heavy metal contents in composts made from animal manure.                         inefficient substrate for rapid natural lignocellulosic composting. Bioresour.
     Waste Manage. 28, 813–820.                                                                       Technol. 209, 402–406.
Komilis, D., Kanellos, D., 2012. A modified dynamic respiration test to assess                   Zhang, L., Sun, X., 2016. Improving green waste composting by addition of
     compost stability: Effect of sample size and air flowrate. Bioresour. Technol.                   sugarcane bagasse and exhausted grape marc. Bioresour. Technol. 218, 335–
     117, 300–309.                                                                                    343.
Komilis, D.P., 2015. Compost quality: Is research still needed to assess it or do we             Zhang, L., Sun, X., Tian, Y., Gong, X., 2013. Effects of brown sugar and calcium
     have enough knowledge? Waste Manage. 38, 1–2.                                                    superphosphate on the secondary fermentation of green waste. Bioresour.
Liang, J., Li, X., Yu, Z., Zeng, G., Luo, Y., Jiang, L., et al., 2017a. Amorphous MnO2                Technol. 131, 68–75.
     modified biochar derived from aerobically composted swine manure for                        Zucconi, F., Monaco, A., Debertoldi, M., 1981. Biological evaluation of compost
     adsorption of Pb(II) and Cd(II). ACS Sustain. Chem. Eng. 5, 5049–5058.                           maturity. Biocycle 22, 27–29.
Liang, J., Yang, Z., Tang, L., Zeng, G., Yu, M., Li, X., et al., 2017b. Changes in heavy
     metal mobility and availability from contaminated wetland soil remediated
     with combined biochar-compost. Chemosphere 181, 281–288.
Please cite this article in press as: Luo, Y., et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Manage-
ment (2017), https://doi.org/10.1016/j.wasman.2017.09.023
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