2003_F.Morgan-Sagastume_Effects of temperature transient conditions on aerobic biological treatment of wastewater.pdf

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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 efficiency, solids discharges, sludge physicochemical properties and microbiology. The effects of controlled

temperature shifts (from 35 to 45C; from 45 to 35C) and periodic temperature oscillations (from 31.5C to 40C, 6-

day period, for 30 days) were assessed in 4 parallel, lab-scale sequencing batch reactors (SBRs) that treated pulp and

paper mill effluent.

Overall, the temperature shifts caused higher effluent suspended solids (ESS) levels (25100 mg/L) and a decrease (up

to 20%) in the removal efficiencies of soluble chemical oxygen demand (SCOD). Lower ESS levels were triggered by a

slow (2C/day) versus a fast (10C/12 h) temperature shift from 35 to 45C, but the SCOD removal efficiencies

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 filament 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

efficiency (5% decrease), and did not seem to select for robust microorganisms that withstood the temperature shift.

Sludge deflocculation and filament 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 effluent

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

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

dissolved oxygen (DO), pH, temperature]. The effects

of substrate concentration transients on internal poly-

mer 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, specifically anaerobic condi-

tions, have been related to sludge deflocculation[8], and

toxic transients (e.g., phenol spikes) have induced sludge

ARTICLE IN PRESS

*Corresponding author. Tel.: +1-416-978-8517; fax: +1-

416-971-2106.

E-mail address: [email protected]

(D.G. Allen).

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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deflocculation 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 drastictemperature transients that affect treatment perfor-

mance. 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 effluents,

similar to those from several food processing industries,

are characterised by high temperatures (above 2035C)

[11]. A better understanding of mesophilic and thermo-

philic aerobic treatment of pulp and paper mill effluent

has been achieved, especially, in relation to steady-state

operation at different temperatures [1218]. Neverthe-

less, the effects of temperature transitions on sludgemetabolism, microbial community structure, settling

characteristics, and bioflocculation are not well under-

stood.

Temperature shifts have been related to decreased

treatment performance and system instability [e.g.,

lower activity, poor settling, high effluent suspended

solids (ESS)], as in full-scale biological plants treating

pulp and paper mill effluent over 38C 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].

Effluent turbidity increase has been related to defloccu-

lation and weak flocculation due to a temperature

decrease from 20C to 4C[24].

Biological treatment plants of high-temperature ef-

fluent traditionally operate within the mesophilic tem-perature range of 2535C. In aerobic treatment systems

that operate at the limit of the mesophilic range (35

40C), operating at higher temperatures (e.g., 45C)

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 effluent dilution. Treating industrial effluent

at higher temperatures (e.g., 4045C) may be feasible,

as demonstrated for pulp and paper mill effluent by

Tripathi and Allen [16]. However, the transition

from 3035C to 4045C in the summer, and back to

3035

C in the fall-winter, may represent a challenge

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 ofan activated-sludge-type system. The impacts of a 10C

temperature upshift and a 10C temperature downshift

on the sludge metabolic activity, settling and biofloccu-

lation characteristics were assessed at the upper limit of

mesophilic treatment (3045C). In addition, the poten-

tial 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 effluent

was used in this study. Approximately 2200 L of mill

effluent were collected from the outlet of the primary

clarifier during a period of 1.5 h, and immediately

refrigerated at 4C. 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 fine paper. The

treatment plant handles about 128,000 m3/day of waste-

water.

The biomass used as inoculum (approximately 0.35 L/

reactor) was return-activated-sludge mixed liquor ob-

tained from the same mill wastewater treatment plant,

and was refrigerated until inoculation. The sludge was

aerated for 1 day at room temperature before inoculat-

ing 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 effluent from the mill was transported to our

research laboratory in a refrigerated truck, and then

frozen at 20C. The wastewater was thawed as

required (about 84 L/week). Nitrogen (N) and phos-phorus (P) were added to the thawed, raw mill effluent

as ammonium chloride (NH4Cl; Mallinckrodt Inc.,

Paris, Kentucky) and di-ammonium hydrogen ortho-

phosphate [(NH4)2HPO4; BDH Inc., Toronto, Ontario],

in a soluble-COD:N:P ratio of 200:5:1. The pH of the

feed (conditioned mill effluent) was decreased to 6 by

adding 20% v/v sulphuric acid (H2SO4, Reagent A.C.S.

Fischer Scientific, 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 Scientific, Mississauga, Ontario) at 4

C in a 153-L

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F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 35903601 3591


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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

28C by means of a water bath. The pre-warmed feed at

28C caused the temperature of the sludge in thereactors at 35 or 45C to decrease to a minimum of

33.5C (from 35C) and to a minimum of 40C (from

45C) during feeding, respectively. The initial tempera-

ture of 35 or 45C 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 significant 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 feed-

storage 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 filling phase with mixing, a

reaction phase with continuous mixing and aeration

(385min), 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 filling, 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 effluent.

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 first shift (Day 117), the 4 reactors were

acclimated at 35C, and the sludge was mixed and

redistributed among the 4 SBRs (Day 111). One SBR(SBR1) was subjected to a fast temperature increase

(10C/12 h) from 35 to 45C. A second SBR (SBR2)

was subjected to a slow, 2C/day temperature increase

during 5 days to achieve a net increase from 35 to 45C.

The temperature in a third SBR (SBR3) was initially

increased from 35 to 40C, and after 3 days at 40C,

decreased to approximately 32.5C to begin periodic

temperature oscillations from 31.5 to 40C with a 6-

day period. The fourth reactor (SBR4) acted as control

at 35C for the temperature shifts, and provided for a

paired experiment showing that the shift effects were not

due to random operating characteristics.

Twenty-nine days after the first 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 45C, the temperature in SBR2 was

decreased from 45 to 35C, SBR3 was subjected to

an increase from 31.5 to 45C, and the temperature in

SBR4 was increased from 35 to 45C. In this case, the

reactor performance after 4535C decrease (SBR2) was

compared to that under constant temperature at 45C

(SBR1), and the effects of a 31.545C increase after

temperature oscillations (SBR3) were compared to those

of a 3545C increase after constant temperature

operation at 35C (SBR4).

The reactors temperature was monitored with 76 mm

mercury thermometers. Deep-chamber water baths

(3 SBRs: 33 L, 1295 PC, VWR Scientific, Mississauga,

Ontario; 1 SBR: MagniWhirl Constant Temperature

Bath, Blue M Electric Company, Blue Island, Illinois)

connected to the reactors water jackets were used tocontrol the reactors temperatures. The accuracy of the

temperature readings was 71C.

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 effluent

discharged and collected at the end of a cycle. The

samples were filtered through 1.5-mm-pore-size glass

microfibre filters (934-AH, Whatman Inc., Clifton, New

Jersey), and stored at 4

C before digestion. COD

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30

35

40

45

50

100 110 120 130 140 150 160 170

Time of operation (days)

T

emperature(C)

SBR1

SBR2

30

35

40

45

50

100 110 120 130 140 150 160 170

Time of operation (days)

Temperature(C)

SBR3

SBR4

(B)

(A)

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

temperature upshift, the 4535C temperature downshift, and

during temperature oscillations. (A) Profiles of SBRs 1 and 2

and (B) profiles of SBRs 3 and 4.

F. Morgan-Sagastume, D.G. Allen / Water Research 37 (2003) 359036013592


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measurement in the filtrates was conducted following

Standard Methods[25].

The total COD of the fresh raw pulp mill effluent

when collected was about 800 mg/L. The average

SCOD of the effluent was 578720mg/L before

storage at 20C. A reduction in the SCOD levels

of the original effluent took place after freezing,thawing and refrigerating the effluent. 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

effluent; however, the 4 SBRs were fed with the same

prepared batches of mill effluent.

Specific 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 effluent 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 hexadi-

methrine-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

significant differences between SVIs measured within the

reactors and in a 1000 mL graduated cylinder were

obtained.

2.6. Microbiology

The abundance of filamentous 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 identification was conductedbased 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 Scientific, Blue Bell, Philadel-

phia) under phase contrast microscopy at 400

magnification.

2.7. Statistical analyses

Mean values are reported with 71 standarddeviation, except for the SCOD removals before (Days

1116) and after (Days 117146) the shift from 35 to

45C (Day 117; as in Fig. 2) and SCOD from days

147165 (as in Fig. 2) for which 95% confidence limits

are used.

The statistical significance 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 significance 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% confidence level. The levels of significance of

the tests (p) are reported for those cases where a

significant difference was found.

The relationships between sludge settling parameters

(SVI and ZSV), filament abundance, temperature and

ESS were evaluated with the Pearsons product moment

linear coefficient at the 99% or 95% confidence

level. Whenever a linear correlation was not

statistically significant at the 95% confidence level, the

relationship was evaluated with the Spearmans rank-

order correlation coefficient at the 99% or 95%

confidence level.

ARTICLE IN PRESS

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) Influent SCOD (mg/L) pH DOb (mg/L)

1 2678 29007390 374749 7.770.3 2.871.0

2 26710 29007590 368757 7.670.3 3.371.2

3 22711 26007400 372750 7.670.3 4.071.3

4 2577 28007390 372756 7.670.3 4.971.4

aData from stable conditions after initial acclimation and before transient conditions (days 40120).b

Values from DO levels during the react phase from stable and transient conditions (days 40165).



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3. Results and discussion

3.1. Sludge acclimation and 3035C 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 filamentous bulking

(SRTB22 d in SBR 3) or due to temperature transients

after day 140. Although lower DO levels were main-

tained 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 profiles within a cycle were

relatively constant among the reactors operating at the

same temperature.SBRs 1 and 4 were started up at 30C and SBRs 2 and

3 at 35C. Steady performance was reached in approxi-

mately 30 days and the temperature in SBRs 1 and 4 was

increased to 35C on day 60. The increase in tempera-

ture from 30 to 35C was conducted in duplicate, in

SBRs 1 and 4 at the same time.

During the 165 days of operation, the reaction-phase

SOUR profiles were consistent among reactors, both

before and after temperature shifts. This indicated that

the microorganisms had similar oxygen require-

ments across the 4 reactors, even under temperature

transients.

The performance of SBRs 1 and 4 was not affected by

the 3035C temperature increase (Day 60); therefore,

this mesophilic temperature shift seems insignificant. In

the 4 reactors, during the first 116 days of operation, the

SCOD removals were not significantly different (Days

1116: SBR1=6572%; SBR2=6673%; SBR3=

6972%; SBR4=6772%), the filament abundance

remained within common to very common (3.3

4), the dominant filaments were Haliscomenobacter-

hydrossis-like type and type 021N, the effluent sus-

pended 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 significant

difference in performance among the 4 reactors during

the early acclimation period (Days 360): between SBRs

1 and 4 at 30C, between SBRs 2 and 3 at 35C, and

between the SBRs at 30C and those at 35C.

The performance of the 4 reactors at 35C (Days 60

116) was reproducible since no significant 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 reproduci-

bility in performance obtained by operating the 4 SBRsin parallel at the same temperature of 35C 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 first 104 days of

operation, but these were due to filamentous 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 filamentous

ARTICLE IN PRESS

Fig. 2. Soluble chemical oxygen demand (SCOD) average removals in the 4 SBRs before and after the 3545C temperature upshifts

(SBRs 1 and 2; SBR4), the 4535C temperature downshift (SBR2), during 31.540C temperature oscillations (SBR3), and the period

from day 147 to 165. The error bars represent 95% confidence levels.



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proliferation (>3.5, common) and high ESS levels

(>30mg/L, up to 900 mg/L in SBR3), but not to

temperature. These incidents of filamentous bulking in

SBR 1 at 30C and SBR 3 at 35C remained without

apparent explanation and point out the potential forfilamentous bacteria to bloom unpredictably.

3.2. Temperature upshift from 35C to 45C

The temperature shift from 35 to 45C was

conducted relatively rapidly in SBR1 (10C/12 h), and

more slowly (2C/day) in SBR2. SBR4 was operated as

a control at 35C. 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 downshiftfrom 45C t o 3 5C in SBR2 (Day 146). For this

temperature shift, SBR1 remained as a reference at

45C.

3.2.1. Soluble chemical oxygen demand (SCOD)

removal

Increasing the temperature (Day 117) from 35C to

45C quickly (SBR1) and slowly (SBR2) reduced the

SCOD removals up to 1820% with respect to those of

the control reactor at 35C (SBR4) (Fig. 2). The SCOD

removals in the constant-temperature reactor (SBR4 at

35

C) were the same before and after the temperatureshift: 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 significantly 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 45C.

No statistically significant difference in SCOD removals

was observed between conducting the 3545C tem-

perature shift quickly and slowly. The SCOD-concen-

tration profiles over a cycle time were similar among

reactors, and showed that the treated effluent 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 de-

creased from 45C to 35C (Day 147), no statistically

significant increase in SCOD removal was observed

between operating at 35C (SBR2: 5875%) and 45C

(SBR1: 5872%). The SCOD removal in SBR1 after the

3545C shift (Days 117146: 5174%) increased

significantly (p 0:017) after operating SBR1 for 19

more days at 45C (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 efficiencies, 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 efficiencies

due to the temperature upshift was not correlated with

any change in SOUR profiles. Therefore, the release of

soluble products from the sludge flocs due to defloccula-

tion and lysis, as reported by Barker and Stuckey[30], is

also a plausible cause of increased effluent SCOD levels.

3.2.2. Sludge settling characteristics

The temperature shifts, both 3545C upshift and 45

35C downshift, deteriorated the sludge settling char-

acteristics. Before the 3545C upshift (Day 117), the

sludge in the 4 SBRs was settling slowly (ZSVp1.5cm/

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 3545C upshift

(Day 117) caused the sludge compressibility to decrease

further (SBRs 1 and 2: SVI=120210 mL/g MLSS),

ARTICLE IN PRESS

Table 2

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

SBR SCOD removal (%) Filament abundance SVI (mL/g MLSS) ZSV (cm/min) ESS (mg/L)

Before After Before After Before After Before After Before After

1 6675 6578 3.5 3.53.7 98742 87727 1.871.9b 3.271.8 1974 19711

2a 66711 6775 33.5 3.53.7 61719 115756 3.571.6 2.371.8 23717 1875

3a,b 6975 6977 2.83.8 3.74 115756 177771 2.371.9 0.770.5 2477 1697303

4 6775 6776 2.83.5 3.5 55711 5979 4.071.1 4.171.1 2073 2176

Before=days 1559; After=days 60104, except for the SCOD removals where Before=days 360 and After=days 60112.aReactors continuously at 35C.bHigher variability and/or different after values reflect filamentous-bulking incidents.



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

continued to settle poorly (SBRs 1 and 2: ZSV o1cm/

min) during the 20 days after the shift. On the contrary,

the compressibility and settleability in the control SBR4

at 35C 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

filament abundance (sludge bulking). One cause of high

ESS levels (>100 mg/L), as in the cases of SBRs 1 and 3shown inFig. 5, was poor sludge settling characteristics

since the sludge blanket rose above the outlet port where

the treated effluent was discharged, and biomass was

washed out. Filament abundance may have been

promoted by the temperature shifts. A slight increase

in filament abundance (up to B4) with respect to that in

the control reactor (SBR4 at 35C; filament abundance

B3.53.7) occurred in the fast-shift (SBR1) and slow-

shift (SBR2) reactors after the 3545C temperature

shift. The filament abundance in SBR2 remained similar

to that of SBR1 (at 45C) 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 Car-

penter et al.[19] in continuous stirred-tank reactors that

treated pulp and paper mill effluent and operated with

acclimated activated sludge at 37C, 42C, 47C, and

52C. Krishna and Van Loosdrecht [6] reported a

continuous decrease in sludge settleability (SVI increase)

with increasing temperature (15C, 20C, 25C, 30C,

and 35

C) in aerobic SBRs treating an acetate mediumunder steady state. Some authors report similar sludge

settling characteristics at temperatures between 35C

and 45C [12,16], but at steady state. Tripathi [23]

reported higher variability in SVIs during a transient

between 35C and 45C than at a constant temperature

of 45C.

About 25 days after the 3545C upshift (Days 144

153), the sludge that had been operating at 45C (SBRs

1 and 2) changed significantly: a firmer, more compact,

less negatively charged sludge with common abundance

of filamentous organisms and improved settleability and

compressibility was observed. This could be explained

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300

350

105 110 115 120 125 130 135 140 145 150 155 160 165

Time of operation (Days)

SVI(mL/g

MLSS)

SBR1

SBR2

SBR3

SBR4

T=35C(4 SBRs) T=45C(SBR1&2); T=35C(SBR4); T=30-40C(SBR3) T=45C(SBR1,3&4); T=35C(SBR2)

0

1

2

3

4

5

6

7

105 110 115 120 125 130 135 140 145 150 155 160 165


Zonesettlingvelocity

(cm/min)

SBR1

SBR2

SBR3

SBR4


Fig. 3. Sludge volume index (SVI) and zone settling velocity (ZSV) measured in the 4 SBRs before and after the 3545C temperature

upshifts, the 4535C temperature downshift, and during temperature oscillations (31.540C). The SBRs conditions are labelled on

top of each graph.



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

temperature in SBR2 from 45C to 35C (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 45C) and SBR2 (4535C downshift).

These observations suggest that both temperatureupshifts and downshifts cause poor sludge compressi-

bility and settleability, and that this condition is

irreversible with respect to temperature downshifts

within the time frame studied.

3.2.3. Sludge deflocculation

The temperature increase from 35C to 45C (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 character-

istics, among the SBRs were measured before the 35

45

C temperature shift (SBRs 1 and 2). A slowtemperature shift (SBR2) in comparison to a faster

one (SBR1) delayed the sludge becoming more nega-

tively charged, but a similar sludge surface charge was

ultimately reached in both reactors after 8 days of the

shift (SBR1: 0.2470.03meq/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 tempera-

ture from 45C to 35C in SBR2 (Day 147) did not

change the sludge charge in SBR2, which remained

similar to that of SBR1 at 45C. The sludge charge

among SBR1 (at 45C), SBR2 (at 35C since day 147),

and SBR4 (at 45C since day 147) were similar, ranging

from 0.11 to 0.22 meq/g MLSS (Fig. 4).

Sludge surface charge is believed to influence sludge

floc stability and floc formation due to the interaction of

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 pin-

point flocs and probably deflocculation. The increase in

negative surface charge may have been due to the

presence of more soluble compounds with anionicfunctional groups released by floc 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 floc surface[33,34]. Deflocculation

may have also increased the sludge surface area per g of

sludge due to the presence of smaller floc fragments with

increased surface, thereby increasing the sludge surface

charge. Lower sludge hydrophobicity (and presumably

more negatively charged sludge) has been associated

with deflocculating sludge under phenol disturbancesand 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 deflocculation,

although associated with sludge physico-chemical prop-

erties, is not known. Further research in this area is

being conducted in our laboratory.

Further evidence of deflocculation as a result of the

3545C shift (Day 117) came from the high ESS levels

(SBRs 1 and 2). High ESS levels (25100 mg/L) were due

to pin-point flocs in suspension in the treated effluent,

which may have come from stressed flocs that became

structurally weak and deflocculated. Before the tem-

perature shift, the ESS concentrations amongst the 4

reactors were similar and below 25mg/L (Fig. 5).

However, after one day of the temperature shift (Day

118), the ESS concentration increased above 25 mg/L in

ARTICLE IN PRESS

-0.40

-0.35

-0.30

-0.25

-0.20

-0.15

-0.10

-0.05

0.00105 110 115 120 125 130 135 140 145 150 155 160 165


Sludgecharge(meq/gM

LSS)

SBR1

SBR2

SBR3

SBR4


Fig. 4. Sludge surface charge in the 4 SBRs before and after the 3545C temperature upshifts, the 4535C temperature downshift,

and during temperature oscillations (31.540

C). The error bars represent standard deviations of surface charge measurements.



9/12

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 32mg/L) was

registered compared with the control at 35C (SBR4:

ESS o 25 mg/L) and to the period before the shift.

These results show that a 3545C 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 tempera-

ture transients. Lee et al. [12]mention slight settleability

deterioration as a result of a 3545C shift in a lab-scale

aerated lagoon treating bleached kraft mill effluent.

Although contradictory results have been reported on

settling at different temperatures when treating pulp mill

effluent, 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 40C under steady state.

Reproducibility of the effects of the shift from 35C to

45C 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 4535C 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, de-

creasing temperature counteracts this effect.

3.2.4. Sludge microorganisms

A shift in the Eikelboom types of filaments may have

occurred due to the 3545C shift. Before the shift in

SBRs 1 and 2, the prevalent types were Haliscomeno-

bacter-hydrossis -like,Thiothrixspp., 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 ofThiothrix spp. and Type 021N in the

full-scale pulp and paper mill wastewater treatment

plant during the summer, from where the inoculum and

the effluent were collected. In the control reactor at

35C (SBR4), Haliscomenobacter-hydrossis-like and type

0041 were the dominant types. No further changes in

filament type dominance were recorded. The types of

filaments identified in the reactors have been identified

as some of the dominant types in bulking sludge of

activated sludge plants treating pulp and paper mill

effluent [36].

Protozoa and metazoa concentrations decreased

significantly with the 3545C temperature shift (SBRs

1 and 2). After the 3545C 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 micro-

organisms/mL sludge) were significantly lower than

those in the control at 35C (SBR4=130,000759,000

microorganisms/mL sludge). Whereas the low concen-

trations of higher life forms prevailed at 45C (SBRs 1

and 2), the protozoan/metazoan concentrations in-

creased to about 150,000 microorganisms/mL sludge 2days after the temperature was decreased from 45C to

35C (SBR2, day 147). A diverse microfauna was

observed at 35C (stalked ciliates, small free-swimming

ciliates, flagellates, rotifers, rotifer cysts, and nema-

todes), but mostly small free-swimming ciliates/flagel-

lates and inactive/dead rotifers, inactive/dead stalked

ciliates and inactive/dead nematodes were observed after

the shift (SBRs 1 and 2 at 45C). These observations

give additional evidence of floc fragmentation since

thriving of small flagellates and free-swimming ciliates

may be indicative of deflocculation[29]and the presence

of soluble organic matter.

ARTICLE IN PRESS

0

25

50

75

100125

150

175

200

225

105 110 115 120 125 130 135 140 145 150 155 160 165


ESS(m

g/L)

SBR1SBR2

SBR3

SBR4

T=35C (4 SBRs) T=45C (SBR1&2); T=35C (SBR4); T=30-40C (SBR3) T=45C (SBR1,3&4); T=35C (SBR2)

Fig. 5. Effluent suspended solids (ESS) in the 4 SBRs before and after the 3545C temperature upshifts, the 4535C temperature

downshift, and during temperature oscillations (31.540C). The error bars represent standard deviations of ESS measurements.



10/12

3.3. Temperature oscillations (31.540C)

At the same time of the 3545C temperature shift

(SBRs 1 and 2 on day 117), another SBR (SBR3) was

subjected to a fast temperature increase from 35C to

40C, and to periodic temperature oscillating condi-

tions. The oscillations consisted of variations in tem-perature from 40C to 31.5C with a period of 6 days,

operating consecutively for 3 days at 40C and 3 days at

31.5C (Fig. 1). After 29 days under oscillations (Day

146), a temperature upshift from 31.5C to 45C was

conducted in the oscillating reactor (SBR3) to test the

hypothesis that temperature oscillations select for a

microbial community that handles temperature varia-

tions. Also on day 146, the control reactor at 35

(SBR4) was subjected to a 3545C temperature shift,

after operating for 86 days at a constant temperature of

35C.

Temperature oscillations (Days 117146) had nosignificant effect on the SCOD removal efficiency

(SBR3: SCOD removal=6174%) compared to that of

the control at 35C (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 significant difference (p 0:002)

between the SCOD removals before (6972%) and after

(6174%) oscillations in the SBR3 (Fig. 2). No

statistically significant differences in SCOD removals

were observed between the oscillating (SBR3) and

control (SBR4) reactors before or after the temperature

upshift to 45C (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 35C (SBR4:

SVIo75 mL/g MLSS and ZSV=13.1 cm/min). After

the temperature increase to 45

C in SBRs 3 and 4 (Day147), 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 45C and reached similar values as in SBR3 after 13

days of the upshift. This agrees with the previous

observations from the 3545C shift (SBRs 1 and 2: day

117), and supports the reproducibility of the experi-

ments and the conclusions on the negative impacts of

temperature upshifts on sludge compressibility and

settleability.

This poor sludge settling may have also been a

consequence of filament proliferation. In the oscillating

reactor (SBR3), a change in filament 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 45C (Day

147). Similarly, in the control (SBR4) an increase infilament abundance from B3.53.7 to B3.84.1 was

scored after increasing the temperature in this reactor

to 45C.

The sludge surface became more negatively charged

under temperature oscillations, decreasing steadily (Fig.

4) until it reached a value of0.3570.03 meq/g MLSS,

the most negative charge measured in the 4 SBRs. This

was significantly 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 inboth reactors (Day 147). The sludge surface charge in

SBR4 did not change significantly after the 3545C

temperature upshift.

The ESS levels during temperature oscillations (SBR3:

1632 mg/L) were higher than those of the control at

35C (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 45C (Day

47). Although the temperature increase to 45C in SBR4

was followed by an increase in the ESS concentrations

(above 15mg/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 35C (SBR4) improved the stability

during the transition.

Similar to the 3545C shift (SBRs 1 and 2), the

temperature increment to 45C 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 microorgan-

isms/mL sludge). Conversely, the temperature oscilla-

tions did not cause any change in the protozoan/

metazoan diversity and concentration (B150,000 micro-

organisms/mL sludge) with respect to those of the

control at 35

C (SBR4). Overall, the changes inprotozoan/metazoan diversity and concentration due

to the temperature shifts suggest that from 35C to 41C

a similar, diverse, and active protozoan-metazoan

community exists, and that some microorganisms

survive up to 4145C.

In conclusion, these types of periodic temperature

oscillations (31.540C, 6-day period, for 30 days) did

not select for a microbial community that handled

temperature variations (up to 45C) 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



11/12

3.4. Overall correlation of sludge settling characteristics

and temperature

Statistically significant correlations (Table 3) amongsludge filament abundance, settling characteristics, and

temperature suggest that filament proliferation was

promoted by the temperature upshifts studied here

(filament abundance vs. temperature), and that sludge

settling deteriorated due to filament proliferation (SVI

and ZSV versus temperature and filament abundance).

In addition, an overall correlation of ESS versus

temperature confirmed that the temperature upshifts

within the temperature range examined here lead to

higher ESS concentrations.

4. Conclusions

The temperature upshifts (from 35C to 45C) had 2

major effects: a reduction (up to 20%) in SCOD removal

efficiency and an increase in effluent suspended solids

(ESS) levels.

Temperature upshifts (from 35C to 45C) and

periodic temperature oscillations (from 31.5C to

40C, 6-day period, for 30 days) deteriorated the sludge

settling characteristics [poorer sludge compressibility

(high SVIs) and settleability (low ZSVs)] by promoting

filament proliferation.

Poor sludge compressibility and settleability, and highESS levels due to the 3545C shift were attenuated by

a gradual temperature increase (2C/day), compared to

a faster temperature increase (10C/12h) in these

experiments. The SCOD removals, however, decreased

in a similar fashion under fast and slow temperature

upshifts.

Periodic temperature oscillations (from 31.5C to

40C, 6-day period, for 30 days) did not select for a

microbial community that handled temperature varia-

tions more robustly from the ESS and sludge settling

perspective. These periodic oscillations slightly de-

creased the SCOD removal efficiency in 5%.

Sludge deflocculation and poor sludge settling due to

the temperature shifts were the origin of high ESS levels.

Sludge deflocculation could have decreased the SCOD

removal efficiency by increasing the effluent SCODconcentrations.

Temperature upshifts (from 35C to 45C) and

periodic temperature oscillations (from 31.5C to

40C, 6-day period, for 30 days) caused a more

negatively charged sludge, a shift in filamentous organ-

isms, and a reduction in protozoan/metazoan concen-

trations and diversity.

Acknowledgements

The authors acknowledge the financial support fromthe 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-Pacific Corporation, Irving

Pulp and Paper Ltd., Japan Carlit Co. Ltd., ERCO

worldwide (formerly sterling Pulp Chemicals Ltd.), and

Tembec Inc. In addition, the financial 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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ARTICLE IN PRESS

Table 3

Pearsons product moment linear and Spearmans rank-order correlation (Italics) coefficients among sludge settling parameters,

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