Accepted Manuscript

Life cycle assessment of biogas production through anaerobic co-digestion of nopal

cladodes and dairy cow manure

Félix Rafael Ramírez-Arpide, Göksel N. Demirer, Clemente Gallegos-Vázquez,

Guadalupe Hernández-Eugenio, Vinicio Horacio Santoyo-Cortés, Teodoro Espinosa-
Solares
PII: S0959-6526(17)32853-6
DOI: 10.1016/j.jclepro.2017.11.180
Reference: JCLP 11319

To appear in: Journal of Cleaner Production

Received Date: 18 March 2017

Revised Date: 2 November 2017
Accepted Date: 22 November 2017

Please cite this article as: Ramírez-Arpide FéRafael, Demirer GöN, Gallegos-Vázquez C, Hernández-
Eugenio G, Santoyo-Cortés VH, Espinosa-Solares T, Life cycle assessment of biogas production
through anaerobic co-digestion of nopal cladodes and dairy cow manure, Journal of Cleaner Production
(2017), doi: 10.1016/j.jclepro.2017.11.180.

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 ACCEPTED MANUSCRIPT

1 Life cycle assessment of biogas production through anaerobic

2 co-digestion of nopal cladodes and dairy cow manure

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4 Félix Rafael Ramírez-Arpidea, Göksel N. Demirer b, Clemente Gallegos-

5 Vázqueza, Guadalupe Hernández-Eugenioa, Vinicio Horacio Santoyo-

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6 Cortésa, Teodoro Espinosa-Solaresa*

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a
7 Universidad Autónoma Chapingo, Chapingo, Estado de México, 56230,

8 MÉXICO.

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b
9 Middle East Technical University, Inönü Bulvari, 06800, Ankara-

10 TURKEY.
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13 Abstract
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14 Nopal (Opuntia ficus-indica (L.) Mill.) has the ability to grow in climatic
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15 conditions that are adverse for most conventional crops. It can be an

16 alternative for biogas production by co-digestion with dairy cow manure,

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*
Corresponding author.

Address: Departamento de Ingeniería Agroindustrial, Universidad Autónoma Chapingo,

km. 38.5 Carretera México-Texcoco, Chapingo, Estado de México 56230, MÉXICO. Tel.:

+52 (595) 952 1569.

E-mail: t.espinosa.s@taurus.chapingo.mx

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17 the second largest source of greenhouse gas emissions in dairy farms.

18 To evaluate the feasibility of using nopal as a biogas source, the

19 environmental impacts associated with the process need to be

20 quantified. In this study, a life cycle assessment is carried out to

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21 evaluate the environmental impacts and energy balance of biogas

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22 production through co-digestion of nopal cladodes and dairy cow

23 manure. A Baseline and three scenarios that had different farming

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24 systems and digestate storage management strategies were compared.

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25 Cropping system and direct field emission data were experimentally
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26 obtained from two plots using an organic farming system and a

27 conventional farming system; biogas production and yield data were

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28 obtained in a 10-L anaerobic digester. Results indicated that the energy

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29 return on investment for biogas production ranged from 8.1 to 12.4.

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30 Organic farming system decreases the environmental impact by 22.5%

31 in the global warming potential category but increases the acidification

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32 potential and eutrophication potential impact category values by 47.2

33 and 45% respectively, while covering the digestate tank results in a

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34 2.3% reduction in global warming potential and in a 1.7% reduction in

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35 photochemical ozone creation potential. Based on these results, biogas

36 production from nopal cladode and dairy cow manure co-digestion and

37 digestate management offers cleaner energy production since the global

38 warming potential has a lower value than that reported for similar

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39 feedstocks. The use of these two biomasses combines the strengths of a

40 plant that accumulates biomass efficiently and the reduction of

41 greenhouse gas emissions by using one of the main wastes in dairy

42 production.

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43 Keywords: Bioenergy, sustainability, LCA, environmental impacts, cow

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44 manure, Opuntia ficus-indica.

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45 1. Introduction

46 The nopal (Opuntia ficus-indica (L.) Mill.), known as cactus pear or

47
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prickly pear, is cultivated around the world. In the Americas, it is grown
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48 in Mexico, Argentina, Bolivia, Brazil, Chile, Peru and the United States of

49 America; in Africa, nopal can be found in Algeria, Ethiopia, Morocco,

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50 South Africa and Tunisia; in Asia, in Jordan, Lebanon, Syria, the Gulf
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51 countries, Yemen and Israel; in Europe in countries like Italy, Portugal

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52 and Spain; and in Oceania, mainly in Australia (Ochoa and Barbera,

53 2017). In most of these countries, nopal is cultivated for commercial

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54 fodder and forage (Le Houérou, 1996). Cladodes (edible paddles of flat-
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55 stemmed spiny cacti mainly of the Opuntia genus used as vegetables)

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56 (Corrales-Garcia et al., 2004) and the fruits (tuna) (Gallegos-Vazquez

57 and Méndez-Gallegos, 2000) are also cultivated for human consumption.

58 The plant is also used for soil conservation (Le Houérou, 1996) and

59 medicinal purposes (Feugang et al., 2006).

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60 It has been recognized that nopal cladodes (NCs) have potential value

61 for bioenergy production of ethanol, biodiesel or methane (CH4). Kuloyo

62 et al. (2014) suggest that NCs might serve as a second generation

63 feedstock for the production of ethanol. Caballero-Nolasco (2017),

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64 working with NCs and dairy cow manure (DCM) in co-digestion in semi-

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65 continuous 10-L laboratory reactors, reported a CH4 yield of 245.6 mL

66 per g of total solids (TS). This amount was obtained using a 75:25

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67 NCs:DCM ratio under mesophilic conditions. Nopal plants could also be

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68 used in hybrid bioenergy and renewable energy production systems in
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69 an integrated solar photovoltaic-nopal system (Cushman et al., 2015).

70 Zika and Erb (2009) reported that arid and semi-arid areas in the world
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71 cover 15.5 and 22.5 M km2 respectively. The use of crassulacean acid
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72 metabolism (CAM) plants has great potential since they are highly
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73 water-use efficient crops. Since nopal is a CAM plant, it is a suitable

74 option for expanding production into semi-arid marginal lands (Owen et

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75 al., 2016). Cushman et al. (2015) indicated that the area used for

76 growing CAM plants for both biofuel and food purposes could be
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77 expanded by developing drought-tolerant bioenergy feedstocks; these

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78 plants can be grown in an environmentally responsible manner on

79 abandoned agricultural lands where traditional food crops are typically

80 not cultivated. Depending on prevailing social and economic conditions,

81 nopal can be used as food, bioenergy feedstock, or even both. Mason et

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82 al. (2015) reported that up to 5 PW·h can be obtained from CAM plants;

83 this would require between 1 and 3.75 M km2 of available semi-arid

84 land, depending on the yield and biogas production assumptions used.

85 This amount of energy is similar to the 5.1 PW·h of electricity produced

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86 annually in the world using natural gas, and more than 50 % of that

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87 produced by coal (IEA, 2016). CAM plants could help reduce fossil fuel

88 emissions, which in 2010 reached 32 Gt of carbon dioxide (CO2),

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89 accounting for 65 % of world CO2 emissions (IPCC, 2014).

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DCM is the second largest source of greenhouse gas (GHG) emissions
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91 from dairy farms after enteric CH4 ones (Aguirre-Villegas and Larson,

92 2017). Worldwide, mean GHG emissions related to manure management

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93 were 50.9 Mt CO2-eq·a-1 during 2000-2014 (Dangal et al., 2017). Thus,

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94 CH4 production from co-digestion of DCM and NCs could help reduce
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95 GHG emissions; Holly et al. (2017) found that anaerobic digestion (AD)

96 reduces CH4 emissions by up to 25%, compared to untreated manure

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97 slurries.
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98 Life cycle assessment (LCA) has been recently applied to analyze the
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99 environmental impact of energy crops, in particular those used for CH4

100 production such as sorghum and wheat (Pacetti et al., 2015), and maize

101 silage in mono-digestion (Lijó et al., 2014) or in co-digestion with pig

102 slurry (Bacenetti et al., 2013). The above studies found that crop

103 fertilization is a key factor in emission levels. Field emissions are also

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104 influenced by soil type, crop, climatic conditions and agricultural

105 management practices. The experimental evaluation of these factors is

106 not usually included in LCA studies due to financial and time constraints

107 (Brentrup et al., 2000).

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108 The sustainability of using different biomass sources to produce

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109 alternative energies is the subject of continuing debate. Despite this,

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110 different public policies have been enacted in several countries to

111 encourage the production and consumption of different feedstocks. The

112
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NC-DCM combination is a possible alternative for the sustainable
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113 production of CH4 through well-proven AD technology. The use of these

114 two feedstocks combines different strengths: a plant that accumulates

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115 biomass efficiently, and treatment of DCM which allows reducing GHG
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116 emissions. This combination has not been previously studied to

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117 determine whether it actually offers an alternative for cleaner energy

118 production. The aim of the present work is to analyze the environmental
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119 and energy sustainability of the process, and to identify potential

120 opportunities to reduce the environmental impacts resulting from the

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121 use of NCs and DCM as feedstocks. The work is reinforced by the use of
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122 experimental results, such as crop emissions measured on site and

123 methane production quantified in continuous laboratory-scale digesters.

124 Additional data are from the relevant literature, including: fuel

125 consumption and vehicle emissions (INE 2005) and CH4 emissions from

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126 digestate storage (Baldé et al., 2016). Background data were taken

127 from the Ecoinvent database.

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128 2. Materials and methods

129 In order to assess the environmental aspects and potential impacts

130 associated with energy produced by co-digestion of NCs and DCM, LCA

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131 was used. This study follows the LCA framework stipulated by ISO

132 14040 standard (ISO, 2006). LCA consists of the following four steps: a)

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133 goal and scope definitions, b) life cycle inventory, c) life cycle impact

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134 assessment, and d) interpretation. OpenLCA 1.6.3 (GreenDelta, 2017),

135 an open source software for LCA and sustainability assessment, was

136 used for LCA evaluation.

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137 2.1. Goal and scope definitions
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138 The case study was based on biogas production from NC and DCM co-

139 digestion, using a covered lagoon anaerobic digester. The characteristics

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140 of a digester located in “Rancho la Hondonada”, Queretaro, Mexico were

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141 used (Figure 1).

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142
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143 Figure 1. Covered lagoon anaerobic digesters at “Rancho la

144 Hondonada”, Queretaro, Mexico.

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145 The functional unit (FU) was 1 MJ of bioenergy produced. The inputs to
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146 the inventory were detailed according to annual requirements. Input

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147 production and local transportation were also considered within the
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148 system. Material acquisitions and the manufacture and transportation of

149 equipment used in the entire product system were left outside of the
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150 system boundary due to their minimal impact per unit of biogas created
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151 over the lifetime of the equipment (Hijazi et al., 2016). The inputs,

152 emissions and fuel used during crop establishment were not considered

153 based on the same criteria, because, according to previous tests, crop

154 establishment activities contribute less than 1 % of the emissions over

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155 the crop lifespan. Human labor energy was not considered. No allocation

156 was applied in this analysis, as biogas was considered to be the only

157 product. The digestate is frequently used as crop fertilizer either directly

158 or after treatment, so it is considered to be outside of the boundary

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159 system.

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160 2.1.1. Description of the systems under assessment

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161 Baseline and scenarios were defined on the basis of the NC production

162 system used and the way in which the digestate was handled. Two

163
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different NC production systems were studied: i) conventional farming
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164 system (CFS) and ii) organic farming system (OFS); for digestate
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165 storage, two types of tanks were used: a) an open digestate storage

166 (ODS) tank and b) a closed digestate storage (CDS) tank. Nopal cladode
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167 transport (NCT), dairy cow manure transport (DCMT), pre-processing

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168 (PP) and the conversion of the biomass to biogas through AD were

169 considered.
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170 Nopal cladode production: Two different NC production systems were

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171 compared: CFS and OFS. Both systems oriented to biomass energy
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172 production were planted with the Milpa Alta variety at an effective

173 density of 22,988 plants·ha-1. Nopal is a perennial crop with a 20-year

174 lifespan. The first step in crop establishment involved harrowing and

175 plowing the field prior to planting. The nopal was allowed to grow for

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176 one year until reaching its productive stage, during which time DCM was

177 applied as fertilization; pest and disease control were conducted

178 manually. These activities were performed for both NC production

179 systems. The main differences between the two systems occur in the

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180 productive stage, particularly in relation to fertilization and weed and

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181 pest management.

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182 For the CFS, the fertilization source was an inorganic fertilizer compound

183 that provides nitrogen, phosphorus and potassium, based on urea, triple

184
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superphosphate and potassium chloride; weed and pest control were
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185 performed using atrazine and insecticide respectively. For the OFS, the

186 fertilizer source was DCM produced on site; pest control was performed
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187 manually and weed control was carried out both manually and using a
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188 mechanical weed cutter.

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189 In both systems, the harvest was done manually. The cropping area for

190 supplying the anaerobic digester was calculated on the basis of the
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191 digester’s annual NC requirements and annual NC yield volume. It was

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192 determined that 2.8 and 1.7 ha are required for the CFS and OFS
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193 respectively.

194 Pre-processing: After harvest, the NCs were transported from the field

195 site to the anaerobic digester. They were ground and filtered and then

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196 mixed with DCM at a 75:25 (NC:DCM) ratio (w/w); the TS were fixed at

197 3 % using water for dilution. The mixer system included an axial mixer.

198 Anaerobic digestion: The mixture was fed into a 250 m3 anaerobic

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199 digester, which was operated in semi-continuous mode, feeding it once

200 a day. The feed mixture flow was adjusted to achieve a hydraulic

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201 retention time of 30 d. The anaerobic digester was operated under

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202 mesophilic conditions. Fifty percent of the digester liquid was

203 recirculated daily by pumping.

204
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Digestate storage: The digestate generated in the anaerobic digestion
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205 process was discharged and stored in a 120 m3 capacity tank. In this
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206 step two different digestate storage tanks were studied: ODS and CDS.

207 For the ODS, it was assumed that the CH4 produced during the digestate
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208 storage was released into the air, while in the CDS the CH4 produced
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209 was recovered and mixed with the biogas from the anaerobic digestion.
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210 2.1.2. Scenarios

211 Four scenarios were considered in the study; they were differentiated
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212 based on the NC production system (CFS or OFS) and the digestate
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213 storage type (ODS or CDS) used. The four combinations were: Baseline

214 (CFS and ODS), Scenario 1 (OFS and ODS), Scenario 2 (CFS and CDS)

215 and Scenario 3 (OFS and CDS). The system boundaries of the life cycle

216 for each scenario are presented in Figure 2.

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217
218 Figure 2. Scenarios and system boundaries. DCM: dairy cow manure,
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219 CFS: conventional farming system, OFS: organic farming system, NCT:
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220 nopal cladode transport, DCMT: dairy cow manure transport, PP: pre-

221 processing, AD: anaerobic digestion, ODS: open digestate storage, CDS:
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222 closed digestate storage.

223 2.2. Data sources

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224 Data collection and quantification were based on experimental data and

225 complemented with suitable data from the literature and the Ecoinvent

226 database version 3.1 (Wernet et al., 2016). The inputs for NC

227 production were based on data obtained from two sites with different

228 agronomic management, under OFS (Colon, Qro., Mexico) and CFS
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229 (Chapingo, Mex., Mexico). Fuel consumption associated with the

230 transportation of agrochemicals, NCT and DCMT were estimated using

231 data for the selected vehicle obtained from the National Ecology

232 Institute of Mexico (INE, 2005). These data are presented in Table 1.

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233 Table 1. Parameters for fuel consumption and vehicle emissions.

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Vehicle Capacity CO NOX SO2 CH4 N2O CO2 Fuel consumption
kg g·km-1 g·km-1 g·km-1 g·km-1 g·km-1 g·km-1 L·km-1

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LDGT1a 1,700 38 1.1 0.05 0.035 0.236 396 0.1033
HDDV8bb 16,000 22 25 0.3 0.04 0.025 987 0.4144
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234 Light duty gasoline truck 1

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235 Heavy duty diesel vehicle 8b
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236 Source: Authors’ compilation according to INE (2005)

237 It is assumed that NCT and DCMT were by road with a heavy duty diesel
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238 vehicle 8b considering 5.0 and 0.5 km of distance, respectively.

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239 Agrochemicals (including inorganic fertilizers, herbicides and pesticides)

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240 are assumed to be transported 15 km from the local market to the farm

241 using a light duty gasoline truck 1. Additionally, when DCM was a
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242 fertilizer source it was transported 5.0 km from farm to field by

243 HDDV8b.
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244 The biogas production inputs and biogas yield volumes were from data
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245 obtained in a 10-L anaerobic digester, which was operated with the

246 identical technical parameters mentioned above. The electricity

247 consumption for size reduction was estimated by taking the power

248 consumption, time and capacity of the equipment used into

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249 consideration (5.2 kW, 1.1 h and 2,500 kg·h-1 respectively). The energy

250 required for mixing, feeding and recirculating was calculated by an

251 energy balance performed in the covered lagoon anaerobic digester

252 located in “Rancho la Hondonada” (Colon, Qro., Mexico). Energy

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253 requirements for fertilizer, herbicide and pesticide production are from

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254 Ecoinvent database version 3.1 (Wernet et al., 2016).

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255 2.2.1. Emission estimates

256 The emissions associated with agrochemical (fertilizers, pesticides,

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257 herbicides) and fuel production, as well as from electricity production

258 from a mix of power-generating sources were also obtained from

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259 Ecoinvent database version 3.1 (Wernet et al., 2016). Additional data

260 regarding electricity mix by fuel type is presented as Supplementary

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261 Information (SI-1). The emission data due to transportation (Table 1)

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262 were from the National Ecology Institute of Mexico (INE, 2005).
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263 The dinitrogen monoxide (N2O) and CH4 emissions from the soil used for

264 CFS and OFS were experimentally measured using the static chamber
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265 method (Hutchinson and Mosier, 1981), and the results are summarized
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266 in Table 2. Carbon dioxide (CO2) was not taken into consideration

267 because there was no statistical difference with the control as is shown

268 in SI-2. Ammonia (NH3) field emissions and those of the additional

269 nitrogen oxides (NOx) were estimated according to Nemecek and

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270 Schnetzer (2012). The CH4 emissions related to digestate storage were

271 calculated by using the results obtained by Baldé et al. (2016).

272 Table 2. Direct field emissions during nopal cladode production.

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Methane Dinitrogen monoxide
(gCH4·ha-1·a-1) (gN2O·ha-1·a-1)

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Organic farming system 661.5 375.8
Conventional farming system -1,314.60 636

273 2.3. Life cycle inventory

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274 The data for crop characteristics and NC, DCM and digestate

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275 physicochemical characteristics, and CH4 content in biogas are
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276 presented in Table 3. The inputs and outputs of each scenario are

277 detailed in Table 4.

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278 Table 3. Technical crop characteristics and physicochemical parameters

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279 of nopal cladode, dairy cow manure and digestate, and biogas methane
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280 content.

Parameter Units Quantity

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Nopal cladode production

Density plants·ha-1 22,988
Plant Variety Milpa Alta
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Biomass production yield

Conventional farming system kg·ha-1 ·a-1 263,710
kg·ha-1 ·a-1
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Organic farming system 417,130

Nopal cladode
Total solids g·kg-1 70
Volatile solids g·kg-1 56
Dairy cow manure
Total solids g·kg-1 168
Volatile solids g·kg-1 130
Ammonium N % 0.159
Total Carbon % 4.257
Total Nitrogen % 0.400

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Digestate
Total solids g·kg-1 22
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Volatile solids g·kg 0.364
Biogas
Methane content % 60
281 Source: Data obtained experimentally.

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282 Table 4. Material and energy inventory of inputs and outputs (per year).

Parameter Unit Baseline Scenario 1 Scenario 2 Scenario 3

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Inputs
Urea kg·a-1 255.8 255.8
Triple superphosphate kg·a-1 118.3 118.3

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Potassium chloride kg·a-1 184.3 184.3
Dairy cow manure (fertilizer) Mg·a-1 86.85 86.85
Atrazine kg·a-1 16.5 16.5

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Insecticide kg·a-1 16.5 16.5
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Gasoline L·a-1 3.1 3.1
Diesel L·a-1 197.3 222.2 197.3 222.2
Dairy cow manure Mg·a-1 242.02 242.02 242.02 242.02
m3·a-1
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Water 2,073.58 2,073.58 2,073.58 2,073.58

Electricity from the grid MJ·a-1 28271.1 28271.1 28271.1 28271.1
Outputs
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Biogas m3·a-1 30,068.88 30,068.88 30,068.88 30,068.88

Digestate Mg·a-1 3,034.41 3,034.41 3,034.41 3,034.41
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283 2.4. Life cycle impact assessment

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284 Environmental performances of the systems under consideration are

285 compared at midpoint level using the CML baseline 2001 impact
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286 assessment method (Guinée et al., 2001). At midpoint level, CML

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287 baseline uses the following 10 impact categories: global warming

288 potential (GWP) expressed as CO2 equivalents, acidification potential

289 (AP) expressed as sulfur dioxide equivalents (SO2-eq), eutrophication

290 potential (EP) expressed as phosphate equivalent (PO4-eq), abiotic

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291 depletion potential (ADP) expressed as antimony equivalent (Sb-eq), ,

292 ozone layer depletion potential (ODP) expressed as

293 trichlorofluoromethane equivalent (CFC-11-eq), photochemical ozone

294 creation potential (POCP) expressed as ethylene equivalent (C2H4),

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295 terrestrial ecotoxicity potential (TETP) expressed as 1,4-dichlorobenzene

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296 equivalent (DCB-eq), marine aquatic ecotoxicity potential (MAETP) in

297 DCB-eq, freshwater aquatic ecotoxicity potential (FAETP) in DCB-eq and

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298 human toxicity potential (HTP) in DCB-eq. For assessing the

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299 environmental impacts, OpenLCA v1.6.3 software was used.
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300 2.5. Energy balance
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301 The energy balance is reported in terms of the energy return on

302 investment (EROI), a concept which was developed by Hall et al.

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303 (2009). This approach indicates the energy efficiency of a process and is
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304 calculated as shown in Equation 1. When the EROI of a resource is

305 greater than one it can be classified as a net energy producer, whereas
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306 when the EROI is equal to or less than one, the resource is a net energy
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307 consumer. The calorific values related to diesel, gasoline and CH4 are
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308 calculated based on the lower heating value, obtained from Edwards et

309 al. (2013).


     (1)

 =
    

310 3. Results and discussion

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311 3.1. Energy analysis

312 The energy efficiency results of the different scenarios, assessed using

313 EROI, are presented in Figure 3; it also shows the values of the

314 reference systems reported in the literature for macroalgae (Aitken et

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315 al., 2014), straw-cow manure (Pierie et al., 2015) and human feces-

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316 corn straw (Wu et al., 2016) used as feedstocks. EROI theoretically

317 needs to be at least greater than one, although a value of three is

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318 recommended as a minimum for a process to be considered

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319 energetically sustainable (Hall et al., 2009), since below this level the
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320 energy efficiency becomes questionable. The Baseline EROI was 8.14,

321 while the three scenarios had EROI values ranging from 9.48 to 12.41,
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322 all of them above three. The three scenarios also presented better

323 energy performance than the Baseline. The change in NC production

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324 from CFS to OFS enhanced the EROI by 49 %, whereas the

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325 incorporation of CDS (Scenario 2) increased the EROI by only 16.5 %.

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326 Scenario 3 had an EROI 53 % greater than the Baseline, having the

327 positive effect of Scenario 1 and Scenario 2.

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328 In the three reference systems obtained from the literature, two of them
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329 (biogas through anaerobic digestion of macroalgae, and biogas from co-

330 digestion of human feces-corn straw) had an EROI below the

331 recommended minimum, whereas all four scenarios in our study were

332 above the minimum level. Scenario 1 and Scenario 3 provided an EROI

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333 higher than the value of the biogas produced from straw-cow manure

334 co-digestion, which was 10.9.

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335
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336 Figure 3. Energy return on investment (EROI) values for the Baseline,
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337 the different scenarios and the references from the literature (Note 1 -
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338 reference values plotted correspond to the best result of each study).

339 Source: 1Aitken et al. (2014), 2Pierie et al. (2015) and 3Wu et al.
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340 (2016). (Note 2 – the EROI plotted for human feces-corn straw was

341 calculated from scenario 3 of the referenced study, without considering

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342 biogas upgrading and waste management and using the low heat value
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343 reported by Edwards et al. (2013)).

344 The cumulative energy demand (CED) of the different scenarios was

345 calculated based on the FU selected. The specific CED distribution of

346 these scenarios is presented in Figure 4. The contribution of CH4,

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347 considered as additional energy recovered from digestate storage, is

348 also displayed. Figure 4 shows that DCMT has the lowest energy

349 consumption in the Baseline and the three scenarios. The Baseline and

350 CFS have the highest specific energy consumption (52 %), compared to

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351 the 29 % recorded for OFS. This difference is mainly due to the

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352 displacement of energy consumption during the production of

353 agrochemicals, mainly inorganic fertilizer, which accounted for 86 % of

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354 the CFS´s CED.

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NCT is the second largest contributor to CED in all scenarios, accounting
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356 for between 19 to 28 % of the total. The CH4 recovered as a result of

357 covering the digested storage brought about a 1.7 % increase in the
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358 energy produced, which is equivalent to the energy required for the
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359 recirculation process.

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360

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361
362 Figure 4. Contribution of each process to the cumulative energy

363 demand (CED) per functional unit. CFS: conventional farming system,

364 OFS: organic farming system, NCT: nopal cladode transport, DCMT:

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365 dairy cow manure transport, PP: pre-processing, AD: anaerobic

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366 digestion.

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367 3.2. Environmental performance

368 Table 5 shows the total life cycle impact assessment results for the

369
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Baseline and the three scenarios, while Figure 5 includes the
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370 contribution of each process to the system. The results show that the

371 main difference is related to NC production, while digestate

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372 management does not have an important role in most of the impact
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373 categories. The results are discussed below by impact category, focusing
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374 on the comparison between the Baseline and Scenario 1. GWP and POCP

375 impact categories were slightly influenced by digestate storage type.

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376 Table 5. Life cycle impact assessment results.

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GWP AP EP ADP ODP POCP TETP MAETP FAETP HTP

kg CO2- kg SO2- kg PO4- kg CFC-11- kg C2H4- kg DCB kg DCB kg DCB kg DCB
eq·MJ-1 eq·MJ-1 eq·MJ-1 kg Sb-eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1

Baseline 7.65E-03 8.62E-05 1.75E-05 2.86E-08 1.09E-09 2.49E-06 4.20E-05 5.00E+00 1.15E-03 2.75E-03

Scenario 1 5.93E-03 1.27E-04 2.54E-05 7.58E-10 5.78E-10 1.93E-06 2.20E-05 2.74E+00 6.57E-04 1.36E-03

Scenario 2 7.47E-03 8.61E-05 1.75E-05 2.86E-08 1.09E-09 2.44E-06 4.20E-05 4.99E+00 1.15E-03 2.75E-03

Scenario 3 5.75E-03 1.27E-04 2.54E-05 7.57E-10 5.77E-10 1.89E-06 2.20E-05 2.74E+00 6.57E-04 1.36E-03

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C EP
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377 Figure 5. Impact of the biogas production system on the Baseline and

378 the scenarios. Impact categories: a) global warming potential (GWP), b)

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379 acidification potential (AP), c) eutrophication potential (EP), d) abiotic

380 depletion potential (ADP), e) ozone layer depletion potential (ODP), f)

381 photochemical ozone creation potential (POCP), g) terrestrial ecotoxicity

382 potential (TETP), h) marine aquatic ecotoxicity potential (MAETP), i)

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383 freshwater aquatic ecotoxicity potential (FAETP), j) human toxicity

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384 potential (HTP). The stacks represent different phases in the production

385 process.

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386 3.2.1. Global warming potential

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387 As shown in Table 5, all scenarios analyzed can provide a reduction in

388 the GWP category compared to the Baseline. The main influence on the
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389 reduction was the use of DCM instead of inorganic fertilizers. Regardless

390 of the type of fertilizer, covering the digestate storage tank contributed
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391 to reducing the GWP. Biogas production with OFS can prevent the
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392 emission of 1.72 g CO2-eq·MJ-1, which corresponds to a 22.5% GWP

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393 reduction, while covering the digestate tank resulted in a 2.26%

394 decrease. The combined effect of OFS and CDS resulted in a 24.8%
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395 reduction compared to the Baseline.

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396 Figure 5a shows the distribution of GWP by processes. The AD was the

397 major contributor, generating from 37.8% to 50.3% of total GWP. This

398 contribution was directly associated with the electricity consumption,

399 mainly due to the pump used to recirculate the digester liquid. When the

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400 PP is considered, the GWP caused by the use of electricity increases

401 from 63.2 to 83.9%. These results agree with those of Collet et al.

402 (2011), who report that the environmental impacts generated by the

403 production of CH4 from microalgae are strongly correlated to the

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404 electricity consumption involved. The impact on the GWP category

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405 related to the production and use of electricity accounted for 65 % of

406 the whole process. Van Stappen et al. (2016) suggest that these

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407 impacts could be reduced through electricity generation from biogas.

408 3.2.2.
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Acidification potential
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409 In contrast to GWP, the use of CFS to produce NC was the most
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410 favorable in terms of AP. The results (Table 5) show that the

411 substitution of inorganic fertilizer by DCM (Scenario 1) caused an

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412 increase of 40.7 mg SO2-eq·MJ-1, or 47.2% compared to the Baseline.

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413 This may be mainly due to the association of high NH3 field emissions
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414 with the use of manure. According to Sommer and Hutchings (2001),

415 field applied manure contributes significantly to the emission of NH3

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416 from agriculture; one way of reducing these emissions is by rapidly

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417 incorporating the manure into the soil (Webb et al., 2010).

418 High power grid usage resulting from those processes requiring

419 electricity also contributes significantly to acidification potential (Figure

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420 5b). In relation to biomass transportation, NCT emitted 7.1 mg SO2-

421 eq·MJ-1 in all scenarios, while DCMT emitted 0.25 mg SO2-eq·MJ-1.

422 3.2.3. Eutrophication potential

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423 For EP, the Baseline had the best performance in this category; by

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424 contrast, Scenario 1 showed an increase of 45% above the Baseline

425 caused by the fertilizer source substitution (Table 5). The different

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426 contribution processes (Figure 5c) indicated that NC production was the

427 highest contributor to EP through NH3 field emissions, which represented

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428 between 60.3% and 72.7% of the total EP in the whole process.

429 Since the use of OFS to produce NC in this study had the lowest GWP,
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430 but the highest AP and EP, it is necessary to search for alternatives
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431 aimed at reducing NH3 emissions. Sommer and Hutchings (2001)

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432 suggest that manure be incorporated into the soil immediately after its

433 application. Webb et al. (2010) recommend injecting the slurry to

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434 depths which increase the diffusion path to the soil surface: this leads to

435 most of the denitrified nitrogen (N) being emitted as nitrogen gas (N2)
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436 to avoid increasing N2O emissions.

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437 3.2.4. Abiotic depletion potential

438 ADP was the impact category with the greatest difference between the

439 Baseline and Scenario 1. According to the results shown in Table 5, the

440 Scenario 1 ADP value was just 2.7 % of the corresponding Baseline

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441 value. CFS was the major process contributor in the Baseline (Figure

442 5d). These results have a similar magnitude order to the ones reported

443 by Ribal et al. (2017); these authors investigated two citrus farming

444 systems, one organic and one conventional. They found that the organic

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445 farming system ADP value was only 1.7 % of the corresponding

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446 conventional production value.

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447 3.2.5. Ozone layer depletion potential

448 The estimated ODP of 1.09E-09 kg CFC-11-eq·MJ-1 in the Baseline was

449
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mainly caused by CFS, AD, PP and NCT, which contributed 48.6%,
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450 24.4%, 16.3% and 10.3%, respectively (Figure 5e), while, AD, PP and
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451 NCT contributed 46.2%, 30.9% and 19.4%, respectively, in Scenario 1.

452 3.2.6. Photochemical ozone creation potential

D
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453 The total POCP from the Baseline was an estimated 2.49E-06 kg C2H4-

454 eq·MJ-1 (Table 5). The behavior was similar to GWP; the substitution of
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455 CFS for OFS resulted in a 22.5% reduction (Scenario 1), while CDS

456 helped reduce the GWP by 1.7% (Scenario 2). The combined effect of
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457 OFS and CDS resulted in a 24.1% reduction compared to the Baseline
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458 (Figure 5f).

459 3.2.7. Toxicity and Ecotoxicity potential

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460 The TETP, MAETP, FAETP and HTP impact categories had similar

461 patterns. As mentioned before, these categories were not influenced by

462 digestate management; consequently, the analysis of each category was

463 made by comparing only the Baseline and Scenario 1 to avoid repetition.

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464 In general, Scenario 1 had a lower potential than the Baseline (Table

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465 5). The difference between the Baseline and Scenario 1 was due to the

466 use of agrochemicals in CFS.

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467 TETP results for process contributor are illustrated in Figure 6g. The

468
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results show that 48% was due to CFS in the Baseline, while only 0.4%
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469 in Scenario 1 was contributed by OFS. According to Lansche and Müller

470 (2017), the production of mineral fertilizers causes several emissions

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471 that contribute to TETP. PP and AD processes also had an important

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472 role. They emitted 8.57x10-6 and 12.8x10-6 kg DCB-eq·MJ-1,

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473 respectively, which together accounted for 51% of the TETP in the

474 Baseline and 96.8% in the Scenario 1.

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475 The MAETP impact category in the Baseline, shown in Table 5, had a
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476 value of 4.9 kg DCB-eq·MJ-1, of which 45.3% was caused by CFS, 21.4%
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477 by PP and 32% by AD, whereas the other processes contributed less

478 than 1.5% (Figure 6h). For Scenario 1 the main contributor processes

479 were PP and AD, which were responsible in this category for 39.2% and

480 58.5%, respectively.

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481 Regarding FAETP, in all cases, PP and AD processes generated 2.58 x

482 10-4 and 3.85x10-4 kg DCB-eq·MJ-1, respectively (Figure 6i). For this

483 category, CFS, included in the Baseline, was responsible in this category

484 for 43% of the impact. This result is lower than the one reported by

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485 Boulamanti et al. (2013). These authors, working on biogas production

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486 from maize, found that crop production accounts for more than 95% of

487 FAETP.

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488 Finally, for HTP the total values are given in Table 5, whereas Figure

489
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6j presents the contribution by process. According to the results, the
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490 potential for PP was 5.21x10-4 kg DCB-eq·MJ-1, while the potential for

491 AD was 7.78x10-4 kg DCB-eq·MJ-1. CFS in the Baseline emitted 14x10-4

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492 kg DCB-eq·MJ-1 while OFS generated less than 1% of the CFS level.
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493 3.3. Comparison of impact categories

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494 Several LCA studies on biogas production systems have been conducted
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495 throughout the world (Hijazi et al., 2016). Comparing the results of the

496 present study with those in the literature is not easy (Fusi et al., 2016),
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497 because the goals, scope, life cycle impact assessment methodology,
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498 feedstock and geographical regions of those studies vary widely

499 (Bacenetti et al., 2016). Consequently, only the biogas-generated

500 environmental impact results of the present study can be compared to

501 those obtained in other studies using different feedstocks, including:

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502 distiller’s waste, rapeseed cake, whey permeate, fodder milk, bakery

503 residues (Tufvesson et al., 2013), sugar beets-tops-leaves, ley crops,

504 maize, organic household waste, food industry waste, liquid manure

505 (Börjesson et al., 2010) and maize silage-rye silage-liquid manure

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506 (Hahn et al., 2015). Figure 6 shows a summary of these studies.

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C EP

507
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508 Figure 6. Comparison of the impact category results of this study with

509 those of different LCA studies. DW: distiller's waste, RC: rapeseed cake,

510 WP: whey permeate, FM: fodder milk, BR: bakery residues, SB: sugar

511 beets, LC: ley crops, OHW: organic household waste, FIW: food industry

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512 waste, LM: liquid manure, MS: maize silage, RS: rye silage. Source: *

513 Tufvesson et al. (2013), ** Börjesson et al. (2010), *** Hahn et al.

514 (2015).

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515 Figure 6 shows that the GWP results obtained for the systems analyzed

516 in this study were between 15% and 50% lower than those recorded for

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517 the residues used in the above-mentioned studies. When the GWP

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518 obtained in this study is compared with the values recorded in studies

519 where energy crops were used as feedstock, the values were 62-75%

520
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lower. This can be explained mainly by a higher annual NC yield per
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521 hectare compared to the other energy crops.
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522 The AP values estimated in this study using CFS were similar to those in

523 most of the studies used for comparative purposes (Figure 6). When
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524 OFS was used instead of CFS, the AP values were only surpassed by the
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525 value reported by Hahn et al. (2015), who, using maize silage with rye

526 silage and liquid manure as feedstock, obtained a value 650% higher
EP

527 than that reported for the worst scenario in this study.
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528 Regarding EP, the comparison results are shown in Figure 6. The EP
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529 values for this study were comparable to those obtained using residues

530 as feedstock. The EP values for biogas production using energy crops as

531 feedstock were 190% to 568% higher than the value for the worst

532 scenario in this study.

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533 3.4. Sensitivity analysis

534 Previous LCA studies have shown that there are several parameters that

535 lead to uncertainty when they are performed. Since this study is based

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536 on experimental data, this uncertainty can be assumed to be low under

537 the conditions studied (Börjesson et al., 2015). Like other energy crops,

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538 biomass yield depends on orchard design (plant density), cultural

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539 practices, cultivar fertility and environmental conditions; this last-

540 mentioned factor is an external variable that can lead to an increase or

541
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decrease in biomass yield. Nopal is a perennial crop, so its biomass yield
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542 depends on plant age and stage of growth. Nopal plants begin to yield
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543 2-3 years after planting; they reach their maximum potential 6-8 years

544 after planting and remain productive for 25-30 years and even longer.
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545 The sensitivity analysis was carried out to determine the influence of
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546 biomass yield on the impact categories. The alternatives “high NC yield”
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547 and “low NC yield” were based on subtracting and adding 50% of

548 current NC yield data shown in Table 3. The results in Table 6 show
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549 that the “high NC yield” alternative had a lower influence on the impact
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550 categories than the “low NC yield”. The results also show that the

551 overall effect on the environmental impacts was smaller, for most

552 impacts, in scenarios using OFS than CFS, except for AP and EP.

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553 Compared to the original values previously presented in Table 5, the

554 GWP was between 2 and 9% lower considering “high NC yield” and 5 to

555 7% higher considering “low NC yield”. The AP, estimated for "high NC

556 yield”, was 17 to 22% lower and 51 to 66% higher with “low NC yield”.

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557 The eutrophication potential was 20 to 24% lower with the “high NC

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558 yield” alternative and 60 to 73% higher with the “low NC yield”

559 alternative. In the other categories, the effect of NC yield was less than

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560 1% in scenarios with OFS, while in scenarios with CFS the effect of NC

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561 yield, either high or low yield, was more than 15%.
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562 Table 6. Sensitivity analysis results for the biomass production yield
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GWP AP EP ADP ODP POCP TETP MAETP FAETP HTP

kg CO2- kg SO2- kg PO4- kg Sb- kg CFC-11- kg C2H4- kg DCB- kg DCB- kg DCB- kg DCB-
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eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1 eq·MJ-1
High NC yield
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Baseline 6.97E-03 7.19E-05 1.40E-05 1.93E-08 9.15E-10 2.28E-06 3.53E-05 4.24E+00 9.90E-04 2.28E-03
Scenario 1 5.82E-03 9.91E-05 1.92E-05 7.55E-10 5.72E-10 1.91E-06 2.20E-05 2.73E+00 6.60E-04 1.36E-03
Scenario 2 6.80E-03 7.19E-05 1.40E-05 1.93E-08 9.15E-10 2.24E-06 3.53E-05 4.24E+00 9.90E-04 2.28E-03
Scenario 3 5.65E-03 9.90E-05 1.92E-05 7.55E-10 5.72E-10 1.87E-06 2.20E-05 2.73E+00 6.60E-04 1.36E-03
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Low NC yield
Baseline 9.68E-03 1.30E-04 2.80E-05 5.65E-08 1.62E-09 3.10E-06 6.20E-05 7.26E+00 1.65E-03 4.14E-03
Scenario 1 6.24E-03 2.10E-04 4.39E-05 7.66E-10 5.94E-10 1.98E-06 2.21E-05 2.75E+00 6.60E-04 1.38E-03
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Scenario 2 9.51E-03 1.30E-04 2.80E-05 5.64E-08 1.62E-09 3.05E-06 6.20E-05 7.26E+00 1.65E-03 4.14E-03
Scenario 3 6.07E-03 2.10E-04 4.38E-05 7.66E-10 5.94E-10 1.94E-06 2.21E-05 2.74E+00 6.60E-04 1.38E-03
563 variation on the impact categories.
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564

565 4. Conclusions

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566 It has been shown that co-digestion of NC and DCM for biogas

567 production was energetically sustainable; the EROI for the Baseline and

568 the three considered scenarios was above the recommended minimum

569 value (3.0).

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570 The NC production under a CFS was the main contribution process in

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571 most of the impact categories analyzed. The substitution of CFS by OFS

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572 to produce the NC led to environmental impact reduction, except in AP

573 and EP categories. In this context, extending this study in terms of

574
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analyzing different fertilizing sources will help elucidate the best practice
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575 to avoid negatively affecting the AP and EP impact categories; one

576 option could be the use of digestate instead of DCM or inorganic

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577 fertilization. The electricity demand in the systems analyzed also played
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578 an important role in the environmental performance, which was

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579 responsible for 28%, in scenarios with CFS, up to 97%, in scenarios with

580 OFS, of the different impact categories analyzed. In reference to the

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581 digestate management, this had a relatively slight impact, less than 3%,

582 on GWP and POCP, but the methane recovered was comparable to the
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583 energy required by the recirculation of the digester liquid in the

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584 anaerobic digestion process.

585 Biogas production from NC-DCM co-digestion and digestate

586 management offers cleaner energy production since the GWP had a

587 lower value than that reported for similar feedstocks and similar. Thus,

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588 the use of these two biomasses combines the strengths of a plant that

589 accumulates biomass efficiently and a treatment system that reduces

590 GHG emissions by using one of the main wastes in dairy production.

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591 Acknowledgments

592 The authors gratefully acknowledge the funding support provided by

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593 both the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y

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594 Alimentación (Mexico) and the Consejo Nacional de Ciencia y Tecnología

595 (CONACYT, Mexico) for the project entitled “Technical and financial

596
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feasibility of using nopal for the production of methane, ethanol and
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597 coproducts” (Project 2012-08-195157). The authors are also grateful to
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598 CONACYT for the financial support granted to Ramírez-Arpide through its

599 scholarship program (grant #244950) and the Universidad Autónoma

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600 Chapingo. Authors express their gratitude to Bioprocess Laboratory for

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601 the discussion of the manuscript and to Carlos de la Cruz-Ramírez for

602 his help in designing the figures.

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603 5. References
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Highlights

• Life cycle assessment for co-digestion of nopal cladodes and dairy

cow manure.
• Biogas production is energetically sustainable.

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• Close digestate storage reduces the global warming potential.
• The farming system strongly influences environmental
sustainability.

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