Greenhouse gas (GHG) production, as a cause of climate change, is considered as one of the biggest problems society is currently facing. The livestock sector is one of the large contributors of anthropogenic GHG emissions. Also, large amounts of ammonia (NH3), leading to soil nitrification and acidification, are produced by livestock. Therefore other sources of animal protein, like edible insects, are currently being considered.
An experiment was conducted to quantify production of carbon dioxide (CO2) and average daily gain (ADG) as a measure of feed conversion efficiency, and to quantify the production of the greenhouse gases methane (CH4) and nitrous oxide (N2O) as well as NH3 by five insect species of which the first three are considered edible: Tenebrio molitor, Acheta domesticus, Locusta migratoria, Pachnoda marginata, and Blaptica dubia. Large differences were found among the species regarding their production of CO2 and GHGs. The insects in this study had a higher relative growth rate and emitted comparable or lower amounts of GHG than described in literature for pigs and much lower amounts of GHG than cattle. The same was true for CO2 production per kg of metabolic weight and per kg of mass gain. Furthermore, also the production of NH3 by insects was lower than for conventional livestock.
This study therefore indicates that insects could serve as a more environmentally friendly alternative for the production of animal protein with respect to GHG and NH3 emissions. The results of this study can be used as basic information to compare the production of insects with conventional livestock by means of a life cycle analysis.
Citation: Oonincx DGAB, van Itterbeeck J, Heetkamp MJW, van den Brand H, van Loon JJA, van Huis A (2010) An Exploration on Greenhouse Gas and Ammonia Production by Insect Species Suitable for Animal or Human Consumption. PLoS ONE 5(12): e14445. https://doi.org/10.1371/journal.pone.0014445
Editor: Immo A. Hansen, New Mexico State University, United States of America
Received: July 16, 2010; Accepted: November 29, 2010; Published: December 29, 2010
Copyright: © 2010 Oonincx et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was directly funded by Wageningen University, Wageningen, The Netherlands (www.wur.nl) as part of a PhD program. Wageningen University had no other role in study design, data collection and analysis, decision to publish, or preparation of the manuscript, than can be expected with the academic supervision of a PhD candidate.
Competing interests: The authors have declared that no competing interests exist.
Production of greenhouse gasses (GHG) is considered as an important cause of climate change , . The most important GHGs are carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O). Since the end of the 18th century the atmospheric carbon-dioxide concentration has increased by 30% and CH4 concentrations by 50% . CH4 and N2O have considerably greater global warming potentials (GWPs) than CO2. By assigning CO2 a value of 1 GWP, the warming potentials of these other gases can be expressed on a CO2-equivalent basis: CH4 has a GWP of 25, and N2O has a GWP of 298 . The relative contribution of CO2 equivalents (CO2 eq.) of the livestock sector is large, amounting up to 18% of total anthropogenic GHG emissions . Based on a Life Cycle Analysis (LCA) that takes the entire production process of animal products into account, the global contribution to GHG emissions by the animal sector are: 9% for CO2 (fertilizer production for feed crops, on-farm energy expenditures, feed transport, animal product processing, animal transport, and land use changes), 35–40% for CH4 (enteric fermentation in ruminants and from farm animal manure) and 65% for N2O (farm manure and urine) . Direct CO2 production through respiration is not relevant when determining the impact of GHGs as respiration by livestock is not considered a net source of CO2 . The respired carbon, which comes from the feed, was first taken up from CO2 in the air and stored in an organic compound during the production of the feed. However, the ratio between body growth realised and CO2 production is an indicator of feed conversion efficiency and thereby a relevant indicator for the environmental impact .
Livestock is also associated with environmental pollution due to ammonia (NH3) emissions from manure and urine, leading to nitrification and acidification of soil . Although not considered a GHG, NH3 can indirectly contribute to N2O emission , as conversion takes place by specialized soil bacteria . Livestock is estimated to be responsible for 64% of all anthropogenic NH3 emissions . The main source of gaseous NH3 is bacterial fermentation of uric acid in poultry manure ,  and bacterial fermentation of urea in mammals . Besides these environmental problems the livestock sector faces challenges regarding resistance to antibiotics, zoonosis and animal welfare .
All these problems together illustrate the need to find alternatives for conventional sources of animal protein. Mini-livestock, for instance edible insects, have been suggested as an alternative source of animal protein . Production of animal protein in the form of edible insects supposedly has a lower environmental impact than conventional livestock , , . When evaluating the total environmental impact of animal protein production, a LCA, in which all production factors are taken into account, is needed. Differences in environmental impact in a LCA can be explained mainly by three factors: enteric CH4 emissions, feed conversion efficiencies and reproduction rates .
Before performing a LCA, it is necessary to know the GHG production by edible insects. This information is lacking in literature. Therefore, in this study we experimentally quantified the direct production of the GHGs CH4 and N2O for five insect species. CO2 production and average daily gain (ADG) were quantified to provide an estimation of feed conversion efficiency. Additionally, NH3 emissions were quantified. The results of this study represent a quantification of the insect physiological contribution to GHG production by insects and can in turn be used to create a LCA for insect-derived products.
Materials and Methods
2.1 Animals and housing
Five insect species were studied: fifth larval stage mealworms Tenebrio molitor L. (Coleoptera: Tenebrionidae), fifth and sixth nymphal stage house crickets Acheta domesticus (L.) (Orthoptera: Gryllidae), third and fourth stage nymphs of migratory locusts Locusta migratoria (L.) (Orthoptera: Acrididae), third larval stage sun beetles Pachnoda marginata Drury (Coleoptera; Scarabaeidae) and a mix of all stages of the Argentinean cockroach Blaptica dubia (Serville) (Dictyoptera: Blaberidae). Currently, T. molitor, A. domesticus and L. migratoria are considered edible, while P. marginata and B. dubia are not. The latter two species were included since they are a potential source of animal protein, for instance by means of protein extraction. These two species can be bred in large numbers with little time investment and are able to utilise a wide range of substrates as feed , .
Per species three to six repetitions were conducted each for a period of three days. Animals were housed per species in two cages or containers per respiration chamber. These containers were placed in one of two, identical, open circuit climate respiration chambers measuring 80*50*45 cm, with a total volume of 265 L . Within these climate respiration chambers, T. molitor and P. marginata were housed in two stacked plastic containers (50*30*8.7 cm). The three other species were housed in metal wire cages (45*37.5*41 cm; mesh width 1 mm) with a glass cover plate. To increase surface area for A. domesticus and B. dubia, hollow plastic tubes (20 cm long and 3 cm in diameter), were stacked to a height of 30 cm in the wired cages, while for L. migratoria, two V-shaped-folded metal screens (70*15 cm) were entered per cage. Humidity, temperature, and day length were based on rearing conditions used by commercial insect rearing companies (Table 1). All animal masses reported are averages of fresh mass per cage. The starting and final animal mass per cage are provided in Table 1.
Food was provided for each species at the beginning of each repetition, except when mentioned otherwise.
Tenebrio molitor larvae were reared in 300 g mixed grain substrate (wheat, wheat bran, oats, soy, rye and corn, supplemented with beer yeast) with on top pieces of carrot (±15*2 cm) weighing a total average of 637 g per repetition.
Acheta domesticus was provided with chicken mash (501 g) with carrot pieces (784 g) on top for each repetition.
Locusta migratoria was provided with wheat bran (70 g; Arie Blok Animal Nutrition, Woerden, The Netherlands) in a metal bowl at the beginning of each repetition. Fresh Perennial ryegrass (Lolium perenne) was provided daily (463 g in three days). The grass was grown by Unifarm, Wageningen University and Research centre, Wageningen, The Netherlands.
P. marginata larvae were kept in a peat moss substrate (2.0 kg per respiration chamber) in which chicken mash (285 g) was mixed at the beginning of each three-day repetition. Pieces of carrot (±15*2 cm) with an average total mass of 161 g per repetition were put on top of the substrate.
B. dubia was provided with a chicken mash diet (199 g) and carrots (559 g), fresh carrot being added during the repetitions.
Peat moss, chicken mash, and carrots, offered to A. domesticus, P. marginata and B. dubia were provided by Kreca V.O.F, Ermelo, The Netherlands. The carrots and mixed grains substrate offered to T. molitor were provided by Insectra, Deurne, The Netherlands.
2.3 Gas measurements
During the experiment concentrations of CO2 and CH4 were measured every 9 min in the ingoing and outgoing air stream of the respiration chambers. The difference in CO2 and CH4 concentrations between ingoing and outgoing air thus represents the total production of CO2 and CH4 of insects, feed, and substrate. The exact air volumes were measured with a calibrated Schlumberger G1.6 dry gas meter and corrected for measured air temperature and pressure. CO2 and CH4 concentrations were measured in dried gas. Gas was dried in a +2°C dew-point cooler. Nondispersive infrared analyzers were used to measure CO2 (type Uras 3G, Hartmann and Braun, Frankfurt, Germany) and CH4 (type Uras 10E, Hartmann and Braun, Frankfurt, Germany). The refreshed air volume was set so that CO2 levels did not exceed 1%. From each climate respiration chamber, as well as from the incoming air, an air sample was taken for N2O analysis after 24, 48, and 72 h with a 60 ml syringe. The syringes were sealed by a shutoff valve and stored at 20°C until analysis (within 48 h). The N2O concentration was analysed by a gas chromatograph (CE instruments GC8000 Top, Interscience, Breda, The Netherlands) using a Haysep Q 80–100 mesh 2 m×1/8″ SS column, at a constant temperature of 60°C. N2O was detected with an electron capture detector (ECD). Injection volume was 5.0 ml in a fixed loop.
NH3 concentrations in the climate respiration chambers were determined twice daily (at 12.00 and 24.00 h) by means of a gas detection tube system (Kitagawa, type AP-20; Komyo rikagaku kogyo, Tokyo, Japan; type 105 NH3 gas detector tubes with a range of 1–20 ppm).
Production of N2O was calculated by subtracting the N2O concentration from the incoming air from that in the outgoing air. These differences were then used in a formula adapted from Wheeler et al (2003) :
ER = Emission rate of N2O = [N2O] change (ppm×10−6)×VV (m3/day)×44 (g/mol)/0.0224 (m3/mol), where VV = ventilation volume of air in a specified time period. The average concentration difference of the three samples taken during the three-day period was used to determine the average N2O production in a repetition.
The formula used by Wheeler (2003) was also used for the calculation of NH3 production. A molecular mass of 17 was used and instead of a difference in concentration, the measured concentration was used, leading to a slight overestimation of the actual NH3 production (between 0 and 0.1 mg/kg BM/day).
CO2 equivalents were calculated by adding the multiplications of the produced amounts of CH4 and N2O with their global warming potential; 25 for CH4, and 298 for N2O .
Mean body mass was calculated by averaging the body mass at the start of the experiment and the body mass at the end of the experiment. Average daily gain (ADG) was calculated as follows: (((End mass - Start mass)/Start mass)/3)*100%, in which 3 is the number of days the experiment was running.
The ratio between CO2 production per unit biomass per day and ADG gives an indication of the feed conversion efficiency, in which higher values indicate lower efficiencies.
To determine CO2 production from feed and substrate, all feeds were independently tested in the same respiration chambers, without the animals. A linear time course of consumption was assumed and CO2 production was recalculated to kg of live insect.
The N2O and NH3 assay data were subjected to a two-way analysis of variance (ANOVA) with species and time of sampling (24, 48, or 72 h) as fixed factors to determine whether the time of sampling had an effect. No significant effect of the time of sampling was found for N2O (Pillai's trace: F = 1.467, P = 0.199). Therefore, the average of the three samples taken during the 3-day trial period was used to determine the change per repetition and to calculate total production. However, NH3 production was significantly affected by the time of sampling (day or night; Pillai's trace: F = 4.065, P = 0.019) and the day of the repetition (first, second or third; Pillai's trace: F = 17.170, P<0.001). CO2 and CH4 production for all five species were analyzed by means of a one way analysis of variance (ANOVA) followed by a Tukey post hoc test. Statistical analysis of all data was done by means of SPSS 15.0.
Production of CO2 is expressed per kilogram of mean live body mass (BM) per day (24 hours) and per kilogram of mass gain (Table 2) and the average daily gain (ADG) is reported (Table 2). Production of CH4, N2O, CO2 equivalents, and NH3, are expressed per kilogram of mean live body mass (BM) per day (Table 3) and per kilogram of mass gain (Table 4).
3.1 ADG and CO2 production
ADG varied between 4.0% (P. marginata) and 19.6% (L. migratoria) with the three other species having an ADG of 6–7%. CO2 production among the five insect species differed significantly and ranged from 19 (B. dubia) to 110 (L. migratoria) g per kg BM/day. Also, the CO2 production per kg of metabolic weight (i.e. the weight of metabolically active body tissue) differed greatly between species (Table 5). CO2 production expressed per kg of mass gain was intermediary for L. migratoria due to the high ADG. Still, the CO2 production of L. migratoria per kg of mass gain was more than double the production of CO2 by B. dubia. Pachnoda marginata had the highest production of CO2 per kg of mass gain (1,539 g/kg), which was more than double the amount of L. migratoria.
Production of methane was detected for P. marginata and B. dubia, but not for the three other species. Pachnoda marginata produced more than three times as much CH4 per kg of mass gain than B. dubia (4.9 vs 1.4 g). This difference was caused by a higher production of CH4 per kg BM (0.16 g vs 0.08 g) and a lower ADG (4.0% vs 6.1%).
N2O was produced only in significant amounts by T. molitor and L. migratoria (1.5 and 8.0 mg/kg BM/day, respectively). Production of N2O by L. migratoria per kg BM was more than 5-fold the production by T. molitor, this difference decreased to almost 2.5-fold when expressed per kg of mass gain, due to a much higher ADG of L. migratoria.
NH3 was produced by A. domesticus, L. migratoria, and B. dubia (3.0–5.4 mg/kg BM/day), and ranged from 36–142 mg/kg of mass gain (Table 3 and 4). Significant differences (Pillai's trace: F = 4.065, P = 0.019) between daytime (12.00) and night-time (24.00) NH3 emission levels were found for A. domesticus (6.4 and 4.4 mg/kg BM/day), L. migratoria (5.6 and 3.9 mg/kg BM/day), and B. dubia (3.4 and 2.6 mg/kg BM/day).
Insects, being poikilotherms, do not use their metabolism to maintain a body temperature within narrow ranges, contrary to homeothermic animals. This is expected to result in higher feed conversion efficiencies. CO2 production related to growth, has an inverse relationship with feed conversion efficiency in a given situation. CO2 production by insects depends on the species, stage of development , , temperature , feeding status , and on activity level , . A production of 37 g CO2/kg BM/day was reported for Anabrus simplex (Orthoptera, Tettigoniidae), 40 g CO2/kg BM/day for the locust Schistocerca americana (Orthoptera; Acrididae)  and 94 g/kg BM/day for adult Tribolium castaneum (Coleoptera; Tenebrionidae) . All five species in the current study had a fairly high production of CO2. This might to a large extent be explained by ad libitum feeding during the experiment that has been reported to increase oxygen consumption fivefold . Reported CO2 production for inactive, unfed, Tenebrionid adults ranged between 5.4–13.3 g/kg BM/day , which is 5–10 times lower than observed for T. molitor in this experiment. This can partially be explained by the locomotory activities of T. molitor larvae in this experiment . Furthermore, growing larvae are expected to have a higher CO2 production than adults. The range of CO2 production for T. molitor is comparable to the factorial metabolic scope reported for tiger beetles (Cicindela spp: Coleoptera; Cicindelidae) of 6.1–16.5 .
Size differences in animals account for a difference in metabolic rate, and thereby CO2 production. The relation between metabolic rate (B) and body mass (M) was described by Kleiber  as B = aMb, in which a is a constant and b = 0.75. The value of b has been much debated since , , . For poikilotherms values between 0.67 and 1.0 have been reported and a comparison of several arthropod species suggested b approximates 0.82 , . The value chosen for b has a large impact on the metabolic weight and thereby the calculated CO2 production (Table 5). Applying b = 0.75 for pigs and beef cattle and b = 0.82 for insects, resulted in a lower CO2 production based on metabolic weight for the studied insect species (Table 5). For L. migratoria CO2 production was only slightly lower than for beef cattle, however, for the other four species production was between 18% and 54% of that for beef cattle and between 11% and 34% of the CO2 production of pigs.
The CO2 production per kg BM of insect species investigated in this study was higher than for pigs or cattle (Table 3). This concurs with Prothero et al. (1979) , who reported a higher oxygen consumption per kg of BM for insects than for mammals, assuming the respiratory quotient (CO2 production/O2 consumption) has similar values (0.7–1.0) for both animal groups. However, the CO2 production per kg of mass gain for the five insect species in the current study (337–1,539 g/kg) was either 39% (minimum values) or 129% (maximum values) when compared with pigs (865–1,194 g/kg) and much lower (12%–54% respectively) than cattle (2,835 g/kg). Therefore, CO2 production per kg of mass gain suggests higher feed conversion efficiencies for insects than for mammalian livestock. These results concur with those of other authors , , , .
A similar trend was visible for ADG; the ADG for the five insect species studied was 4.0–19.6%, the minimum value of this range being close to the 3.2% reported for pigs, whereas the maximum value was 6 times higher. Compared to cattle (0.3%), insect ADG values were much higher. In general, the rate of ADG depends, amongst others, on life phase. Therefore, where available, literature data on growing animals were used. The fundamental biological differences in growth and development processes between pigs and cattle and the studied insects impeded further synchronization.
CH4 production for the species studied was in agreement with Hackstein and Stumm (1994) ; for insects, only representatives of cockroaches, termites, and scarab beetles produce CH4. This originates from bacterial fermentation by methanobacteriaceae in the hindgut .
We found large variability for the N2O emission rates. Earlier studies in laying hens using a similar method for determining N2O production, concluded that production was either negligible or undetectable , . However, other authors ,  determined a production of 28 mg N2O/kg BM/day and 52 mg N2O/kg BM/day, respectively, indicating the difficulty of accurately determining N2O production .
In earlier studies respiration of feed was considered to have a negligible effect on utilisation of dry mass as determined gravimetrically  and therefore on CO2 production. Later studies suggested that respiration by plant leaves can be an important source of error in the calculation of insect feed intake using gravimetric methods  and can cause major errors in energy budget studies of plant-feeding insects . Our reported CO2 production includes the respiration of the feed (Table 6). The extremely high contribution to total CO2 production by the substrate of P. marginata (92.5%) was most likely due to large amounts of fungal biomass observed in the mixed feed and substrate when insects were absent in the experiments aimed to obtain correction values for CO2-production by the substrate. No fungal growth was apparent during the experiments on feeding P. marginata larvae, suggesting that the contribution of the substrate to total respiration during the experiment was much lower. We conclude that the interaction between actively feeding P. marginata larvae and the substrate suppressed fungal growth through either consumption by the beetle larvae  of fungal biomass or through unknown chemical or combined chemical/mechanical mechanisms. Such interactions hinder the application of realistic corrections for the contribution of feed and substrate to the total CO2 production and thus to quantify the CO2 production arising from insect metabolism separately.
For all other species the relative contribution of the feed to total CO2 production was minor, varying between 1.3% and 3.6%. Although feed respiration did have an impact on production of CO2, still the production of CO2 is much higher for L. migratoria than for the other insect species. A likely explanation for this higher production of CO2 is the 7°C higher temperature L. migratoria was kept at, as a difference of 10°C is expected to double CO2 production. Furthermore, the comparatively high ADG of L. migratoria is expected to result in higher production of CO2.
In one of the repetitions for A. domesticus, a lower ADG and increased mortality were observed. Excluding this repetition, the emission of CO2 per kg BM decreased slightly (68 vs 71 g/kg), but the emission of CO2 per kg mass gain changed considerably (918 vs 1468 g/kg). This difference can for a large part be explained by a decrease in ADG (from 9.0 to 7.2%). Acheta domesticus did not produce CH4, but N2O production doubled (from 0.1 to 0.2 mg/kg BM; 1.9 vs 5.3 mg/kg mass gain). The production of CO2 eq. also increased (0.04 vs 0.05 g CO2 eq. /kg BM and 0.57 vs 1.57 g/kg mass gain). It is well possible that the higher N2O production measured was caused by saprophytic bacteria utilising the dead A. domesticus and producing N2O . Although we included this repetition in the results, it is not clear whether this represents the practical situation best.
Large differences in NH3 emission have been reported for conventional livestock. Pigs for example emit 4.8–75 mg/kg BM/day , , , poultry 72–436 mg/kg BM/day , ,  and cattle 14–170 mg/kg BM/day , , . Several factors influence NH3 emission, such as temperature, relative humidity, food type, moisture content, pH, wind speed, housing type, and substrate , .
In the current experiment, a clear NH3 emission pattern was found; higher amounts of NH3 were emitted during daytime for A. domesticus, L. migratoria and B. dubia, than during nighttime. Day-night rhythms for NH3 excretion have been documented for pigs  and are strongly correlated with activity levels . Quantitatively the differences between day and night emission levels are small; 7–10% with a maximum difference of 25% . In our study this relative difference was approximately 33%. In all cases NH3 emission levels were higher during the daytime than during the night-time. For L. migratoria this is the active period, for the nocturnal B. dubia and A. domesticus it is not, indicating that a different, unknown variable might influence NH3 emission patterns in these insects.
NH3 concentrations in the outgoing air, and consequently calculated NH3 emission, increased from day one to day three in B. dubia (1.57 to 4.29 mg/kg BM/day) and A. domesticus (2.46 to 8.01 mg/kg BM/day). This could indicate that NH3 emissions might be underestimated due to the relatively short time frame of our experiments. For L. migratoria NH3 emission did not increase between day 1 and day 3 (5.57 and 5.05 mg/kg BM/day), suggesting that NH3 production was stable. This might be caused by the faeces of this species that, contrary to those of B. dubia or A. domesticus, dry quickly after defecation.
We conclude that P. marginata and T. molitor probably did not emit NH3. Poultry deep litter systems  have higher NH3 emission rates than battery systems , which is explained by the presence of substrate.
The presence of substrates for P. marginata and T. molitor in this study corresponded with lower NH3 emissions. A possible explanation is that gas exchange in the container is inhibited by the substrate and therefore less emission of NH3 was measured. However, it could also be that these species produce less NH3.
All insect species in this study produced much lower amounts of NH3 (3.0 to 5.4 mg/kg BM/day for A. domesticus, L. migratoria and B. dubia) than conventional livestock (4.8–75 mg/kg BM/day for pigs and 14–170 mg/kg BM/day for cattle). Further research is needed to determine for which insect species and to what extent NH3 emissions increase further when a longer time frame is used.
To the authors' knowledge, the study presented here is the first to report on both GHG and NH3 emissions of edible insect species. An evaluation of the GHG emissions of edible insect species is most relevant when based on CO2 eq. per kg of mass gain. In that way a comparison of the selected species with each other and with conventional livestock is based on a cost-benefit principle, in which the GHG production (environmental cost) is directly linked to food production (benefit). GHG emission of four of the five insect species studied was much lower than documented for pigs when expressed per kg of mass gain and only around 1% of the GHG emission for ruminants.
The measured NH3 emission levels of all insect species in this experiment were lower than reported NH3 emission levels for conventional livestock.
The ADG of all insect species in this study was higher than for conventional livestock, while CO2 production expressed as g/kg mass gain was comparable or lower, which indicates higher feed conversion efficiencies for insects.
This study therefore indicates that insects could serve as a more environmentally friendly alternative for the production of animal protein from the perspective of GHG and NH3 emissions. A complete lifecycle analysis for species of edible insects is lacking at this point in time  and should be the focus point of further studies to allow a conclusive evaluation of the sustainability of insects as a protein-rich food source. The data presented in this study are indispensable for conducting a lifecycle analysis for edible insects.
The authors would like to thank Jean Slangen of the WUR Environmental Sciences Group for his help with the analysis of nitrous oxide. The commercial rearing companies “Kreca” and “van de Ven insectenkwekerij” are kindly acknowledged for their contributions. Dr. T. Vellinga is kindly acknowledged for his careful review of this manuscript.
Conceived and designed the experiments: DO HvdB JvL AvH. Performed the experiments: DO JvI. Analyzed the data: DO JvI MJWH. Contributed reagents/materials/analysis tools: MJWH. Wrote the paper: DO HvdB JvL AvH.
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