ARTICLE IN PRESS

Water Research 37 (2003) 35903601

Effects of temperature transient conditions on aerobic

biological treatment of wastewater
Fernando Morgan-Sagastume, D. Grant Allen*
Department of Chemical Engineering and Applied Chemistry, Pulp & Paper Centre, University of Toronto, 200 College Street,
Toronto, Ont., Canada M5S 3E5
Received 17 May 2002; accepted 10 April 2003

Abstract
The effects of temperature variations on aerobic biological wastewater treatment were evaluated with respect to
treatment efciency, solids discharges, sludge physicochemical properties and microbiology. The effects of controlled
temperature shifts (from 35
to 45
C; from 45
to 35
C) and periodic temperature oscillations (from 31.5
C to 40
C, 6day period, for 30 days) were assessed in 4 parallel, lab-scale sequencing batch reactors (SBRs) that treated pulp and
paper mill efuent.
Overall, the temperature shifts caused higher efuent suspended solids (ESS) levels (25100 mg/L) and a decrease (up
to 20%) in the removal efciencies of soluble chemical oxygen demand (SCOD). Lower ESS levels were triggered by a
slow (2
C/day) versus a fast (10
C/12 h) temperature shift from 35
to 45
C, but the SCOD removal efciencies
decreased similarly in both cases (from 6673% and 6572% to 4973% and 5173%). Temperature oscillations caused
an increased deterioration of the sludge settleability [high sludge volume indices (SVI); low zone settling velocities
(ZSV)], high ESS levels and lower SCOD removals.
The temperature transients were associated with poor sludge settleability (SVI>100 mL/g MLSS, ZSVo1 cm/min),
more negatively charged sludge (up to 0.3570.03 meq/g MLSS), increased lament abundance (B4 to 4.5, subjective
scale equivalent to very common), and decreased concentrations of protozoa and metazoa (25,00050,000
microorganisms/mL sludge). The controlled, periodic temperature oscillations had a slight impact on SCOD removal
efciency (5% decrease), and did not seem to select for robust microorganisms that withstood the temperature shift.
Sludge deocculation and lament proliferation caused by these temperature transients may explain the higher ESS
levels.
r 2003 Elsevier Ltd. All rights reserved.
Keywords: Activated sludge; Temperature transients; Temperature oscillations; SBR; Settleability; Pulp and paper mill efuent

1. Introduction
Transient, non-steady state conditions in biological
wastewater treatment are common, and can be caused
by changes in substrate and nutrient characteristics or
concentration, and by changes in the environmental
*Corresponding author. Tel.: +1-416-978-8517; fax: +1416-971-2106.
E-mail address: allendg@chem-eng.utoronto.ca
(D.G. Allen).

conditions to which the biomass is exposed [e.g.,

dissolved oxygen (DO), pH, temperature]. The effects
of substrate concentration transients on internal polymer storage, growth rate, and substrate accumulation
have been widely investigated and are better understood
than other types of transients [17]. Environmental
transients have been associated with system instability
and/or perturbations, but have been less studied until
recently. DO transients, specically anaerobic conditions, have been related to sludge deocculation [8], and
toxic transients (e.g., phenol spikes) have induced sludge

0043-1354/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0043-1354(03)00270-7

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F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

deocculation and decreased oxygen uptake rates

(OURs) [9,10].
Temperature transients in biological wastewater
treatment can result from seasonal variations, and from
the operation of batch units and shutdowns/start-ups in
upstream industrial processes. Industrial treatment
systems may be subjected to frequent and drastic
temperature transients that affect treatment performance. On the contrary, sewage treatment systems
may experience mainly seasonal transients of which
winters may represent the most challenging due to
reduced microbial activity. Pulp and paper mill efuents,
similar to those from several food processing industries,
are characterised by high temperatures (above 2035
C)
[11]. A better understanding of mesophilic and thermophilic aerobic treatment of pulp and paper mill efuent
has been achieved, especially, in relation to steady-state
operation at different temperatures [1218]. Nevertheless, the effects of temperature transitions on sludge
metabolism, microbial community structure, settling
characteristics, and bioocculation are not well understood.
Temperature shifts have been related to decreased
treatment performance and system instability [e.g.,
lower activity, poor settling, high efuent suspended
solids (ESS)], as in full-scale biological plants treating
pulp and paper mill efuent over 38
C during the
summer [19,20]. There are a few reports of the effects of
temperature shifts on aerobic biological wastewater
treatment, most of which come from temperature
adjustments in steady-state studies. The effects have
been dependent on the magnitude of the shift and on the
temperature range studied, and have been linked to
decreased sludge metabolic activity and/or poor sludge
settling [15,21,22]. Observations of deteriorated sludge
settling due to temperature shifts have been anecdotal,
but not from systematic studies, and have been reported
as biomass washout, increments in ESS levels, and
variability in sludge settling parameters [12,15,23].
Efuent turbidity increase has been related to deocculation and weak occulation due to a temperature
decrease from 20
C to 4
C [24].
Biological treatment plants of high-temperature efuent traditionally operate within the mesophilic temperature range of 2535
C. In aerobic treatment systems
that operate at the limit of the mesophilic range (35
40
C), operating at higher temperatures (e.g., 45
C)
during the summer and back down during the fall-winter
may represent a way of cutting down on costs
of cooling equipment and limited cooling through
direct efuent dilution. Treating industrial efuent
at higher temperatures (e.g., 4045
C) may be feasible,
as demonstrated for pulp and paper mill efuent by
Tripathi and Allen [16]. However, the transition
from 3035
C to 4045
C in the summer, and back to
3035
C in the fall-winter, may represent a challenge

3591

due to system instability. Destabilisation due to

transients is becoming of greater concern as treatment
systems are pushed to work at their treatment limits
to meet more stringent regulations and/or increased
loads.
The goal of this study was to investigate the effects of
controlled temperature transients on the performance of
an activated-sludge-type system. The impacts of a 10
C
temperature upshift and a 10
C temperature downshift
on the sludge metabolic activity, settling and bioocculation characteristics were assessed at the upper limit of
mesophilic treatment (3045
C). In addition, the potential to enhance the robustness of the sludge to handle
temperature shifts through adaptation to temperature
oscillations was evaluated.

2. Experimental procedures
2.1. Experimental apparatus
Bleached hardwood kraft pulp and paper mill efuent
was used in this study. Approximately 2200 L of mill
efuent were collected from the outlet of the primary
clarier during a period of 1.5 h, and immediately
refrigerated at 4
C. The mill produces approximately
300 t/day of Elemental Chlorine Free (ECF) bleached
hardwood kraft pulp, 120 t/day of recycled bleached
corrugated pulp, and 700 t/day of ne paper. The
treatment plant handles about 128,000 m3/day of wastewater.
The biomass used as inoculum (approximately 0.35 L/
reactor) was return-activated-sludge mixed liquor obtained from the same mill wastewater treatment plant,
and was refrigerated until inoculation. The sludge was
aerated for 1 day at room temperature before inoculating and starting up the reactors. This sludge suspension
had a total suspended solids (TSS) concentration of
12,5707230 mg/L and a volatile suspended solids (VSS)
concentration of 98307130 mg/L.
The efuent from the mill was transported to our
research laboratory in a refrigerated truck, and then
frozen at 20
C. The wastewater was thawed as
required (about 84 L/week). Nitrogen (N) and phosphorus (P) were added to the thawed, raw mill efuent
as ammonium chloride (NH4Cl; Mallinckrodt Inc.,
Paris, Kentucky) and di-ammonium hydrogen orthophosphate [(NH4)2HPO4; BDH Inc., Toronto, Ontario],
in a soluble-COD:N:P ratio of 200:5:1. The pH of the
feed (conditioned mill efuent) was decreased to 6 by
adding 20% v/v sulphuric acid (H2SO4, Reagent A.C.S.
Fischer Scientic, Nepean, Ontario), which maintained
the mixed liquor pH between 7 and 8 (pH=7.670.3).
The prepared feed was then stored in 4 separate 9-L
containers (High-density polyethylene carboy, Nalgene,
VWR Scientic, Mississauga, Ontario) at 4
C in a 153-L

ARTICLE IN PRESS
refrigerator (W.C. Wood Co., Ottawa, Ohio), part of the
reactors setup.
An hour and a half before each feeding cycle, 1 L of
feed from each refrigerated container was pumped into a
2-L glass holding tank, where the temperature reached
28
C by means of a water bath. The pre-warmed feed at
28
C caused the temperature of the sludge in the
reactors at 35
or 45
C to decrease to a minimum of
33.5
C (from 35
C) and to a minimum of 40
C (from
45
C) during feeding, respectively. The initial temperature of 35
or 45
C recovered within less than an hour
since the beginning of feeding. These batch-feeding
temperature transients, similar to the feast-starvation
transients inherent to the batch reactors operation, had
no observable disturbing effect on the treatment
performance of the reactors since relatively constant
operating conditions were achieved over time. The
temperature cooling during feeding, therefore, did not
represent a signicant shock to the system.
Four parallel sequencing batch reactors (SBRs) were
operated to mimic the processes taking place in an
activated sludge system, and were connected to the feedstorage refrigerator, preheating tank, and water baths,
as described elsewhere [16,23]. The 4 SBRs were
operated in three 8-h cycles per day. Each 8-h cycle
consisted of a 25-min anoxic lling phase with mixing, a
reaction phase with continuous mixing and aeration
(385 min), a 60-min settling phase, and a 10-min
discharge phase. The DO levels were above 23 mg/L
during the reaction phase in the 4 reactors, except for the
initial 20 min, after anoxic lling, when the DO levels
were below 1 mg/L. A sludge retention time (SRT) of
approximately 25 days in the 4 SBRs was maintained by
the amounts of mixed liquor wasted every 2 days (B8%
of mixed liquor), taking into account the wastage due to
suspended solids in the efuent.
2.2. Temperature transients
Two main temperature variations in the 4 SBRs were
conducted on days 117 and 146, as illustrated in Fig. 1.
Before the rst shift (Day 117), the 4 reactors were
acclimated at 35
C, and the sludge was mixed and
redistributed among the 4 SBRs (Day 111). One SBR
(SBR1) was subjected to a fast temperature increase
(10
C/12 h) from 35
to 45
C. A second SBR (SBR2)
was subjected to a slow, 2
C/day temperature increase
during 5 days to achieve a net increase from 35
to 45
C.
The temperature in a third SBR (SBR3) was initially
increased from 35
to 40
C, and after 3 days at 40
C,
decreased to approximately 32.5
C to begin periodic
temperature oscillations from 31.5
to 40
C with a 6day period. The fourth reactor (SBR4) acted as control
at 35
C for the temperature shifts, and provided for a
paired experiment showing that the shift effects were not
due to random operating characteristics.

Temperature (C)

F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

50
45
40
SBR1

35

SBR2

30
100

110

130

140

150

160

170

160

170

50
SBR3

45

SBR4

40
35
30
100

(B)

120

Time of operation (days)

(A)
Temperature (C)

3592

110

120

130

140

150

Time of operation (days)

Fig. 1. Temperature proles in the 4 SBRs during the 3545
C

temperature upshift, the 4535
C temperature downshift, and
during temperature oscillations. (A) Proles of SBRs 1 and 2
and (B) proles of SBRs 3 and 4.

Twenty-nine days after the rst temperature shift, the

mixed liquors from SBR1 and SBR2 were mixed and
redistributed between the 2 reactors, and a second
temperature transient was conducted (Day 146). SBR1
remained at 45
C, the temperature in SBR2 was
decreased from 45
to 35
C, SBR3 was subjected to
an increase from 31.5
to 45
C, and the temperature in
SBR4 was increased from 35
to 45
C. In this case, the
reactor performance after 4535
C decrease (SBR2) was
compared to that under constant temperature at 45
C
(SBR1), and the effects of a 31.545
C increase after
temperature oscillations (SBR3) were compared to those
of a 3545
C increase after constant temperature
operation at 35
C (SBR4).
The reactors temperature was monitored with 76 mm
mercury thermometers. Deep-chamber water baths
(3 SBRs: 33 L, 1295 PC, VWR Scientic, Mississauga,
Ontario; 1 SBR: MagniWhirl Constant Temperature
Bath, Blue M Electric Company, Blue Island, Illinois)
connected to the reactors water jackets were used to
control the reactors temperatures. The accuracy of the
temperature readings was 71
C.
2.3. Microbial activity
Organic carbon biodegradation was monitored by
measuring soluble chemical oxygen demand (SCOD)
from the inlet of the reactors and the treated efuent
discharged and collected at the end of a cycle. The
samples were ltered through 1.5-mm-pore-size glass
microbre lters (934-AH, Whatman Inc., Clifton, New
Jersey), and stored at 4
C before digestion. COD

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F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

measurement in the ltrates was conducted following

Standard Methods [25].
The total COD of the fresh raw pulp mill efuent
when collected was about 800 mg/L. The average
SCOD of the efuent was 578720 mg/L before
storage at 20
C. A reduction in the SCOD levels
of the original efuent took place after freezing,
thawing and refrigerating the efuent. Therefore, the
feed to 4 SBRs had a lower average SCOD of
371753 mg/L (average from the 4 SBRs in Table 1)
during the 165 days of operation than the original
efuent; however, the 4 SBRs were fed with the same
prepared batches of mill efuent.
Specic oxygen uptake rates (OURs) were calculated
from DO measurements (YSI Model 57, YSI 5750 BOD
Bottle Probe, YSI Inc., Yellow Springs Instrument Co.
Inc., Yellow Springs, Ohio) taken within the reactors at
different points during the reaction phase of an
operating cycle.
Mixed liquor total suspended solids (MLSS), MLVSS,
and efuent total suspended solids (ESS) were measured
based on Standard Methods [25].
2.4. Floc characterisation
Sludge surface charge was determined by
cationic-anionic titration [26,27]. A 0.002-N hexadimethrine-bromide (Polybrene) solution and a 0.001-N
sodium-salt-polyanetholesulphonic-acid solution were
used as the cationic and the anionic standards,
respectively.
2.5. Sludge settling characteristics
Sludge volume indices (SVIs) [25] and zone settling
velocities (ZSVs) [27] were used for assessing
sludge compressibility and settleability, respectively.
Measurements were conducted within the SBRs
during the settling phase of a cycle. No statistically
signicant differences between SVIs measured within the
reactors and in a 1000 mL graduated cylinder were
obtained.

3593

2.6. Microbiology
The abundance of lamentous bacteria was recorded
9 times during 165 days of operation based on Jenkins
et al.s [29] subjective scoring system: none (0), few (1),
some (2), common (3), very common (4), abundant (5),
excessive (6). Filament identication was conducted
based on Eikelboom types [28].
Protozoa and metazoa were enumerated in
an undiluted mixed liquor sample using a
corpuscle counting chamber (Improved Neubauer
Levy Chamber, Hausser Scientic, Blue Bell, Philadelphia) under phase contrast microscopy at 400 
magnication.

2.7. Statistical analyses

Mean values are reported with 71 standard
deviation, except for the SCOD removals before (Days
1116) and after (Days 117146) the shift from 35
to
45
C (Day 117; as in Fig. 2) and SCOD from days
147165 (as in Fig. 2) for which 95% condence limits
are used.
The statistical signicance of differences between
means from the same SBR before and after a
temperature shift was assessed by paired Students t
hypothesis tests, and the statistical signicance of
differences between means from two different SBRs
was assessed by Students t hypothesis tests for
independent samples and unequal variances, both at
the 95% condence level. The levels of signicance of
the tests (p) are reported for those cases where a
signicant difference was found.
The relationships between sludge settling parameters
(SVI and ZSV), lament abundance, temperature and
ESS were evaluated with the Pearsons product moment
linear coefcient at the 99% or 95% condence
level. Whenever a linear correlation was not
statistically signicant at the 95% condence level, the
relationship was evaluated with the Spearmans rankorder correlation coefcient at the 99% or 95%
condence level.

Table 1
Operating conditions in the 4 SBRs as averages71 standard deviation (from at least 25 observations) calculated from data collected
from day 1 to 165, unless indicated
SBR

Actual SRTa (d)

Average MLVSSa (mg/L)

Inuent SCOD (mg/L)

pH

DOb (mg/L)

1
2
3
4

2678
26710
22711
2577

29007390
29007590
26007400
28007390

374749
368757
372750
372756

7.770.3
7.670.3
7.670.3
7.670.3

2.871.0
3.371.2
4.071.3
4.971.4

a
b

Data from stable conditions after initial acclimation and before transient conditions (days 40120).
Values from DO levels during the react phase from stable and transient conditions (days 40165).

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3594

F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

Fig. 2. Soluble chemical oxygen demand (SCOD) average removals in the 4 SBRs before and after the 3545
C temperature upshifts
(SBRs 1 and 2; SBR4), the 4535
C temperature downshift (SBR2), during 31.540
C temperature oscillations (SBR3), and the period
from day 147 to 165. The error bars represent 95% condence levels.

3. Results and discussion

3.1. Sludge acclimation and 3035
C shift
To isolate the impacts of the temperature transients
on system performance, the hydraulic retention time
(HRT), the SRT, pH, macronutrients availability, and
aeration rate were maintained approximately constant
among the 4 reactors (Table 1). The HRT was set at 12 h
and the SRT was approximately 25 days, which was
achieved for most of the operating period except when
biomass washout occurred due to lamentous bulking
(SRTB22 d in SBR 3) or due to temperature transients
after day 140. Although lower DO levels were maintained in the reactors where the temperature was
increased (SBR1, 2 and 3), the DO concentrations were
on average higher than 2 mg/L in all the SBRs.
The biomass within the 4 SBRs was allowed to
acclimate (B3 SRTs) before shifting the temperature.
Acclimation was considered complete when the MLVSS
concentrations, the SCOD removals, the sludge settling
curves, and the DO uptake proles within a cycle were
relatively constant among the reactors operating at the
same temperature.
SBRs 1 and 4 were started up at 30
C and SBRs 2 and
3 at 35
C. Steady performance was reached in approximately 30 days and the temperature in SBRs 1 and 4 was
increased to 35
C on day 60. The increase in temperature from 30
to 35
C was conducted in duplicate, in
SBRs 1 and 4 at the same time.
During the 165 days of operation, the reaction-phase
SOUR proles were consistent among reactors, both
before and after temperature shifts. This indicated that
the microorganisms had similar oxygen requirements across the 4 reactors, even under temperature
transients.

The performance of SBRs 1 and 4 was not affected by

the 3035
C temperature increase (Day 60); therefore,
this mesophilic temperature shift seems insignicant. In
the 4 reactors, during the rst 116 days of operation, the
SCOD removals were not signicantly different (Days
1116: SBR1=6572%; SBR2=6673%; SBR3=
6972%; SBR4=6772%), the lament abundance
remained within common to very common (3.3
4), the dominant laments were Haliscomenobacterhydrossis-like type and type 021N, the efuent suspended solids (ESS) concentrations were below 30 mg/L,
and the sludge volume indices (SVIs) and the zone
settling velocities (ZSVs) were similar before and after
the shift (Table 2). In addition, there was no signicant
difference in performance among the 4 reactors during
the early acclimation period (Days 360): between SBRs
1 and 4 at 30
C, between SBRs 2 and 3 at 35
C, and
between the SBRs at 30
C and those at 35
C.
The performance of the 4 reactors at 35
C (Days 60
116) was reproducible since no signicant difference in
performance was found among reactors with respect to
all of the parameters measured (SCOD removals, SVI,
ZSV, sludge surface charge, and ESS). The reproducibility in performance obtained by operating the 4 SBRs
in parallel at the same temperature of 35
C for
approximately 60 days ensured that the response of
the reactors under the temperature transients was not
random; this reproducibility is shown by similar
operating values7standard deviation among reactors
(Table 2).
Variable ESS levels, SVIs and ZSVs were observed in
SBR1 and especially in SBR3 during the rst 104 days of
operation, but these were due to lamentous bulking
(Table 2). The incidents of poor sludge compressibility
(SVIs>100 mL/g MLSS) and settleability (ZSVs
o1 cm/min) in SBRs 1 and 3 correlated to lamentous

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F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

3595

Table 2
Operating parameters of the 4 SBRs as averages71 standard deviation before and after the 3035
C shift in SBRs 1 and 4 (day 60)
SBR

1
2a
3a,b
4

SCOD removal (%)

Filament abundance

SVI (mL/g MLSS)

ZSV (cm/min)

ESS (mg/L)

Before

Before

Before

Before

After

Before

After

3.271.8
2.371.8
0.770.5
4.171.1

1974
23717
2477
2073

19711
1875
1697303
2176

6675
66711
6975
6775

After
6578
6775
6977
6776

3.5
33.5
2.83.8
2.83.5

After
3.53.7
3.53.7
3.74
3.5

98742
61719
115756
55711

After
87727
115756
177771
5979

1.871.9
3.571.6
2.371.9
4.071.1

Before=days 1559; After=days 60104, except for the SCOD removals where Before=days 360 and After=days 60112.
a
Reactors continuously at 35
C.
b
Higher variability and/or different after values reect lamentous-bulking incidents.

proliferation (>3.5, common) and high ESS levels

(>30 mg/L, up to 900 mg/L in SBR3), but not to
temperature. These incidents of lamentous bulking in
SBR 1 at 30
C and SBR 3 at 35
C remained without
apparent explanation and point out the potential for
lamentous bacteria to bloom unpredictably.
3.2. Temperature upshift from 35
C to 45
C
The temperature shift from 35
to 45
C was
conducted relatively rapidly in SBR1 (10
C/12 h), and
more slowly (2
C/day) in SBR2. SBR4 was operated as
a control at 35
C. At the same time, SBR3 was operated
under oscillating conditions.
The reactors were further monitored for 29 days, after
which time the sludge in SBRs 1 and 2 was mixed
together in preparation for a temperature downshift
from 45
C to 35
C in SBR2 (Day 146). For this
temperature shift, SBR1 remained as a reference at
45
C.
3.2.1. Soluble chemical oxygen demand (SCOD)
removal
Increasing the temperature (Day 117) from 35
C to
45
C quickly (SBR1) and slowly (SBR2) reduced the
SCOD removals up to 1820% with respect to those of
the control reactor at 35
C (SBR4) (Fig. 2). The SCOD
removals in the constant-temperature reactor (SBR4 at
35
C) were the same before and after the temperature
shift: 6772% (Days 1116) and 6373% (Days 117
146). The SCOD removals in the fast-shift reactor
(SBR1: 5174%) and the slow-shift reactor (SBR2:
4974%) were statistically signicantly lower than
those from the control SBR4 (pSBR1 1:9  105 ;
pSBR2 4:7  105 ) and oscillating SBR3 (pSBR1
0:002; pSBR2 0:0003), which shows the reproducibility
of the effect of increasing the temperature up to 45
C.
No statistically signicant difference in SCOD removals
was observed between conducting the 3545
C temperature shift quickly and slowly. The SCOD-concentration proles over a cycle time were similar among

reactors, and showed that the treated efuent SCOD

concentrations from the fast-shift (SBR1) and slow-shift
(SBR2) reactors were approximately 50 mg/L higher
than those from the oscillating (SBR3) and control
(SBR4) reactors (data not shown).
Although the temperature in SBR2 was later decreased from 45
C to 35
C (Day 147), no statistically
signicant increase in SCOD removal was observed
between operating at 35
C (SBR2: 5875%) and 45
C
(SBR1: 5872%). The SCOD removal in SBR1 after the
3545
C shift (Days 117146: 5174%) increased
signicantly (p 0:017) after operating SBR1 for 19
more days at 45
C (Days 147165: 5872%), thereby
indicating a gradual acclimation. It is possible that the
biomass in SBRs 1 and 2 would have acclimated further,
with higher removal efciencies, if the reactors would
have been operated at 45
C for longer than 29 days
(Days 117146), as reported by Tripathi and Allen [16].
A possible explanation for the decrease in SCOD
removal is microbial activity reduction due to the
readjustment of microbial enzymatic activity. Microbial
metabolic deterioration and microbial death and lysis
could have also led to reduced SCOD removals.
However, the reduction in SCOD removal efciencies
due to the temperature upshift was not correlated with
any change in SOUR proles. Therefore, the release of
soluble products from the sludge ocs due to deocculation and lysis, as reported by Barker and Stuckey [30], is
also a plausible cause of increased efuent SCOD levels.
3.2.2. Sludge settling characteristics
The temperature shifts, both 3545
C upshift and 45
35
C downshift, deteriorated the sludge settling characteristics. Before the 3545
C upshift (Day 117), the
sludge in the 4 SBRs was settling slowly (ZSVp1.5 cm/
min) and had a moderate compressibility (SVI=75
150 mL/g MLSS)(Fig. 3), compared to previous values
of highly settleable (ZSV>2 cm/min) and compressible
(SVI o75 mL/g MLSS) sludge. The 3545
C upshift
(Day 117) caused the sludge compressibility to decrease
further (SBRs 1 and 2: SVI=120210 mL/g MLSS),

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3596

T=35C(4 SBRs)

T=45C(SBR1&2); T=35C(SBR4); T=30-40C(SBR3)

T=45C(SBR1,3&4); T=35C(SBR2)

350
SBR1
SBR2
SBR3
SBR4

SVI (mL/g MLSS)

300
250
200
150
100
50
0
105

110

115

120

125

130

135

140

145

150

155

160

165

Time of operation (Days)

T=35C(4 SBRs)

T=45C(SBR1&2); T=35C(SBR4); T=30-40C(SBR3)

T=45C(SBR1,3&4); T=35C(SBR2)

SBR1
SBR2
SBR3
SBR4

Zone settling velocity

(cm/min)

6
5
4
3
2
1
0
105

110

115

120

125

130

135

140

145

150

155

160

165

Time of operation (Days)

Fig. 3. Sludge volume index (SVI) and zone settling velocity (ZSV) measured in the 4 SBRs before and after the 3545
C temperature
upshifts, the 4535
C temperature downshift, and during temperature oscillations (31.540
C). The SBRs conditions are labelled on
top of each graph.

especially in the fast-shift reactor (SBR1), and the sludge

continued to settle poorly (SBRs 1 and 2: ZSV o1 cm/
min) during the 20 days after the shift. On the contrary,
the compressibility and settleability in the control SBR4
at 35
C improved due to stable operation (SVI
o100 mg/L; ZSV=1.53.1 cm/min).
The poorer sludge compressibility and settleability
after the temperature upshift (in SBRs 1 and 2) were
accompanied by higher ESS levels, due to an increase in
lament abundance (sludge bulking). One cause of high
ESS levels (>100 mg/L), as in the cases of SBRs 1 and 3
shown in Fig. 5, was poor sludge settling characteristics
since the sludge blanket rose above the outlet port where
the treated efuent was discharged, and biomass was
washed out. Filament abundance may have been
promoted by the temperature shifts. A slight increase
in lament abundance (up to B4) with respect to that in
the control reactor (SBR4 at 35
C; lament abundance
B3.53.7) occurred in the fast-shift (SBR1) and slowshift (SBR2) reactors after the 3545
C temperature
shift. The lament abundance in SBR2 remained similar
to that of SBR1 (at 45
C) after decreasing the
temperature from 45
C to 35
C in SBR2 (Day 147).

These results agree with observations of poor sludge

settling at higher temperatures under steady-state
conditions. Settleability reduction (SVI increase) at high
temperatures under steady-state was reported by Carpenter et al. [19] in continuous stirred-tank reactors that
treated pulp and paper mill efuent and operated with
acclimated activated sludge at 37
C, 42
C, 47
C, and
52
C. Krishna and Van Loosdrecht [6] reported a
continuous decrease in sludge settleability (SVI increase)
with increasing temperature (15
C, 20
C, 25
C, 30
C,
and 35
C) in aerobic SBRs treating an acetate medium
under steady state. Some authors report similar sludge
settling characteristics at temperatures between 35
C
and 45
C [12,16], but at steady state. Tripathi [23]
reported higher variability in SVIs during a transient
between 35
C and 45
C than at a constant temperature
of 45
C.
About 25 days after the 3545
C upshift (Days 144
153), the sludge that had been operating at 45
C (SBRs
1 and 2) changed signicantly: a rmer, more compact,
less negatively charged sludge with common abundance
of lamentous organisms and improved settleability and
compressibility was observed. This could be explained

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F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

by acclimation at 45
C in SBRs 1 and 2. The decrease in

temperature in SBR2 from 45
C to 35
C (Day 147) did
not improve or maintain the good sludge compressibility
and settleability in this reactor; similar behaviour and
values of SVI and ZSV were registered in both SBR1
(constant at 45
C) and SBR2 (4535
C downshift).
These observations suggest that both temperature
upshifts and downshifts cause poor sludge compressibility and settleability, and that this condition is
irreversible with respect to temperature downshifts
within the time frame studied.

3597

electrostatic forces at the solidliquid interface of sludge

particles, as indicated by Zita and Hermansson [31] and
Mikkelsen et al. [32]. A more negatively charged sludge
(i.e., less hydrophobic) has been correlated [27] with pinpoint ocs and probably deocculation. The increase in
negative surface charge may have been due to the
presence of more soluble compounds with anionic
functional groups released by oc fragmentation and/
or sludge lysis, as a consequence of the temperature
shift. Negative sludge surface charge under neutral
conditions has been attributed to the presence of anionic
functional groups (e.g., carboxyl, hydroxyl, phosphate
groups) on the sludge oc surface [33,34]. Deocculation
may have also increased the sludge surface area per g of
sludge due to the presence of smaller oc fragments with
increased surface, thereby increasing the sludge surface
charge. Lower sludge hydrophobicity (and presumably
more negatively charged sludge) has been associated
with deocculating sludge under phenol disturbances
and has been partially explained by the effect of cellular
components released by lysis [10]. Lysis may be
explained by cell death, at least in some bacteria and
microfauna, due to irreversible damage as a result of
transient conditions; the cause of deocculation,
although associated with sludge physico-chemical properties, is not known. Further research in this area is
being conducted in our laboratory.
Further evidence of deocculation as a result of the
3545
C shift (Day 117) came from the high ESS levels
(SBRs 1 and 2). High ESS levels (25100 mg/L) were due
to pin-point ocs in suspension in the treated efuent,
which may have come from stressed ocs that became
structurally weak and deocculated. Before the temperature shift, the ESS concentrations amongst the 4
reactors were similar and below 25 mg/L (Fig. 5).
However, after one day of the temperature shift (Day
118), the ESS concentration increased above 25 mg/L in

3.2.3. Sludge deflocculation

The temperature increase from 35
C to 45
C (Day
117; SBRs 1 and 2) caused a net decrease in the sludge
surface charge (Fig. 4). Similar sludge surface charge
values, hence similar sludge physico-chemical characteristics, among the SBRs were measured before the 35
45
C temperature shift (SBRs 1 and 2). A slow
temperature shift (SBR2) in comparison to a faster
one (SBR1) delayed the sludge becoming more negatively charged, but a similar sludge surface charge was
ultimately reached in both reactors after 8 days of the
shift (SBR1: 0.2470.03 meq/g MLSS; SBR2:
0.2470.01 meq/g MLSS; SBR4: 0.1570.01 meq/g
MLSS). This suggests that the factors determining the
sludge charge characteristics are a function of
the temperature rather than of the mode in which the
temperature is attained. The later decrease in temperature from 45
C to 35
C in SBR2 (Day 147) did not
change the sludge charge in SBR2, which remained
similar to that of SBR1 at 45
C. The sludge charge
among SBR1 (at 45
C), SBR2 (at 35
C since day 147),
and SBR4 (at 45
C since day 147) were similar, ranging
from 0.11 to 0.22 meq/g MLSS (Fig. 4).
Sludge surface charge is believed to inuence sludge
oc stability and oc formation due to the interaction of

Time of operation (Days)

Sludge charge (meq/g MLSS)

105
0.00

110

115

120

125

130

135

140

145

150

155

160

165

-0.05
-0.10
-0.15
-0.20
-0.25
-0.30
-0.35

SBR1
SBR2
SBR3
SBR4

-0.40
T=35C(4 SBRs)

T=45C(SBR1&2); T=35C(SBR4); T=30-40C(SBR3)

T=45C(SBR1,3&4); T=35C(SBR2)

Fig. 4. Sludge surface charge in the 4 SBRs before and after the 3545 C temperature upshifts, the 4535
C temperature downshift,
and during temperature oscillations (31.540
C). The error bars represent standard deviations of surface charge measurements.

ARTICLE IN PRESS
F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

3598

T=35C (4 SBRs)

T=45C (SBR1&2); T=35C (SBR4); T=30-40C (SBR3)

T=45C (SBR1,3&4); T=35C (SBR2)

225
200

ESS (mg/L)

175

SBR1
SBR2
SBR3
SBR4

150
125
100
75
50
25
0
105

110

115

120

125

130

135

140

145

150

155

160

165

Time of operation (Days)

Fig. 5. Efuent suspended solids (ESS) in the 4 SBRs before and after the 3545
C temperature upshifts, the 4535
C temperature
downshift, and during temperature oscillations (31.540
C). The error bars represent standard deviations of ESS measurements.

the fast-shift reactor (SBR1). In this fast-shift reactor

(SBR1), high ESS concentrations of 45 mg/L and up to
187 mg/L were registered within 15 days after the shift
(Fig. 5). In contrast, in the slow-shift reactor (SBR2),
only a slight increase in ESS (up to 32 mg/L) was
registered compared with the control at 35
C (SBR4:
ESS o 25 mg/L) and to the period before the shift.
These results show that a 3545
C temperature upshift
produces higher ESS levels, and suggests that the higher
the magnitude of the temperature upshift, the higher the
ESS levels.
There are few reports on ESS levels under temperature transients. Lee et al. [12] mention slight settleability
deterioration as a result of a 3545
C shift in a lab-scale
aerated lagoon treating bleached kraft mill efuent.
Although contradictory results have been reported on
settling at different temperatures when treating pulp mill
efuent, as pointed out by Barr et al. [15], the results
from the present work are consistent with those from
some researchers [16, 35] in that high ESS levels occur at
temperatures higher than 40
C under steady state.
Reproducibility of the effects of the shift from 35
C to
45
C on high ESS levels are demonstrated by the
increase in ESS concentrations in the 4 SBRs when
subjected to temperature transients within this range
(Fig. 5).
After the 4535
C decrease in temperature in SBR2
(Day 147), the ESS levels returned to the normal levels
below 25 mg/L, which supports the idea that while
increasing temperature causes higher ESS levels, decreasing temperature counteracts this effect.
3.2.4. Sludge microorganisms
A shift in the Eikelboom types of laments may have
occurred due to the 3545
C shift. Before the shift in
SBRs 1 and 2, the prevalent types were Haliscomenobacter-hydrossis-like, Thiothrix spp., and types 0041 and

021N; however, after the shift, the dominant types were

type 021N and Thiothrix spp. This is in agreement with
the prevalence of Thiothrix spp. and Type 021N in the
full-scale pulp and paper mill wastewater treatment
plant during the summer, from where the inoculum and
the efuent were collected. In the control reactor at
35
C (SBR4), Haliscomenobacter-hydrossis-like and type
0041 were the dominant types. No further changes in
lament type dominance were recorded. The types of
laments identied in the reactors have been identied
as some of the dominant types in bulking sludge of
activated sludge plants treating pulp and paper mill
efuent [36].
Protozoa and metazoa concentrations decreased
signicantly with the 3545
C temperature shift (SBRs
1 and 2). After the 3545
C shift, the protozoan/
metazoan concentrations in the fast-shift reactor
(SBR1=46,000726,000 microorganisms/mL sludge)
and slow-shift reactor (SBR2=47,000725,000 microorganisms/mL sludge) were signicantly lower than
those in the control at 35
C (SBR4=130,000759,000
microorganisms/mL sludge). Whereas the low concentrations of higher life forms prevailed at 45
C (SBRs 1
and 2), the protozoan/metazoan concentrations increased to about 150,000 microorganisms/mL sludge 2
days after the temperature was decreased from 45
C to
35
C (SBR2, day 147). A diverse microfauna was
observed at 35
C (stalked ciliates, small free-swimming
ciliates, agellates, rotifers, rotifer cysts, and nematodes), but mostly small free-swimming ciliates/agellates and inactive/dead rotifers, inactive/dead stalked
ciliates and inactive/dead nematodes were observed after
the shift (SBRs 1 and 2 at 45
C). These observations
give additional evidence of oc fragmentation since
thriving of small agellates and free-swimming ciliates
may be indicative of deocculation [29] and the presence
of soluble organic matter.

ARTICLE IN PRESS
F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

3.3. Temperature oscillations (31.540
C)

At the same time of the 3545
C temperature shift
(SBRs 1 and 2 on day 117), another SBR (SBR3) was
subjected to a fast temperature increase from 35
C to
40
C, and to periodic temperature oscillating conditions. The oscillations consisted of variations in temperature from 40
C to 31.5
C with a period of 6 days,
operating consecutively for 3 days at 40
C and 3 days at
31.5
C (Fig. 1). After 29 days under oscillations (Day
146), a temperature upshift from 31.5
C to 45
C was
conducted in the oscillating reactor (SBR3) to test the
hypothesis that temperature oscillations select for a
microbial community that handles temperature variations. Also on day 146, the control reactor at 35

(SBR4) was subjected to a 3545
C temperature shift,
after operating for 86 days at a constant temperature of
35
C.
Temperature oscillations (Days 117146) had no
signicant effect on the SCOD removal efciency
(SBR3: SCOD removal=6174%) compared to that of
the control at 35
C (SBR4: SCOD removal=6373%).
Nevertheless, a slight reduction of 5% in SCOD
removals was observed during oscillations (Days 117
146) in the SBR3 compared to the previous removals
before oscillations in the same reactor (Days 1116);
there was a statistically signicant difference (p 0:002)
between the SCOD removals before (6972%) and after
(6174%) oscillations in the SBR3 (Fig. 2). No
statistically signicant differences in SCOD removals
were observed between the oscillating (SBR3) and
control (SBR4) reactors before or after the temperature
upshift to 45
C (Day 146; Fig. 2). Nevertheless, the
sludge settling characteristics, the physico-chemical
sludge characteristics, and ESS concentrations changed
under temperature oscillating conditions.
Under temperature oscillations (SBR3: days 117
146), the sludge settling characteristics deteriorated
steadily with time (Fig. 3). In the oscillating reactor
(SBR3), both the sludge compressibility and settleability
were poor (SVI>100 mL/g MLSS; ZSVo1 cm/min)
compared to those of the control at 35
C (SBR4:
SVIo75 mL/g MLSS and ZSV=13.1 cm/min). After
the temperature increase to 45
C in SBRs 3 and 4 (Day
147), the sludge settling characteristics in the previously
oscillating reactor (SBR3) further deteriorated, and the
SVIs reached values as high as 345 mL/g MLSS
after 6 days of the shift. In the control (SBR4), the
SVI also increased as a result of the temperature upshift
to 45
C and reached similar values as in SBR3 after 13
days of the upshift. This agrees with the previous
observations from the 3545
C shift (SBRs 1 and 2: day
117), and supports the reproducibility of the experiments and the conclusions on the negative impacts of
temperature upshifts on sludge compressibility and
settleability.

3599

This poor sludge settling may have also been a

consequence of lament proliferation. In the oscillating
reactor (SBR3), a change in lament abundance was
scored from B3.7 up to B4 (very common) after
shifting to oscillating conditions, and from B3.8
up to B4.5 after the temperature upshift to 45
C (Day
147). Similarly, in the control (SBR4) an increase in
lament abundance from B3.53.7 to B3.84.1 was
scored after increasing the temperature in this reactor
to 45
C.
The sludge surface became more negatively charged
under temperature oscillations, decreasing steadily (Fig.
4) until it reached a value of 0.3570.03 meq/g MLSS,
the most negative charge measured in the 4 SBRs. This
was signicantly lower (po0:05) than the sludge charge
of the control (SBR4: 0.1570.01 meq/g MLSS). The
sludge surface in the oscillating reactor (SBR3) was
more negatively charged than in the control (SBR4)
before and after the temperature increase to 45
C in
both reactors (Day 147). The sludge surface charge in
SBR4 did not change signicantly after the 3545
C
temperature upshift.
The ESS levels during temperature oscillations (SBR3:
1632 mg/L) were higher than those of the control at
35
C (SBR4: >15 mg/L), and they increased steadily
after 25 days under oscillating conditions (up to 49 mg/
L) and also due to the subsequent upshift to 45
C (Day
47). Although the temperature increase to 45
C in SBR4
was followed by an increase in the ESS concentrations
(above 15 mg/L), this was not as drastic as in the
previous temperature shifts (SBRs 1 and 2); this suggests
that the long run of 86 days under a constant
temperature of 35
C (SBR4) improved the stability
during the transition.
Similar to the 3545
C shift (SBRs 1 and 2), the
temperature increment to 45
C in the oscillating (SBR3)
and control (SBR4) reactors (Day 147) caused a
decrease in protozoan/metazoan concentrations (from
approximately 150,000 to 25,00050,000 microorganisms/mL sludge). Conversely, the temperature oscillations did not cause any change in the protozoan/
metazoan diversity and concentration (B150,000 microorganisms/mL sludge) with respect to those of the
control at 35
C (SBR4). Overall, the changes in
protozoan/metazoan diversity and concentration due
to the temperature shifts suggest that from 35
C to 41
C
a similar, diverse, and active protozoan-metazoan
community exists, and that some microorganisms
survive up to 4145
C.
In conclusion, these types of periodic temperature
oscillations (31.540
C, 6-day period, for 30 days) did
not select for a microbial community that handled
temperature variations (up to 45
C) more robustly. On
the contrary, operating the reactor at a constant
temperature for a long period seemed to have helped
buffer the effect of the 45
C temperature upshift.

ARTICLE IN PRESS
3600

F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601

Table 3
Pearsons product moment linear and Spearmans rank-order correlation (Italics) coefcients among sludge settling parameters,
lament abundance, temperature and ESS for an extended period of operation (174 days) of the 4 SBRs within the temperature range
from 35
C to 50
C
Correlation
SVI vs. lament abundance
ZSV vs. lament abundance
Filament abundance vs. temperature
SVI vs. temperature
ZSV vs. temperature
ESS vs. temperature
a
b

Overall
a

0.61
0.61a
0.46a
0.43a
0.28a
0.59a

N
56
56
56
152
152
280

SBR 1
0.47
0.38
0.23
0.58b
0.31
0.47b

SBR 2

SBR 3

SBR 4

0.22
0.51
0.67b
0.14
0.06
0.61b

0.55
0.79b
0.61b
0.46b
0.44b
0.43b

0.82
0.83b
0.56b
0.66b
0.45b
0.15

n/SBR
14
14
14
38
38
70

Statistically signicant at the 99% condence level.

Statistically signicant at the 95% condence level. N=total pair of observations. n/SBR=pair of observations per reactor.

3.4. Overall correlation of sludge settling characteristics

and temperature
Statistically signicant correlations (Table 3) among
sludge lament abundance, settling characteristics, and
temperature suggest that lament proliferation was
promoted by the temperature upshifts studied here
(lament abundance vs. temperature), and that sludge
settling deteriorated due to lament proliferation (SVI
and ZSV versus temperature and lament abundance).
In addition, an overall correlation of ESS versus
temperature conrmed that the temperature upshifts
within the temperature range examined here lead to
higher ESS concentrations.

4. Conclusions
The temperature upshifts (from 35
C to 45
C) had 2
major effects: a reduction (up to 20%) in SCOD removal
efciency and an increase in efuent suspended solids
(ESS) levels.
Temperature upshifts (from 35
C to 45
C) and
periodic temperature oscillations (from 31.5
C to
40
C, 6-day period, for 30 days) deteriorated the sludge
settling characteristics [poorer sludge compressibility
(high SVIs) and settleability (low ZSVs)] by promoting
lament proliferation.
Poor sludge compressibility and settleability, and high
ESS levels due to the 3545
C shift were attenuated by
a gradual temperature increase (2
C/day), compared to
a faster temperature increase (10
C/12 h) in these
experiments. The SCOD removals, however, decreased
in a similar fashion under fast and slow temperature
upshifts.
Periodic temperature oscillations (from 31.5
C to
40
C, 6-day period, for 30 days) did not select for a
microbial community that handled temperature variations more robustly from the ESS and sludge settling
perspective. These periodic oscillations slightly decreased the SCOD removal efciency in 5%.

Sludge deocculation and poor sludge settling due to

the temperature shifts were the origin of high ESS levels.
Sludge deocculation could have decreased the SCOD
removal efciency by increasing the efuent SCOD
concentrations.
Temperature upshifts (from 35
C to 45
C) and
periodic temperature oscillations (from 31.5
C to
40
C, 6-day period, for 30 days) caused a more
negatively charged sludge, a shift in lamentous organisms, and a reduction in protozoan/metazoan concentrations and diversity.

Acknowledgements
The authors acknowledge the nancial support from
the members of the Consortium Minimizing the Impact
of Pulp and Paper Mill Discharges at the Pulp and
Paper Centre, University of Toronto: Aracruz Celulose,
Carter Holt Harvey Tasman, S.A., Domtar Inc., EKA
Chemicals Inc., Georgia-Pacic Corporation, Irving
Pulp and Paper Ltd., Japan Carlit Co. Ltd., ERCO
worldwide (formerly sterling Pulp Chemicals Ltd.), and
Tembec Inc. In addition, the nancial support from the
Government of Ontario/DuPont Canada Graduate
Scholarship in Science and Technology is gratefully
acknowledged, as well as the partial support from the
Natural Sciences and Engineering Research Council
(NSERC) of Canada. The authors thank Amy Lo at
Domtar Inc. for facilitating wastewater samples.

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