Journal of Material Cycles and Waste Management

https://doi.org/10.1007/s10163-018-0738-1

ORIGINAL ARTICLE

Anaerobic digestion of fish waste and seagrass/macroalgae: potential

sustainable waste management for tropical Small Island Developing
States
Nadeem Nazurally1

Received: 19 October 2017 / Accepted: 18 April 2018

© Springer Japan KK, part of Springer Nature 2018

Abstract
This study presents the preliminary investigation of the biogas production potential from fish wastes (FW) and seagrass
(SG) mixed with macroalgae (MA). Substrates were prepared for total solids of 10–12% and were analysed in Biochemical
Methane Potential (BMP) assays. The inoculum used in all BMPs was acclimated sludge in a ratio of 1:3 for inoculum to
substrate on a mass basis. There were effectively four vessel reactors (VRs) with different compositions: VR1 100% fish
wastes, VR2 60% fish wastes and 40% seagrass/macroalgae, VR3 40% fish wastes and 60% seagrass/macroalgae, and VR4
100% seagrass/macroalgae. VR5 acted as control with 100% inoculum. The maximum cumulative biogas productions (CBPs)
reached 8288 ml for VR1, 8410 ml for VR2, 4236 ml for VR3 and 2746 ml for VR4 with a concentration of methane gas of
61.1, 65.07, 68.07, and 53.28%, respectively. One-way ANOVA test results (p < 0.05) indicated that there was significant
difference in the variations in VS, salinity, COD, soluble COD and cumulative biogas production amongst the test vessel
reactors. This potential for biogas production represents a clean source of cheap fuel for sustainable development in Small
Island Developing States having aquaculture and seafood industries along coastal regions.

Keywords  Fish waste · Macroalgae · Seagrass · Anaerobic digestion · Biogas

Introduction for beach clean-up as well as the removal of the decaying sea-
grasses and macroalgae. In 2014, the Government embarked
The Republic of Mauritius is a tropical Small Island Develop- on a new sector for the economy, namely the ocean. Marine
ing State (SIDS) occupying a lagoonal area of almost 245 km2 aquaculture and Seafood Industry is a key among the vari-
in the southwest Indian Ocean. The Republic of Mauritius ous activities identified for future development contributing
is subject to leaching of pollutant [1] into the lagoon which to national food security [5]. Marine aquaculture and Seafood
results in seagrasses and macroalgae blooms affecting our Industry is a tremendous potential, but it has also its draw-
seashores [2]. Yet, rotting seagrass and macroalgae are potent backs in terms of waste generations. Currently, Mauritius has
source of hydrogen sulphide [3]. In some places in Mauritius, only one operational floating cage fish farm with an output of
excessive nutrient input by agricultural activities has triggered around 1000 tons of fish per year in 2016 and increasing to
seagrasses and macroalgae overgrowths causing nuisance upon 3000 tons in the coming next 2 years. Intensive aquaculture
decomposition and accumulation on seashores. Hence, sea- and processing of fish creates a lot of fish wastes in terms of
grasses/macroalgae pose an environmental nuisance on coastal dead fish, fish intestines, skins and other unused parts [6]. Up
zones when left unused or untreated [4] as Mauritius is known to 12% (about 120 g of waste per kg of fish) is considered as
for its touristic destination and allocates large sum of money waste [7] and usually not preferred for human consumption.
Similar to other types of food-processing industries, fish-pro-
cessing operations also produce vast amount of solid waste
* Nadeem Nazurally (fish carcasses, viscera, skin and heads) or liquid waste such
[email protected] as bloodwater used for cleaning. With the rapid development
1 of aquaculture and seafood industry sector in Mauritius, fish
Department of Agricultural and Food Science, Faculty
of Agriculture, University of Mauritius, Reduit 80837, wastes can be a major concern and could negatively impact the
Mauritius marine environment if illegal dumping is practiced or dumping

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 Journal of Material Cycles and Waste Management

Table 1  Mass of substrate used Vessel reactors Solid content Moisture content (%) Mass (g)
for mixing
Substrate (%) Substrate Inoculum Substrate Inoculum Water Total

VR 1 0.51 0.49 0.92 296.06 98.69 1205.25 1600

VR 2 0.36 0.64 0.92 413.93 137.98 1048.09 1600
VR 3 0.28 0.72 0.92 516.81 172.27 910.92 1600
VR 4 0.13 0.87 0.92 1027.62 342.54 229.84 1600
VR 5 – – 0.92 – 1600 – 1600

is done near shores. Even though they are natural pollutants, of the island. Moisture content (MC), total solids (TS)
they can cause major algal bloom with addition of nutrients and volatile solids (VS) were analysed prior to mixing
[8] resulting in diseases and fish stock decrease. Worldwide, the substrates in the test ratios. pH, salinity and electrical
the majority of fish waste is turned into fish meal or fish oil conductivity were analysed for these samples as shown
which may not apply to Mauritius in investing large amount of in Table 2.
capital due to competitiveness of the international market and
low price of fish meal and fish oil. Thus, alternatives such as
aerobic digestion to produce fertilizers and anaerobic digestion Substrates for BMP tests and setups
to produce biogas could become potential treatment routes for
fish wastes. All the Biochemical Methane Potential (BMP) assays were
carried out with similar quality and quantity of solids and
Anaerobic digestion within the same tolerable, starting and operating condi-
tions. 5 plastic bottles of 2000 ml capacity were used as
The organic fraction of solid wastes generated in Mauri- digester reactors (anaerobic digester) for the BMP. The
tius from municipal solid wastes (MSW) represents about digesters were kept under dark conditions to promote dark
70–80% of the waste [9]. Currently, Mauritius has only one fermentative processes and assist the methanogenic pro-
sanitary landfill at Mare Chicose [10] where a large portion cess [17]. The five vessel reactors (VR1, VR2, VR3, VR4
of the wastes generated around the Island are dumped. Alter- and VR5) each had the following mass-weighted ratios
native to landfilling is crucial for the proper management of of substrates: VR 1 (fish waste 100%), VR 2 (fish waste
the only landfill as space is limited and is also near satura- 3:2 seagrass/macroalgae), VR 3 (fish waste 2:3 seagrass/
tion. The disadvantage pertaining to landfilling is that there macroalgae), VR 4 (seagrass/macroalgae 100%) and VR
is the release of harmful gases [11, 12] which contributes 5 (100% inoculum) as detailed in Table 1. A headspace
significantly to global climate change. Anaerobic digestion of 20% by volume was kept at the start of the anaero-
offers a route for remediating high-pollution-load organic bic digestion processes in each digester. Biogas from the
wastes such as sewage sludge [13], MSW [14], livestock digesters was collected in airtight Tedlar bags and was
effluents [15], food wastes [16] and fish wastes [6]. Further- analysed in a Geotech Gas Analyzer model GA10754 for
more, anaerobic digestion offers a clean source of energy methane and carbon dioxide.
which can be harnessed whereby suitable organic wastes
are available. The aim of this study was to characterize the
wastes from a fish farm and mixed seagrass/macroalgae
Table 2  Initial parameters for each bulk crushed waste
washed along the eastern seashores in Mauritius in view to
assess the biogas production potential from anaerobic diges- Property Units of Substrate
measure-
tion in different mass weighted mixtures. ment Fish wastes Seagrass/macroalgae

Moisture content % 48.6 ± 0.3 87.1 ± 0.7

Materials and methods (wet)
Volatile solids % 96.2 ± 0.5 55.8 ± 0.9
Sampling Total solids % 51.4 ± 0.1 12.9 ± 0.2
Ash content % 3.8 ± 0.4 44.2 ± 0.1
Fresh seagrasses/macroalgae washed along the eastern pH _ 7.2 ± 0.01 7.8 ± 0.01
coast of Mauritius were collected. Fresh fish wastes which Electrical conduc- mS/cm 4.1 ± 0.1 7.1 ± 0.1
tivity
consisted of fish intestines, gills and skins were collected
Salinity ‰ 0.6 ± 0.02 2.1 ± 0.01
from the only operational fish farm in the eastern region

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Journal of Material Cycles and Waste Management

Low‑solid (LS) BMP determine if the variable mixing ratios were treatments
giving significantly different variations in the parameters
A low solid (LS)—TS < 15%—was used for the experiments. monitored. One-way ANOVA tests were performed on
‘Low-solid’ mixtures are mostly used because of the rela- pH, salinity, TS, VS, COD, sCOD, VFAs and biogas gen-
tively high biodegradable rates and faster biogas production eration data.
[15]. The inoculum used in all the BMPs was a sludge that
had been acclimatized for 10 days under thermophilic condi-
tions by feeding this inoculum with small quantities of fish
Results and discussion
wastes and seagrass/macroalgae every 3 days. The initial
total solids in the BMPs ranged from 10 to 12%.
Substrate characteristics
The head space was then purged with nitrogen gas to
remove the air (oxygen) inside, thereby attaining anaero-
All samples were collected the same day and processed
bic conditions. The vessel reactors were then immediately
accordingly. The fish wastes consisted of mainly fish intes-
closed with rubber-tight bungs and sealed with silicon glue
tines, liver and skin while the seagrass to macroalgae was in
and fixed with tape to prevent any loss of gas. A leakage
the percentage of 80% seagrass:20% macroalgae.
test was done so as to ensure that there was no leakage. This
The physical parameters differ significantly for fish
was done by placing the digester in a large water basin and
wastes to seagrass/macroalgae as shown in Table 2. Fish
nitrogen gas was passed. No leakage was detected.
wastes had lower moisture contents at 48.6 ± 0.3% because
of the high fat and oil contents [18] while seagrass/macroal-
Analytical methods
gae had higher moisture content as they comprise mainly
water [19]. Consequently, the volatile solids were also higher
All analytical tests for MC, TS and VS were carried out once
in fish wastes due to the fat and oil contents as compared to
weekly. COD was evaluated once weekly and biogas gen-
seagrass/macroalgae.
eration was monitored daily. All analytical tests were per-
formed in triplicates. TS were determined based on the final
constant mass method using a hot-air drying oven (Mem- pH and VFAs
mert, model 800, Schwabach, Germany). VS content was
determined by the loss on ignition BS 1377 method in an Anaerobic digestion is generally conducted under neutral
air-muffle furnace (Fisher Model 750-58, Fisher Scientific, pH conditions 6.4–7.6 [20–22]. All samples had a start-
Pittsburgh, PA). All masses were recorded using Mettler ing pH at 6.4–7.4 after grinding and mixing as shown in
PM3000 top pan balance (± 0.1 g). pH was measured using Fig. 1. Hence, pH adjustments were not necessary at the
a soil pH meter (Hanna Instruments, Direct soil pH meter start of experiment. However, pH adjustments were done
model 08921, Romania) by applying the probe into the sub- (after 5 days) using ammonium bicarbonate (< 2 g) in the
strate and results were automatically displayed. Conductivity BMP assays as pH continued to decrease until stability was
was also used by the same principle of pH analysis using reached. After adaptation within the system due to ability
a probe (Conductivity/Salinity meter Hach CO150, CAM- to resist pH change, pH started to increase to the desired
LAB). Salinity (conductivity/salinity meter, Hach CO150, range (6.4–7.6) of what Chugh et al. [20] and Buffiere et al.
CAMLAB) was taken using the same principle, while tem- [21] suggested as an optimum; pH 6.3 will inhibit biogas
perature was measured using a mercury thermometer. For production [22]. VFA values were calculated in meq/l using
the VFA analysis, a raw sample from the vessel reactors TITGRAM software. The components formed during the
was diluted and then filtered for solid removal. The filtrate hydrolysis steps [17, 23] are further solubilized in the aci-
was then processed for five pH titration points. When all the dogenic reactions and yield volatile fatty acids (VFAs),
titrant volumes reached the different pH points, the pH and and ammonia [24], ­CO2 and H ­ 2S [25, 26]. Basically, VFA
titrant values were processed in the TITGRAM software, concentration is reported to increase in the cases of ammo-
which then reported the VFAs’ content. Chemical oxygen nia toxicity [22, 27]. pH is directly related to VFA produc-
demand (COD) and soluble COD were evaluated following tion [28, 29], as VFA production increased, pH eventually
the standard potassium dichromate (VI)/ferrous ammonium decreased due to high content of undissociated volatile fatty
sulphate titration method as per APHA (2005). acid formation [29]. With the right pH, VR 1, 2 and 3 had
the highest VFA production due to high organic contents in
Statistical analysis terms of fatty acids from the fish wastes while sample 4 had
a low VFA content as no fish waste was present. There was
SPSS 16.0 was used for conducting ANOVA parametric a general increase of VFA in all vessel reactors as shown in
tests (Post hoc analysis and Tukey’s HSD) at p = 0.05 to Fig. 1. VR 1 had the highest VFA content attributed to the

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Fig. 1  Variation in the physical parameters of the pretreatments over 26 days. a pH; b volatile fatty acids; c salinity; d conductivity; e total sol-
ids; f volatile solids

relatively high fatty acid content (920) from the fish waste Salinity and conductivity
and it increased to 948 in the following 8 days and dropped
to 121 over the next 18 days. Figure  1 shows that salinity was significantly different
amongst the digesters (p < 0.05). Following the Tukey’s
HSD test, VR1, VR2 and VR3 differed from VR4 (p < 0.05).
The seagrasses/macroalgae contributed greatly to high

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Journal of Material Cycles and Waste Management

Fig. 1  (continued)

salinity of VR4 as the latter used substrates that had not and 3; vessel reactor 1 contained only fish wastes with lower
been washed with freshwater. Eventually, salinity decreased salinity content (0.7) as it decreased for 12 days (0.4) after
over the BMP course due to nutrient usage and other reac- which an increase was noted for 3 days onward (+ 22%) and
tions occurring in the systems. At start of the experiment, a gradual decrease till 26 days. Presence of certain ions such
salinity decreased, then started to rise after 5 days for VR1, 2 as ­Na+, ­Ca+ and C
­ l− in seawater contributes to high-saline

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Fig. 1  (continued)

seawater. However, the role of the anions is more associ- and no fish waste content. Conductivity in vessel reactor 4
ated with pH changes [30]. High concentrations of sodium decreased (− 15%) over the 26 days whereas in vessel reac-
are normally produced in the food-processing industry [31] tors 1, 2 and 3 it decreased at startup of BMP and gradually
including fish-processing plants [32]. Conductivity in vessel increased over the 26 days [VR1 (+ 12.5%), VR2 (+ 2%) and
reactor 1 was also much higher (7.1 mS/cm) compared to VR3 (+ 8.5%)], respectively. Salinity is positively correlated
vessel reactors 1, 2 and 3 due to the presence of high salinity to conductivity due to the presence of chloride ions. A P

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Journal of Material Cycles and Waste Management

value of 0.00 was obtained following the descriptive statistic content while in VR 3 there were organics but very little
for each vessel reactor implying that they were significantly fatty acid molecules. Initially, degradation in VR 3 was slow
different. as the cell wall of the plant materials need to be destroyed by
microorganisms [35,] and reaction rates normally take place
Total solids and volatile solids very slowly. The reduction of COD is a measure of biodeg-
radation occurring in the digester [36]. From Fig. 2, it is
A decrease in TS and VS for all samples was noted in the noticed that VR 1 and VR 2 had a decreasing trend in COD
BMPs as shown in Fig. 1. TS and VS for vessel reactor 1 and this could be accounted for the removal of organic mat-
and 2 were greater than samples from vessel reactors 3 and ter in the systems through AD process [18] while VR 3 and
4 because of the high content of fish wastes compared to VR 4 had a slow increase on the final days probably coming
seagrasses/macroalgae. Significance test revealed TS to be from some organics settled below the vessel reactors. This
roughly equal (p < 0.05) in all vessel reactors with VS dif- increase was also probably due to the hydrolysis stage which
ferent in each vessel reactor (p < 0.05). Reductions in solid involved the breaking down of the cells of the seagrasses/
contents have equally been reported by Meynell [33] and macroalgae wastes. In inference, it may be deduced that most
Uzodinma and Ofoefule [34]. Coskuner and Curtis [26] of degradation of organic matter occurred approximately on
showed that the decomposition rate of organic substances is the 11th day, indicating that most of the easily degraded
affected by the slow growth of microorganisms. In this study, organic molecules had almost degraded [37].
the TS started on average of 12.30–13.50% and decreased Soluble COD was significantly different in all vessel
to 8.50–10.70%, while the percentage VS was around reactors (p < 0.05) as shown in Fig. 3. There was a gen-
55.80–96.70% and decreased to 37.10–80.30%. eral increased in soluble COD for both VR 1 and VR 2 at
From Fig. 2, it is noticed that COD was significantly start. VR1 had a decrease in soluble COD but gradually
different in all vessel reactors (p < 0.05). In vessel reactors after 8 days, there is a steep growth and attains its peak
(VR) 1 and 3, the COD values were very high while in VR 4 (13,138 ± 1000  mg/L) after 17 days, it then gradually
the values were low. The high values of COD indicated that decreased (3649 ± 100 mg/L). There was a steady growth
they had a high content of organic matter [6, 13]. The main in amount of soluble COD for VR 2 and attains its peak
reason behind the high organic content was that in VR 1, VR (13,200 ± 1000 mg/L) after 20 days after that it decreased
2 and VR 3, there were fish wastes which had a high con- gradually (8759 ± 100 mg/L). VR 3 also decreased in sol-
tent of fatty acids which corresponds to the high total solid uble COD content after setup but increases in a constant

Fig. 2  Variation in chemical oxygen demand

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 Journal of Material Cycles and Waste Management

Fig. 3  Variation in soluble chemical oxygen demand over 25 days

flow after 8 days and attains its peak (8760–200  mg/L) This was indicative of the biogas being formed from the
after 13 days after which it also decreases gradually fish wastes and seagrasses/macroalgae.
(7299 ± 300 mg/L). VR 4 had a very low soluble COD con- Following a one-way ANOVA and grouping by Duncan
tent at start (584 ± 0.00) and increases after 8 days arriving test (Table 4), the 4-vessel reactors were grouped into 2
at peak (2920 ± 100 mg/L) while maintaining a low level of categories with significant differences (Anova, p < 0.05).
soluble COD throughout the experiment with final level of Group 1 consisting of lower production vessel reactors 3
(1460 ± 100 mg/L). VR 1, 2 and 3’s high contents can be and 4, while Group 2 higher production vessel reactors
attributed to the fact that the samples contained large amount 3 and 4 (Table 4). The amount of biogas produced by a
of fatty acids from the fish liver and other waste content. system directly depends on the VS content [17], thus VRs
VR 4’s very low soluble content is related to the very low 1, 2 and 3 had the highest volatile solid content which
organic content (TS of initial seagrasses/macroalgae sam- in turn produced the highest biogas compared to VR4.
ples < 12.9 ± 0.2 mg/L) and high moisture content. The solu- Biogas production was significantly different in each ves-
ble COD to total COD ratios in this study increased for VR sel reactor (p < 0.05). The maximum cumulative biogas
1, 2 and 4 at start while VR 3 had a decrease in sCOD/COD productions (CBPs) reached 8288 ml for VR1, 8410 ml
ratio but increased over time. sCOD to TCOD ratios gener- for VR2, 4236  ml for VR3 and 2746  ml for VR4. The
ally give an indication of the extent of hydrolysis [38, 39]. maximum CBP for the control was only 158 ml. The high
biogas production correlates with the greatest destruc-
Efficiency of vessel reactors for production of biogas tion of volatile solids [13, 25, 41]. Overall, following the
Tukey’s HSD test, VR1 with p > 0.05 to VR2 suggest the
Biogas production increased in all vessel reactors, clean similarity in biogas production as the mixing ratio of 3
energy recovery from organic wastes is one of the most fish wastes:2 seagrasses/macroalgae and 2 fish wastes:3
important attributes of anaerobic digestion [40]. The first seagrasses/macroalgae had nearly the same composition.
week as shown in Fig. 4 saw a rapid biogas production VR4 had no fish wastes but only seagrasses/macroalgae,
due to the highly degradable wastes present within the its biogas production started as from day 4 and it had the
samples. The control VR5 had a zero production for the lowest production as compared to the other vessel reactors
first 4 days and consequently very few amounts of biogas deducing that the high salinity played a negative role in
were detected all over the 26 days as shown in Table 3. biogas generation on the overall process.

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Journal of Material Cycles and Waste Management

Fig. 4  Cumulative biogas pro-

duction over 26 days

Table 3  Average production Biogas production

of biogas from the four-vessel
reactors Vessel reactor N Mean Std. deviation Std. error Minimum Maximum

1 26.0 4163.8 3060.5 600.2 30.0 8324.0

2 26.0 4172.6 3148.5 617.5 24.0 8412.0
3 26.0 2114.3 1520.8 298.3 18.0 4236.0
4 26.0 1207.7 998.8 195.9 0.0 2746.0
Total 104.0 2914.6 2678.4 262.6 0.0 8412.0

Vessel reactors 1 and 2 showed higher production reaching a maximum of 8412. While vessel reactors 3
and 4 show lower productivity

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 Journal of Material Cycles and Waste Management

Table 4  Duncan test Duncan All vessel reactors had generated methane with variable
amount in each different component as shown in Fig. 5. In
Vessel N Subset for
reactor
this study, we considered only methane to carbon dioxide
alpha = 0.05
enrichment ratios while the other gases formed were not
1 2 assessed. VR1 had the highest amount of biogas production
4 26 1207.70 with methane enrichment of 61.10% C ­ H4 (36.70% C­ O2 and
3 26 2114.30 2.2% unknown gases), VR2 had 65.07% C ­ H4 (30.17% C­ O2
1 26 4163.80 and 4.76% unknown gases), VR3 had 68.07% C ­ H4 (30.11%
2 26 4172.60 ­CO2 and 1.82% other gases) while VR4 had the lowest meth-
ane content with 53.28% C ­ H4 (34.09% C ­ O2 and 12.63%
unknown gases). The highest methane enrichment was from
vessel reactors 2 and 3 as they had a mixture of fish wastes
and seagrasses/macroalgae. The high methane enrichment

Fig. 5  Percentage variation of methane and carbon dioxide

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Journal of Material Cycles and Waste Management

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