Science of the Total Environment 615 (2018) 1176–1191

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Organophosphonates: A review on environmental relevance,

biodegradability and removal in wastewater treatment plants
Eduard Rott a,⁎, Heidrun Steinmetz b, Jörg W. Metzger a
a
Institute for Sanitary Engineering, Water Quality and Solid Waste Management, University of Stuttgart, Bandtäle 2, 70569 Stuttgart, Germany
b
Chair of Resource Efficient Wastewater Technology, University of Kaiserslautern, Paul-Ehrlich-Str. 14, 67663 Kaiserslautern, Germany

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Phosphonates are removed with N 80%

from wastewater treatment plants
(WWTPs).
• Sole enhanced biological phosphorus
removal may not lead to such high re-
moval rates.
• To date, phosphonates may not remobi-
lize heavy metals from sediment signifi-
cantly.
• Phosphonates, except some degradation
products, are harmless to most aquatic
organisms.
• Phosphonates contribute to eutrophica-
tion and interfere with phosphate re-
moval in WWTPs.

a r t i c l e i n f o a b s t r a c t

Article history: The worldwide increasing consumption of the phosphonates 2-phosphonobutane-1,2,4-tricarboxylic acid
Received 10 August 2017 [PBTC], 1-hydroxyethane 1,1-diphosphonic acid [HEDP], nitrilotris(methylene phosphonic acid) [NTMP],
Received in revised form 18 September 2017 ethylenediamine tetra(methylene phosphonic acid) [EDTMP] and diethylenetriamine penta(methylene phos-
Accepted 21 September 2017
phonic acid) [DTPMP] over the past decades put phosphonates into focus of environmental scientists and agen-
Available online xxxx
cies, as they are increasingly discussed in the context of various environmental problems. The hitherto difficult
Editor: D. Barcelo analysis of phosphonates contributed to the fact that very little is known about their concentrations and behavior
in the environment. This work critically reviews the existing literature up to the year 2016 on the potential en-
Keywords: vironmental relevance of phosphonates, their biotic and abiotic degradability, and their removal in wastewater
Phosphonates treatment plants (WWTPs). Accordingly, despite their stability against biological degradation, phosphonates
Degradation can be removed with relatively high efficiency (N 80%) in WWTPs operated with chemical phosphate precipita-
Biodegradability tion. In the literature, however, to our knowledge, there is no information as to whether an enhanced biological
Phosphate precipitation phosphorus removal alone is sufficient for such high removal rates and whether the achievable phosphonate
Eutrophication
concentrations in effluents are sufficiently low to prevent eutrophication. It is currently expected that
phosphonates, although being complexing agents, do not remobilize heavy metals from sediments in a signifi-
cant amount since the phosphonate concentrations required for this (N 50 μg/L) are considerably higher
than the concentrations determined in surface waters. Various publications also point out that phosphonates
are harmless to a variety of aquatic organisms. Moreover, degradation products thereof such as N-
(phosphonomethyl)glycine and aminomethylphosphonic acid are regarded as being particularly critical. Despite
their high stability against biological degradation, phosphonates contribute to eutrophication due to abiotic deg-
radation (mainly photolysis). Furthermore, the literature reports on the fact that phosphonates in high

⁎ Corresponding author.
E-mail address: eduard.rott@iswa.uni-stuttgart.de (E. Rott).

https://doi.org/10.1016/j.scitotenv.2017.09.223
0048-9697/© 2017 Elsevier B.V. All rights reserved.
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191 1177

concentrations interfere with phosphate precipitation in WWTPs. Thus, it is recommended to remove

phosphonates, in particular from industrial wastewaters, before discharging them into water bodies or WWTPs.
© 2017 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1177
1.1. Motivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1177
1.2. Physicochemical properties of phosphonates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1178
1.3. Areas of application of phosphonates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1178
1.4. Phosphonate analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1179
2. Biodegradability of phosphonates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1179
2.1. C\\P bond cleavage by bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1179
2.2. Aerobic and anaerobic degradation tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1180
3. Phosphonate adsorption onto activated and digested sludge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1180
3.1. Adsorption onto activated sludge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1180
3.2. Adsorption onto digested sludge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1181
4. Phosphonate removal in municipal wastewater treatment plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1182
5. Effect of phosphonates on chemical phosphate precipitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1183
6. Environmental relevance of phosphonates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1183
6.1. Phosphonates in the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1183
6.2. Environmental behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1185
6.3. Ecotoxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1185
6.4. Contribution to eutrophication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1186
6.5. Remobilization of heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1187
7. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1188
8. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1188
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1189
Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1189
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1189

1. Introduction
1.1. Motivation
In nature, phosphorus is the main limiting factor for biomass growth.
Thus, its removal from wastewater is a significant means to reduce the
amount of nutrients entering the aqueous environment and thereby
preventing algal bloom and eutrophication of water. Within the scope
of the European Water Framework Directive (EU, 2000), environmental
objectives have been defined which in some cases require higher phos-
phorus removal efficiencies in wastewater treatment plants (WWTPs)
to achieve a good quality of water bodies. For this reason, for WWTPs
in Europe target values of 0.1–0.5 mg/L total P (depending on the size
of the WWTP) have already been established. WWTP operators can
meet these more stringent requirements, among others by means of im-
proved precipitant dosing and a more efficient secondary clarification.
However, the optimization potentials are limited since the P removal ef-
ficiency depends on the composition with respect to the different kinds
of phosphorous compounds present in the wastewater.
With the beginning of the usage of phosphonates in the formulations
of washing agents (Grohmann and Horstmann, 1989) and their applica-
tion in technical processes (Reichert, 1996), the fraction of dissolved
organic phosphorus (DOP) (cDOP = cdissolved P − cinorganic P; c: concentra-
tion) in the effluents of European WWTPs started to increase
substantially (Neft et al., 2010; Gu et al., 2011). Phosphonates have al-
ready been identified in the influents of several German and Swiss
WWTPs as part of the DOP (Fürhacker et al., 2005; Nowack, 1998,
2002b). Furthermore, due to their high tendency to adsorb onto particu-
late matter and solid surfaces (Nowack, 2003), phosphonates contribute
to the particulate phosphorus fraction (PP) (cPP = ctotal P − cdissolved P). In
particular, the DOP fraction is increasingly problematic for WWTP oper-
ators, as it cannot be reliably removed by P precipitation, thus making it
more difficult to meet the required target values (Neft et al., 2010).
The quantitatively most important phosphonates are 2-
phosphonobutane-1,2,4-tricarboxylic acid (PBTC), 1-hydroxyethane
1,1-diphosphonic acid (HEDP), nitrilotris(methylene phosphonic
acid), ethylenediamine tetra(methylene phosphonic acid) (EDTMP)
and diethylenetriamine penta(methylene phosphonic acid) (DTPMP).
These compounds are versatile metal complexing agents forming
complexes of high stability (Gledhill and Feijtel, 1992) and act as
“thresholders” which are effective also in low, i.e., substoichiometric
concentrations (Maise, 1984). Due to these properties, they are used
in the paper and textile industries, for water conditioning and they are
added to household and industrial cleaning products. In the early
1990s, the Europe-wide polyphosphonate consumption (excluding
PBTC) was 11,820 t/a (Gledhill and Feijtel, 1992). Davenport et al.
(2000), cited by Nowack (2003), estimated the phosphonate use for
1998 in Europe at 15,000 t/a and the worldwide use at 56,000 t/a. For
2012, the European Phosphonate Association indicated a European
phosphonate consumption of 49,000 t/a and a worldwide consumption
of 94,000 t/a (EPA, 2013). Unfortunately, EPA (2013) did not provide
more detailed data on the distribution of phosphonate consumption in
other continents. The enormous increase in Europe is paralleled by the
global phosphonate consumption, which was 56,000 t/a in 1998
(Davenport et al., 2000) and grew by about 70% to 94,000 t/a in 2012
(EPA, 2013).
With this enormous increase in consumption, phosphonates are
discussed more and more from an environmental point of view and
in connection with various problems such as eutrophication of water,
potential remobilization of heavy metals, the formation of critical
1178 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191

degradation products, and the interference with phosphate precipita-
tion as well as the aggravating compliance with phosphorus limits on
WWTPs. This review summarizes the current findings up to the year
2016 on the biodegradability and removal of phosphonates in WWTPs
and gives an overview on the existing literature regarding their environ-
mental relevance.
and Held-Beller, 1993). Thus, the strongly pronounced pH stability of
phosphonates against oxidative and thermal decomposition enable
their use as bleaching stabilizer in bleaching liquors, where high tem-
peratures prevail at high pH.
• Household and industrial cleaners:

1.2. Physicochemical properties of phosphonates

In phosphonic acids and their salts, the phosphonates, the phospho-
rus atom has the oxidation state +3, whereas the most frequent oxida-
tion state for inorganic phosphorus in nature is + 5, as found, e.g., in
ortho-phosphoric acid (H3PO4) or ortho-phosphates. Table 1 gives an
overview of the characteristics of the most widely used phosphonates
PBTC, HEDP, NTMP, EDTMP and DTPMP (structural formulae see Fig. 1).
The phosphonates listed in Table 1 can be divided into two
groups, the group of nitrogen-free phosphonates, which also carry
characteristic carboxyl and hydroxyl groups, and into the group
of aminophosphonates having three to five phosphonate groups
(C–PO(OH)2). Phosphonates with more than one phosphonate group
are also termed ‘polyphosphonates’. Phosphonic acids and in particular
their salts have a high solubility in water (≥21 g/L), a low solubility in
organic solvents (log Kow b −1.3) and a very low volatility (Henry con-
stant b6 ∙ 10− 17 atm ∙ m3/mol) (Nowack, 2003; Gledhill and Feijtel,
1992; RSC, 2016; HERA, 2004).
1.3. Areas of application of phosphonates
Phosphonates are used as complexing agent, scaling inhibitor and
bleaching stabilizer (Nowack, 2003).
• Membrane filtration:
The addition of phosphonates as antiscalants counteracts the
blocking of the membrane.
• Conditioning of cooling water:
Circulation cooling systems are particularly affected by scaling and
related troublesome deposits of precipitates such as calcium carbonate
and calcium phosphate due to the intended evaporation of the cooling
water (Gartiser and Urich, 2002). Phosphonates can sub-
stoichiometrically complex “free” calcium and magnesium ions
(“threshold effect”) and thus increase the degree of thickening.
• Building materials industry:

Due to their stability and threshold effectiveness, there is a wide

At high temperatures, the curing of the cement is delayed by phos-
range of technical applications of phosphonates. Phosphonic acids
phonate addition (Knepper, 2003).
have been chemically synthesized for N70 years, but have gained
importance only since the beginning of the 1980s. Since then they • Cosmetics:
have increasingly replaced the highly controversially discussed
aminopolycarboxylic acids, such as ethylenediaminetetraacetic acid
(EDTA) and diethylenetriaminepentaacetic acid (DTPA). In the follow- Phosphonates serve, for example, as stabilizers for bleaching agents
ing, the areas of application of the five phosphonates PBTC, HEDP, in hair bleaching (Maise, 1984).
NTMP, EDTMP and DTPMP are described:
• Electroplating:
• Textile and paper production:

In the degreasing bath, the formation of interfering hydrophobic

Native textile fibers are often contaminated with iron hydroxides lime soaps, i.e., water-insoluble calcium salts of fatty acids, can occur
and iron oxides. In addition, iron from stainless steel appliances can dis- when saline water is used (Reichert, 1996). Phosphonates complex in-
solve and deposit as hydroxide on the product. Iron, manganese and terfering calcium cations and thus inhibit this undesirable process.
copper ions interfere with the bleaching and dyeing process by causing • Medicine:
the catalytical decomposition of the bleaching agent with negative
effect on the degree of whiteness of the treated textiles and causing cat-
alytic damage to the substrate. Phosphonates complex metals in the al-
The use of HEDP and EDTMP has been approved for the treatment of
kaline pH range and thus limit the precipitation of metals in the form of
bone diseases (EPA, 2013; de Klerk et al., 1992; Wilky and Loeb, 2013).
metal hydroxides. For example, at pH 10, despite the high hydroxide
concentration, one mol of DTPMP still binds three moles of Fe (Bachus • Oil production:

Table 1
Physicochemical properties of phosphonates (aRSC, 2016; bJaworska et al., 2002, and sources cited herein; cGledhill and Feijtel, 1992; dHERA, 2004).

PBTC HEDP NTMP EDTMP DTPMP

CAS-No. 37971-36-1 2809-21-4 6419-19-8 1429-50-1 15827-60-8

Molecular formula C7H11O9P C2H8O7P2 C3H12NO9P3 C6H20N2O12P4 C9H28N3O15P5
Molar mass 270.13 206.03 299.05 436.12 573.20
Phosphorus content (%) 11.5 30.1 31.1 28.4 27.0
Phosphonate groups 1 2 3 4 5
Amine groups 0 0 1 2 3
Water solubility (g/L) N100a N100b N100b 21c N100b
KHenry (atm∙m3/mol) 3.3 ∙ 10−17 a 5.2 ∙ 10−17 a 8.1 ∙ 10−18 a 1.2 ∙ 10−17 a 7.3 ∙ 10−18 d
log Kow −1.36a −3.49c −3.53c −4.10c −3.40c
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
Fig. 1. Structural formulae of widely used phosphonic acids (based on ACS, 2016).
The use of scaling-inhibiting phosphonates reduces the stone forma-
tion in oil drilling (Maise, 1984).
1.4. Phosphonate analysis
The knowledge of problems with regard to the determination of
phosphonates in the low concentration range in samples with highly
pronounced organic and inorganic contamination is of great impor-
tance, as very little information on the presence of phosphonates
in the environment is available due to this fact. This section therefore
summarizes briefly the development of phosphonate analysis and its
challenges.
The analysis of phosphonates is particularly difficult due to their low
reactivity and lack of chromophores absorbing in the UV and IR range
(Knepper, 2003). Various techniques for the analysis of phosphonates
are presented in the literature (Nowack, 1997, 2002a; Esser et al.,
2007; Fürhacker et al., 2005; Thompson et al., 1994; Klinger et al.,
1997; Meek and Pietrzyk, 1988; Weiß and Hägele, 1987; Tschäbunin
et al., 1989a, 1989b, 1989c; Vaeth et al., 1987; Wagner et al., 1990;
Tewari and van Stroe-Biezen, 1997; Wong et al., 1987; Shamsi and
Danielson, 1995; Ammann, 2002; Schmidt et al., 2014), most of which
cannot be applied to environmental or wastewater samples due to a
high susceptibility to interferences to matrix effects (cations, anions, or-
ganics, etc.) and high limits of quantification (LOQ N 1 mg/L).
The first systematic analyses of the phosphonate concentrations in
municipal wastewater samples (influent and effluent) of WWTPs
were presented by Nowack (1998, 2002b). The method is based on a
precomplexation of the phosphonates with FeIII followed by the photo-
metric detection (at 260 nm) of the Fe-phosphonate complexes sepa-
rated by means of ion-pair high-performance liquid chromatography
(HPLC) (Nowack, 1997). This method allows the detection of
aminophosphonates with limits of detection (LODs) between 0.05 and
0.5 μmol/L (15–57 μg/L for aminophosphonates). A disadvantage is
that individual phosphonates are identified solely by means of the re-
tention time (Knepper, 2003); in addition HEDP is detectable only at
concentrations N100 μg/L. If several phosphonates are present simulta-
neously, there is also the possibility that the competition for FeIII leads
to deviations of concentrations of some phosphonates compared to
the results of the complexation of individual phosphonates alone. It is
also questionable whether the process can reliably be applied to
1179
concentrates with very high water hardness. Although the process en-
visages the use of H+-cation exchange columns to remove interfering
Ca and Mg ions, these columns reach their limits when applied to very
hard wastewater samples.
Fürhacker et al. (2005) later presented a method that, like the meth-
od of Nowack (1997), also provided for a separation of the non-
complexed aminophosphonates by means of an HPLC anion exchange
column. The detection (via the element phosphorus) was performed
by means of mass spectrometry with inductively coupled plasma
(HPLC-ICP-MS), so that no precomplexation of the phosphonates with
FeIII was necessary. The measurement method was applicable to munic-
ipal wastewater (influent and effluent), but had too high LOQs for
these types of samples of around 100 μg/L (the LODs were between 25
and 40 μg/L).
Coupled systems of ion chromatography (IC) and mass spectrometry
with inductively coupled plasma (ICP-MS) are known for their high per-
formance with regard to the highly selective and excellently sensitive
determination of element species (Schmidt et al., 2014). The first at-
tempts to determine phosphonate complexes with heavy metals with
this method was described by Ammann (2002), whose measurement
method did not have the objective to determine the phosphonate itself,
but to determine the complexed metal species (Schmidt et al., 2014).
Recently, Schmidt et al. (2014) suggested a phosphonate detection
method using the IC-ICP-MS principle, which combines the advantages
of low LOQs for polyphosphonates in the range of 0.1 μg/L (compared to
the LOQs in studies of Nowack, 1997, of at least 15 μg/L) with the appli-
cability to environmental samples. The novelty of the method is the use
of a strong cation exchanger for transferring the complexed
phosphonates into “free” phosphonic acids, followed by the fiftyfold
pre-concentration of the phosphonates by a weak anion exchanger
prior to the analysis. Schmidt et al. (2014) applied the method only to
river water. Accordingly, the method still has to be examined and mod-
ified for the applicability to wastewater.
2. Biodegradability of phosphonates
2.1. C\\P bond cleavage by bacteria
There are several articles on the biodegradability of C\\P bonds
in less complex and partly naturally occurring phosphonates (2-
1180 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
aminomethylphosphonic acid (2-AEP), aminomethylphosphonic acid
(AMPA), glyphosate, etc.) (Zeleznick et al., 1963; Rosenberg and La
Nauze, 1967; Kittredge and Roberts, 1969; La Nauze et al., 1970; Cook
et al., 1978; Daughton et al., 1979; Ripke et al., 1987; Lerbs et al.,
1990; Ternan et al., 1998; Kononova and Nesmeyanova, 2002;
Martinez et al., 2010; Kamat and Raushel, 2013). However, there are
only a few studies on the phosphonates PBTC, HEDP, NTMP, EDTMP
and DTPMP, which are used as complexing agents. These industrial
chemicals are not formed naturally. From an earth-historical perspec-
tive, microorganisms have been confronted with these compounds
only for a very short time and thus the enzyme repertoire for efficiently
degrading these substances is widely missing.
Schowanek and Verstraete (1990) examined seven different envi-
ronmental samples (peat soil, water from an oligotrophic lake, two sam-
ples of activated sludge, river water, aerobic compost, digested sludge)
on microorganisms that are able to convert natural and xenobiotic
phosphonates as the sole P source for their growth. In this respect, 19
pure bacterial cultures exemplarily selected were examined, as well.
2-AEP was best utilized by these strains. Only one strain out of these
19, Arthrobacter sp. strain GLP-1, was capable of degrading all four
phosphonates HEDP, NTMP, EDTMP and DTPMP. The majority of the
enriched cultures from the environmental samples could solely convert
one of the phosphonate groups from the polyphosphonates. However,
in a few enriched cultures, almost a complete C\\P bond cleavage in
HEDP and EDTMP was observed. DTPMP could not be completely de-
graded by neither strain. NTMP was not considered in these studies.
The following average proportions of phosphonate-utilizing microor-
ganisms isolated from the environmental samples were determined
by comparing the number of each colony forming unit in nonselective
and selective nutrient medium: 2-AEP: 24.33%, glyphosate: 6.56%,
HEDP: 0.18%, EDTMP: 2.49%, DTPMP: 1.31%. Thus, glyphosate as the
sole P source could be utilized more easily than the polyphosphonates,
which were degraded by comparatively only few microorganisms. Envi-
ronmental samples, which can be expected to usually be contaminated
more frequently with phosphonates, did not contain significantly more
polyphosphonate-utilizing microorganisms than samples without
polyphosphonates. Thus, the authors concluded that phosphonate-
utilizing microorganisms are ubiquitous.
Raschke et al. (1994) investigated the aerobic microbial utilization of
PBTC using enriched cultures of microorganisms from eight different
samples (4× activated sludge, 2× river sediment, 2× river water) and
the anaerobic microbial utilization of PBTC using three different envi-
ronmental samples (2× river sediment, digested sludge of a WWTP), re-
spectively. In all cultures, PBTC could not be identified as a carbon
source. In the presence of alternative carbon sources (e.g., sodium ace-
tate, ethanol) and offered as the sole P source, PBTC was degraded
in all enrichment cultures. The following five strains were identified
as phosphonate-utilizing strains: Acinetobacter spec. DNA group II,
Acinetobacter baumannii, Alcaligenes spec., Pseudomonas spec.,
Methylobacter spec. These pure cultures were also unable to utilize
PBTC as the sole carbon source, but converted N90% of 0.2 mmol/L of
the compound within 200 h in the presence of alternative carbon
sources. The authors showed that Methylobacter spec., with sufficient la-
tency (ca. 50 h), completely utilized PBTC in an environment poor in
phosphate and in the presence of pyruvate, although increasing phos-
phate concentrations were observed during the reaction time. Apparent-
ly, the availability of inorganic phosphorus is no longer limiting the
degradation of PBTC after the enzymes necessary for C\\P bond cleavage
(phosphonatase, C–P-lyase) have already been induced. Based on this
finding, the authors concluded that PBTC can be degraded also in a natu-
ral environment where similar conditions prevail. The PBTC-utilizing mi-
croorganisms could not be assigned to a specific bacterial family. Slow
degradation took place both in the aerobic and in the anaerobic environ-
ment, with increased conversion rates in the presence of oxygen.
Schowanek and Verstraete (1990) and Raschke et al. (1994) thus
agreed to the finding that PBTC- and polyphosphonate-degrading
microorganisms are ubiquitous. However, these organisms are only
present in very small proportions in environmental samples. Moreover,
phosphonate degradation would preferably take place in a phosphate-
free environment and in the presence of suitable carbon sources.
2.2. Aerobic and anaerobic degradation tests
Table 2 contains a summary of results of OECD degradation tests ap-
plied to phosphonates. The Zahn-Wellens test (OECD 302 B, ISO 9888)
provides information on the inherent biodegradability of the tested
chemical substance. None of the tested phosphonates was inherently
biodegradable. Elimination rates measured in Zahn-Wellens tests
were generally attributed to adsorption onto the inoculum. Only the re-
sults of Reichert (1996) hint to biological degradation of NTMP and
EDTMP to an increased extent, since primary substance decline rates
of 50–80% were observed while at the same time very low DOC removal
rates were observed. This result also proves that phosphonates are not
completely mineralized to CO2 and phosphate, not even after several
weeks (the typical duration of Zahn-Wellens tests is 28 days). The de-
gree of CO2 formation of b10% observed in the SCAS test (OECD 302 A,
ISO 9887) by Saeger et al. (1978) substantiates this finding. Similarly,
the very low extents of removal in the modified OECD screening tests
(OECD 301 E, ISO 7827), the closed bottle tests (OECD 301 D, ISO
10707), the CO2 evolution test (modified Sturm test, OECD 301 B, ISO
9439) and the manometric respiration tests (OECD 301 F, ISO 9408)
are a clear indication of the strong stability of the tested phosphonates
against aerobic degradation.
In the studies carried out under anaerobic conditions by Steber and
Wierich (1986, 1987), b4% of HEDP and NTMP were converted into di-
gester gas (CO2, CH4) within 28 days. On the other hand, however, an in-
creased adsorption on sludge was observed (only 4–6% of the initial
phosphonate concentration was found in the supernatant). Nowack
(1998) also did not find any anaerobic degradability of the
polyphosphonates HEDP, NTMP, EDTMP and DTPMP complexed with
CaII. Furthermore, 0% of 20 mg/L Na4PBTC was degraded (related to
DOC) by anaerobic sludge within 56 d (OECD SIDS PBTC, n.d.).
The vast majority of the tests in which the formation of CO2 or the
actual concentration of the primary substance, i.e. phosphonate, was an-
alyzed (Reichert, 1996; Saeger et al., 1978; Steber and Wierich, 1986,
1987; Schöberl and Huber, 1988) thus agree that phosphonates are
not significantly mineralized by activated sludge bacteria even within
several weeks of exposure. Only Reichert (1996) found significant min-
eralization of aminophosphonates. In exceptional cases, the degradabil-
ity can therefore depend on the individual activated sludge sample.
However, Schowanek and Verstraete (1990) had shown that usually
no increased degradation of phosphonates by activated sludge samples
whose biocenosis should be adapted to phosphonates over several years
in comparison to other environmental samples of bacteria is observed
(Section 2.1). All sources, including Reichert (1996), either way agreed
that the nitrogen-free phosphonates PBTC and HEDP are not or only in-
significantly mineralized by activated sludge bacteria. Due to the very
slow degradation and the small number of phosphonate-utilizing spe-
cies of microorganisms, it is thus assumed that phosphonates cannot
be mineralized in conventional biological WWTPs, neither aerobically
nor anaerobically. Accordingly, phosphonates remain in adsorbed
form in the sewage sludge in their original form and can only be
completely oxidized (‘mineralized’) and thereby removed from the en-
vironment by combustion of the sewage sludge.
3. Phosphonate adsorption onto activated and digested sludge
3.1. Adsorption onto activated sludge
Results of experiments on the adsorption behavior of phosphonates
onto activated sludge are shown in Table 3. Reichert (1996) used rela-
tively high phosphonate initial concentrations (50 and 500 mg/L) and
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191 1181

Table 2
Elimination of phosphonates in OECD tests (in %).

OECD test Analytical parameter PBTC HEDP NTMP EDTMP DTPMP Reference

302 B COD 60–80a 50 Held (1989)

DOC – – 20b – – Bachus (2003)
DOC – – 45c – – Bachus (2003)
DOC – 33 23 – – Steber and Wierich (1986, 1987)
DOC – – – – 50 Cegarra et al. (1994)
DOC 17 – – – – BADSR (1989)
DOC 0 0 5 20 0 Reichert (1996)
Primary substance 0 0 80 50 30 Reichert (1996)
302 A DOC b20 100 85 65 0 Horstmann and Grohmann (1988)
14
CO2/C – 6.7 2.0 – 3.5 Saeger et al. (1978)
n.i. – – 90 – – Bachus (2003)
301 E DOC No biodegradability Horstmann and Grohmann (1988)
14
CO2/C – b3 20 – – Steber and Wierich (1986, 1987)
DOC – – 0 – – AAW (1984)
301 D BOD30/COD 0 – – – – BADSR (1976)
BOD30/COD – b10 b38 – – Steber and Wierich (1986, 1987)
301 F O2 consumption No consumption – – Huber (1975)
O2 consumption n.c. – – – – Metzner and Nägerl (1982)
301 B CO2 evolution – b10 b10 – – Schöberl and Huber (1988)

OECD 302 B: Zahn-Wellens test, OECD 302 A: modified semi-continuous activated sludge test (SCAS test), OECD 301 D: closed bottle test, OECD 301 E: static modified OECD screening test,
OECD 301 F: manometric respiration test (sapromat), OECD 301 B: carbon dioxide evolution test (modified Sturm test), n.i.: no information, n.c.: no consumption, COD: chemical oxygen
demand, DOC: dissolved organic carbon, BOD30: biochemical oxygen demand after 30 days.
a
Use of technical solutions without specification of the phosphonate.
b
Pure mineralization.
c
15% mineralization and 30% adsorption with a 20-fold sludge excess.

detected comparatively high adsorption efficiencies (N 60%) at 1.5 g/L
dry substance, in particular for polyphosphonates. Steber and Wierich
(1986, 1987) obtained similar results with the phosphonates HEDP
(0.7–21 mg/L) and NTMP (1–300 mg/L) with 2–3 g/L dry substance.
Reichert (1996) as well as Metzner and Nägerl (1982) with a maximum
of 50% for PBTC found a significantly poorer adsorption affinity to acti-
vated sludge compared to the polyphosphonates.
Nowack (2002b) investigated the adsorption affinity of NTMP to
1 g/L of activated sludge biomass after 2 h as a function of pH and in
the presence of metals. Regardless of the complexed species (CuII-
NTMP, FeIII-NTMP, NTMP/1 mmol/L CaII), for an initial concentration of
1.1 mg/L NTMP the best elimination efficiency (between 80 and 100%)
was observed in the pH range 3 to 5. In the pH range between 6 and
9, the elimination efficiency ranged from 40 to 60%. Furthermore,
Nowack (2002b) found a better adsorption of NTMP at pH 6.5 with in-
creasing CaII concentrations.
A large number of the studies discussed here and presented in
Table 3 were carried out with initial phosphonate concentrations
of higher than 50 mg/L, which are not very representative for WWTP
influents. All in all, however, the results suggest that, despite the
lack of biodegradation (see Section 2), in particular, a removal of
polyphosphonates via adsorption may occur in WWTPs. It is also strik-
ing that compared to other phosphonates PBTC is the most difficult
phosphonate to eliminate. The exact mechanism of adsorption is still
unclear, as most of the publications lack information on whether the ac-
tivated sludge used was obtained from WWTPs operating with simulta-
neous precipitation, i.e., whether the activated sludge contained a
significant quantity of metal hydroxides or metal oxides to which the
phosphonates could have been preferentially adsorbed (Nowack and
Stone, 1999; Zenobi et al., 2005). The results of Nowack (2002b) show
that the adsorption depends strongly on the polarity of the surface.
With CaII adsorbed, the polarity of the surface becomes more positive.
This results in reduced charge repulsion to the phosphonate, so that
NTMP can adsorb via ternary complexes (Stone et al., 2002). However,
it is still unclear whether this effect of CaII increasing the adsorption of
NTMP is also valid for other phosphonates.
3.2. Adsorption onto digested sludge
The abovementioned results suggest a relatively high extent of re-
moval of phosphonates by adsorption onto activated sludge under aer-
obic conditions in the wastewater treatment process. As a result, being

Table 3
Removal efficiencies of phosphonates in sludge adsorption experiments (in %).

Phosphonate (mg/L) DS (g/L) PBTC HEDP NTMP EDTMP DTPMP Reference

Adsorption experiments with activated sludge:

500 1.5 40a 60a 60a 45a 70a A
50 1.5 50b N90a N95a N90a N90c A
5.0–200 n.i. 40–50 – – – – B
0.7–21 2–3 – N90a – – – C
1.0–300 3.0 – – N90 – – D
1.1 1.0 – – 80–100d – – E
1.1 1.0 – – 40–60e – – E

Adsorption experiments with digested sludge:

100 1.8 10c 65c 85c N95c 80c A

A: Reichert (1996), B: Metzner and Nägerl (1982), C: Steber and Wierich (1986), D: Steber and Wierich (1987), E: Nowack (2002b), DS: dry substance, n.i.: no information.
a
After 1 day.
b
After 1 week.
c
After 1 h.
d
pH 3–5.
e
pH 6–9, in the presence of 0.5–2 mmol/L CaII: N60% removal rates.
1182 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
concentrated in the primary or secondary sludge, phosphonates are fed
into the anaerobic digestion process. Consequently, Reichert (1996) in-
vestigated whether this change of milieu may lead to changes in the ad-
sorption behavior, possibly even to desorption processes. For this
purpose, activated sludge from a municipal WWTP (fresh sludge,
4.5 g/L dry substance), which had been spiked with phosphonate
(100 mg/L), was aerated for one week and then mixed with digested
sludge (ratio of fresh sludge to digested sludge 1:5). The filtrate was in-
vestigated at various times to determine any desorption/dissolution
under anaerobic conditions at 35 °C. It turned out that
polyphosphonates that were adsorbed onto activated sludge did not de-
sorb during the anaerobic digestion process. Thus, polyphosphonates
which have already been removed from the wastewater during the aer-
obic treatment process do not return to the WWTP via the surplus
water. The monophosphonic acid PBTC, on the other hand, exhibited
an accumulation tendency with ca. 30% re-dissolution. Reichert (1996)
also investigated the adsorption behavior of phosphonates onto
digested sludge under anaerobic conditions and found quite high differ-
ences in the behavior of the phosphonates tested (see Table 3). b20% of
NTMP, EDTMP and DTPMP were detected in the filtrate at the end of the
experiment of 1 h. Approximately 90% of PBTC and 35% of HEDP, how-
ever, were still found in the filtrate indicating that the monophosphonic
acid could be problematic in WWTPs.
Thus, so far, there are only few studies on the adsorption of
phosphonates onto digested sludge. However, these few studies indi-
cate that phosphonates adsorbed on activated sludge remain adsorbed
in the anaerobic environment. Why PBTC, which apparently has the
lowest adsorption tendency of all five phosphonates anyway, tends to
desorb more strongly, is still unclear. PBTC is a phosphonate with only
one phosphonate group, three carboxyl groups and has smaller complex
formation constants in comparison to aminophosphonates (Knepper,
2003). This complex binding capacity is obviously a decisive factor for
the adsorption of phosphonates. Furthermore, complexing agents
based on carboxyl groups (e.g. ethylenediaminetetraacetic acid) usually
have a lower adsorption affinity towards activated sludge than
complexing agents based on phosphonate groups (Fischer, 1991,
1992; Bucheli-Witschel and Egli, 2001).
4. Phosphonate removal in municipal wastewater treatment plants
In a field test described by Hoelger et al. (2008), DTPMP was dosed
into the grinding shop of a paper production for three days and a bal-
ance of the phosphorus loads from the grinding shop over the effluent
of the paper company to the end of a biologically operated WWTP
was made (no concentration data). A small portion of the dosed
DTPMP was already retained by adsorption onto the paper in the
paper machine. Further additional adsorption processes resulted in 70
to 80% of the phosphonate still entering the WWTP. There, N90% of
the incoming DTPMP was eliminated.
Metzner (1990) carried out field tests in two WWTPs, the influents
of which were spiked with 2 mg/L HEDP or NTMP. Neither in the
WWTP with an oxidation ditch nor in the WWTP with an activated
sludge process, negative effects on the BOD5, COD and DOC elimination
were found. The elimination efficiency of HEDP in the oxidation ditch
was between 25 and 70%, on average ca. 50%. A similar result was ob-
served for the activated sludge process. 60% of NTMP was removed by
this method, whereas the largest proportion was removed in the prima-
ry treatment.
Müller et al. (1984) determined a higher removal efficiency for
HEDP. At a spiked concentration of 2 mg/L in the influent of a WWTP,
a removal of 50 to 70% already occurred in the primary sedimentation.
In the aeration tank with simultaneous phosphorus precipitation, the
remaining phosphonate was almost completely eliminated from 90 to
about 97.5% (with regard to the influent concentration). The authors
predominantly attributed the removal to the adsorption of phosphonate
on freshly precipitated iron hydroxide flocks.
Nowack (2002b) dosed DTPMP into the influent of a Danish WWTP
with a load of 7.6 kg/d. Depending on the flow rate, concentrations of
2.5 to 6.9 mg/L of DTPMP were obtained in the influent stream. The bi-
ological treatment resulted in a 95% removal of this compound. In a fur-
ther step, by the addition of aluminum sulphate, the removal efficiency
was increased to 97%.
To date, the non-availability of a sensitive phosphonate analysis
method (see Section 1.4) has led to the fact that only a few aforemen-
tioned field experiments with predominantly high phosphonate con-
centrations in the still measurable range of mg/L in the WWTP
influent were carried out in order to determine the phosphonate re-
moval performance of WWTPs. However, these comparatively high
phosphonate concentrations are unlikely in WWTPs. In the following,
the few known publications investigating phosphonate concentrations
in WWTPs without spiking beforehand are described (Nowack, 1998,
2002b; Fürhacker et al., 2005).
Nowack (1998) investigated the inflow and outflow concentrations
of the polyphosphonates NTMP, EDTMP and DTPMP from seven Swiss
WWTPs. The WWTP Herisau received discharges from the textile indus-
try. NTMP was found in concentrations above the LOD (15 μg/L) in five
WWTPs. With a week-average concentration of 0.25 mg/L (equivalent
to 0.08 mg/L P), the WWTP Herisau had the highest value here.
EDTMP was found in the inflow of six WWTPs. The highest average con-
centration found was 0.09 mg/L EDTMP (equivalent to 0.03 mg/L P). In
all WWTPs, these two phosphonates could be removed to concentra-
tions below the LOD (NTMP: 15 μg/L, EDTMP: 21 μg/L). DTPMP was de-
tected in the inflow of three WWTPs in concentrations above the LOD
(57 μg/L). The WWTP of Herisau had an average concentration of
0.97 mg/L DTPMP, which corresponds to a phosphorus content of
0.27 mg/L. The example of the WWTP in Herisau shows that phospho-
nate concentrations of N 1.25 mg/L (corresponding to 0.4 mg/L P) can
be present in WWTP inflows. WWTPs with predominantly domestic
wastewater had only very low phosphonate concentrations. The ques-
tion whether the use of precipitants contributed to an increased elimi-
nation efficiency could not be answered since the wastewater of the
only WWTP without phosphate precipitation had too low phosphonate
concentrations. When the WWTP of Herisau was examined in more de-
tail, a typical weekly course of the DTPMP concentration with low con-
centrations at the weekend was determined. NTMP was removed by at
least 80% and EDTMP by at least 70% in all WWTPs. All samples were
membrane-filtered (0.45 μm pore size) prior to the analysis. Thus, any
phosphonates adsorbed onto solids in the influent as well as in the efflu-
ent were not taken into account.
Furthermore, Nowack (2002b) analyzed the NTMP loads in the in-
flow and outflow of a German WWTP operated with simultaneous
chemical precipitation (Weil) with multiple indirect dischargers of the
textile industry. Here, the NTMP concentration in the inflow varied be-
tween 60 μg/L and 0.3 mg/L. Occasionally, NTMP loads of 18 kg/d in the
inflow were achieved. The two-week survey ultimately resulted in an
NTMP removal efficiency of at least 93%.
Fürhacker et al. (2005) analyzed the concentrations of
aminophosphonates in the influent and effluent of five WWTPs.
EDTMP was detected above the LOD of 29 μg/L (LOQ: 125 μg/L) only
in the feed of the two WWTPs with the highest textile industry share
(167 and 49 μg/L EDTMP). In these WWTPs, EDTMP was removed to
concentrations below the LOD. NTMP (LOD: 35 μg/L) and DTPMP
(LOD: 38 μg/L) were not detected.
In all publications but one (25–70% removal efficiency; Metzner,
1990) usually a good phosphonate removal efficiency of N 80% in munic-
ipal WWTPs is described with phosphonate concentrations in the efflu-
ent below the LODs (see also Table 4). However, relatively high LODs,
like 0.057 mg/L in the case of DTPMP (Nowack, 1998), are in a range
that does not rule out a potential impact of phosphonates on the eutro-
phication of surface waters. In particular, the concentration of all
phosphonates in total can be much higher than the LOD of a single phos-
phonate. Furthermore, extensive studies on individual compounds such
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
as the nitrogen-free phosphonates PBTC and HEDP are still missing. For
example, PBTC shows the lowest tendency towards adsorption onto ac-
tivated sludge in laboratory tests (Reichert, 1996). Furthermore, the
very low removal efficiencies described by Metzner (1990) also suggest
that some mechanical-biological WWTPs without chemical phosphorus
precipitation can only achieve removal efficiencies of 25–70%.
5. Effect of phosphonates on chemical phosphate precipitation
If phosphate precipitation is carried out with aluminum or iron salts
on WWTPs, phosphonates, which are capable of complexing metals,
play an important role on this precipitation process. Accordingly, they
can contribute to increased β values (molar ratio of precipitant concen-
tration to initial total P concentration), i.e., precipitant concentrations,
as reported on in the following publications.
Horstmann and Grohmann (1984, 1986) fed a test apparatus
equipped with a gravel filter for flocculation filtration with formazine-
spiked tap water (pH 6.8–7.4). This tap water was spiked with different
mixing ratios of phosphonate-P and ortho-phosphate-P. The total P con-
centration was constant regardless of the mixing ratio and lay between
0.6 and 2.2 mg/L depending on the individual tested phosphonate. Even
with a share of only 33% HEDP of total P, the β value required for an 80%
total P removal increased from 1 (in the case of 0% HEDP-P) to 5. For
EDTMP, already a share of 10% of total P led to an increase of the β
value from 1 to 5.
Reichert (1996) carried out experiments with municipal raw waste-
water (simulation of a pre-precipitation) and clarified wastewater (sim-
ulation of a post-precipitation). In the tests with raw wastewater,
disturbances of the phosphate removal were already observed at con-
centrations of around 1 mg/L PBTC and NTMP. In the case of clarified
wastewater, slightly higher concentrations of NTMP (between 1 and
10 mg/L) were required for this effect.
When FeIII is used for phosphate precipitation in WWTPs, iron hy-
droxide is precipitating in parallel to FePO4. Phosphonates and phos-
phate compete for free adsorption sites of the formed flocks. Nowack
and Stone (2006) modeled the simultaneous presence of NTMP and
phosphate under representative conditions in WWTPs (pH 7.0, FeIII con-
centration of 5 mg/L) in order to estimate the phosphonate-induced re-
duction in phosphate removal efficiency. For example, a 10% reduction
can occur in the presence of 3 mg/L phosphate and an NTMP concentra-
tion of 0.15 mg/L (which according to the authors is usually present in
WWTPs). At a concentration of 1 mg/L NTMP (which is a rare, but pos-
sible phosphonate concentration; see Section 4), the reduction ranged
from 10% in the presence of 9.5 mg/L phosphate to 50% in the presence
of 0.95 mg/L phosphate. From this, it can be concluded that the presence
of phosphonates makes it difficult to attain the desired low phosphate
effluent concentrations.
Wenger-Oehn et al. (2005) reported on problems with the treat-
ment of wastewater from the beverage industry in a biological WWTP.
The reduction of the total P concentration of ca. 15 mg/L (70% of
it constituted phosphonates) was only possible with a high excess of
Table 4
Removal efficiencies of phosphonates in municipal WWTPs (in %).
Phosphonate in the influent (mg/L) PBTC HEDP
a
n.i. – –
2.0a – 25–70
2.0a – N90
2.5–6.9a – –
0.06–0.3b – –
Max. 0.25b – –
Max. 0.07b – –
Max. 0.97b – –
0.167b – –
A: Hoelger et al. (2008) B: Metzner (1990) C: Müller et al. (1984) D: Nowack (2002b) E: Nowack (1998) F: Fürhacker et al. (2005) n.i.: no information.
a
Spiking of phosphonate.
b
Without spiking of phosphonate.
1183
precipitant (β value = 2.5). As a result, there was a shortage of phos-
phorus as essential nutrient in the biological treatment step resulting
in sudden growth of filamentous bacteria and disturbance of plant oper-
ation. Furthermore, König et al. (2002) reported on a WWTP in Austria
that had problems with the compliance with the phosphorus limit value
of 0.5 mg/L since it had high feed loads of phosphonates, presumably via
indirect discharges.
An overall assessment of the influence of phosphonates on phos-
phate precipitation has not yet been possible. Especially for cases
where industrial wastewater with elevated phosphonate loads is indi-
rectly discharged, there are still insufficient data on phosphonate con-
centrations in WWTP influents. In the publications mentioned
(Horstmann and Grohmann, 1984, 1986; Nowack and Stone, 2006),
there are indications that phosphonate concentrations in the sub-ppm
range can lead to increased β values. In order to ensure stable P removal,
the consideration of individual cases of indirect discharges is therefore
important. Although the removal of phosphonates can be predominant-
ly successful, for example by adsorption onto activated sludge in
WWTPs (see Section 4), this fact should not distract from a possible
cost-increasing disadvantage that increased phosphonate concentra-
tions in the influent entail. Furthermore, it is also irrelevant whether
the phosphonates are adsorbed onto the activated sludge or onto
metal flocks. By ternary ligand-like complex formation, i.e., the simulta-
neous bonding of two metal atoms by a single phosphonate as described
by Stone et al. (2002), the phosphonate can also bind dissolved metals
in the adsorbed state.
6. Environmental relevance of phosphonates
6.1. Phosphonates in the environment
According to EPA (2013), the amount of phosphonate used in 2012
in Europa was 49,000 t, which is 52% of the global consumption of
94,000 t/a. Accordingly, Europe is the continent with the highest con-
sumption of phosphonates. A breakdown of the consumption quantities
of the individual areas of application in Europe is shown in Fig. 2 (EPA,
2013). Destatis (2013, 2015) provides information on domestic dis-
charges and delineates the wastewater amounts of direct and indirect
discharges in a sector-specific manner so that the phosphonate loads
can be divided roughly into the abovementioned three wastewater
streams (Fig. 2) (the data from Germany are considered to be largely
representative of total Europe). It can be seen that approximately 85%
of phosphonates in WWTPs can be attributed to domestic use. However,
the appearingly small share from the indirect dischargers should not be
neglected. Thus, in certain cases, very high proportions of wastewater
from indirect dischargers, e.g., the textile industry, may lead to greatly
increased phosphonate concentrations in influents of WWTPs (Neft
et al., 2010; Nowack, 1998, 2002b). A significant proportion of the phos-
phonate load in water is obtained by means of membrane concentrates
polluted with antiscalants as well as cooling waters for which pretreat-
ment is not standard (Gartiser and Urich, 2002).
NTMP EDTMP DTPMP Reference
– – N90 A
60 – – B
– – – C
– – 95–97 D
N93 – – D
N80 – – E
– N70 – E
– – 85 E
– N80 – F
1184 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
Fig. 2. Phosphonate loads of direct dischargers and municipal WWTPs in Europe based on values from the years 2012 and 2013 (EPA, 2013; Wiechmann et al., 2012; Nowack, 1998, 2002b;
Destatis, 2013, 2015; Eurostat, 2017a; Schmidt et al., 2014).
According to Fig. 2, the approximate phosphonate load in the inflow
of European WWTPs is 24,600 t/a (7400 t/a phosphonate-P; calculations
based on EPA, 2013; Destatis, 2013, 2015; neglecting the connection
rate; see Supplementary data). Considering a phosphonate removal
efficiency of 80–95% in municipal WWTPs mainly by adsorption
onto activated sludge (Section 2.2 and Section 4), approximately
19,700–23,400 t/a phosphonate is adsorbed onto sewage sludge. Ac-
cording to Eurostat (2017a), ca. 15 million tonnes of sewage sludge
dry substance are generated annually on European municipal WWTPs.
Accordingly, the average phosphonate loading of sewage sludge is
1.2–1.5 g of phosphonate/kg of dry substance. In Europe, approximately
37% of the sewage sludge is used in agriculture as fertilizer and for soil
improvement (Wiechmann et al., 2012). Thus, approximately
7300–8700 t/a phosphonate is discharged via sewage sludge in agricul-
ture. Phosphonates have a very low mobility in soils (Steber and
Wierich, 1986, 1987). This explains why the risk of contaminating the
groundwater with phosphonates via the application of phosphonate
contaminated sewage sludge appears to be rather low (Gledhill and
Feijtel, 1992). Notwithstanding this finding, Knepper (2003) critisized
the lack of a comprehensive risk assessment regarding the input of
phosphonates via sewage sludge applied in agriculture.
The phosphonate load discharged into receiving water by municipal
WWTPs in Europe can be estimated at 1200–4900 t/a at an assumed
removal efficiency of 80–95% (Section 4). These numbers can be even
higher since the calculations do not take into account the low connec-
tion rates of WWTPs that still are fact in some European countries
such as Romania and Albania (Eurostat, 2017b). A selective phospho-
nate removal is not yet state of the art in the industries directly
discharging their effluents. Thus, a very rough estimate of
7800–13,700 t/a can be given for the phosphonate load discharged by
direct dischargers into receiving water. The largest share of this load is
probably caused by membrane concentrates and cooling water (about
65–90%). In total, 9000–18,600 t/a phosphonate is thus discharged
into receiving waters in Europe.
Only recently, Schmidt et al. (2014) developed a method that allows
the quantification of phosphonates in environmental samples with
LOQs in the range of 0.018–0.1 μg/L. Before, there was no sensitive ana-
lytical method available (Section 1.4). Thus, due to the lack of measured
phosphonate concentrations in surface water, the necessity for calcula-
tions based on models arose. In the early 1990s, Gledhill and Feijtel
(1992) described a model calculation for Western European countries
considering an annual polyphosphonate consumption of 6300 t (esti-
mated consumption in the whole of Europe was 11,820 t/a). The authors
estimated the concentrations of polyphosphonates in municipal
WWTPs at 170 to 290 μg/L (details of calculation are missing) and as-
sumed effluent concentrations between 90 and 235 μg/L. Considering
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
dilution effects in the receiving water, accumulation in the sediment
(100:1) and partial degradation by photolysis and microorganisms,
they calculated dissolved concentrations of polyphosphonates in West-
ern European waters in the order of 0.25 μg/L. Using model calculations,
Jaworska et al. (2002) presented the following predicted concentrations
of dissolved phosphonates in waters in the Netherlands: 0.32–4.90 μg/L
HEDP, 0.07–1.15 μg/L NTMP, 0.04–0.64 μg/L DTPMP. In addition, the en-
richment in sediments was calculated to be 0.08–1.18 mg HEDP/kg DS
(dry substance), 0.02–0.30 mg NTMP/kg DS and 0.003–0.10 mg
DTPMP/kg DS.
Fürhacker et al. (2005) measured the concentration of phosphonates
by means of HPLC-ICP-MS in a number of Austrian receiving waters.
However, all phosphonates were below the LOQs of approximately
100 μg/L, so that based on the abovementioned estimates, a phospho-
nate content above this order of magnitude is unlikely in rivers.
The only previously known analyses of phosphonates in surface wa-
ters with sufficiently low LOQs were described by Schmidt et al. (2014).
They determined HEDP concentrations between 0.3 and 1.6 μg/L and
DTPMP concentrations between 0.1 and 1.3 μg/L in six German rivers
using IC-ICP-MS with metal complex cleavage and phosphonate pre-
concentration using ion exchangers as analytical method. NTMP,
EDTMP and HDTMP (hexamethylenediamine tetra(methylene phos-
phonic acid)) were not quantified in any river above their LOQs be-
tween 0.095 and 0.117 μg/L. The concentration ranges of HEDP and
DTPMP measured were in good agreement with the model calculations
of Jaworska et al. (2002). Thus, the hypothesis of Gledhill and Feijtel
(1992), that the total concentration of phosphonates in Western
European waters would be usually of the order of 0.25 μg/L, was not
confirmed. In all rivers examined, total phosphonate concentrations of
at least 0.5 μg/L were measured. In part, the measured total concentra-
tion of phosphonates even exceeded the value given by Gledhill and
Feijtel (1992) by one order of magnitude (highest total concentration
in the river Pfinz in Karlsruhe, Germany: 2.9 μg/L). The concentrations
reported on by Gledhill and Feijtel (1992) were calculated for the
1990s and are therefore no longer relevant because the amount of
phosphonates used since then has increased considerably.
6.2. Environmental behavior
Phosphonates predominantly exist in water in the form of com-
plexes with the alkaline earth metal ion Ca2+ (Nowack, 2003) and the
Fe2 + ion as predominant central ions (Jaworska et al., 2002). Fig. 3
gives an overview of the characteristic degradation and adsorption
Fig. 3. Presence, degradation and adsorption pathways of phosphonates in natural waters (Me: metal) (with permission from Rott et al., 2017a).
1185
pathways of phosphonates, which are essential for understanding the
behavior of phosphonates in natural waters.
Despite their high solubility and due to their strong polarity,
phosphonates have a very high tendency to adsorb onto sediments
and suspended matter. Thus, they are considered to exist in the
adsorbed state in waters (Steber and Wierich, 1986, 1987; Fischer,
1992). Phosphonates can be oxidized by oxygen when present as man-
ganese complex (Nowack and Stone, 2000). Another possible form of
degradation reaction of phosphonates is hydrolysis. Schowanek and
Verstraete (1990, 1991) found light-independent hydrolytic degrada-
tion of aminophosphonates in the range of 6 to 15‰ per day measured
as the conversion of organic phosphorus into inorganic phosphorus. At a
rate of 0.5‰ per day, the nitrogen-free HEDP hydrolyzed only insignifi-
cantly. Different from the metal-free state, phosphonates can be easily
cleaved by UV radiation in the complexed state (Matthijs et al., 1989;
Grohmann and Horstmann, 1989). Thus, the degradation of
phosphonates by hydrolysis is less pronounced than the metal-
catalyzed degradation by photolysis (Jaworska et al., 2002). This form
of phosphonate degradation takes place in the surface-near layer of
water bodies, where UV radiation is not completely absorbed
(Grohmann and Horstmann, 1989; Fischer, 1993).
In water, only few species of microorganisms are capable of metab-
olizing polyphosphonates (Schowanek and Verstraete, 1990) and PBTC
(Raschke et al., 1994) (Section 2.1). In particular, HEDP, with its high
persistence against microbial degradation and extraordinary resistance
to hydrolysis, is considered to have a lasting stability in aquatic ecosys-
tems (Fischer, 1993). Microbial phosphonate degradation is possible
both in sediment and in solution (Steber and Wierich, 1987). Further-
more, bacterial metabolism of phosphonates occurs in parallel to
phosphate release by abiotic degradation mechanisms, in particular,
metal-catalyzed photolysis (Gledhill and Feijtel, 1992). Accordingly, mi-
croorganisms devoid of enzymes capable of cleaving C\\P bonds can
utilize abiotically formed phosphate and, thus, indirectly assimilate
phosphonates and their degradation products.
6.3. Ecotoxicity
In various fish studies, phosphonates were found to be active in con-
centrations of N100 mg/L (predominantly measured as no observed ef-
fect concentration (NOEC) or lethal concentration for 50% of the test
population (LC50) after 96 h) (Knepper and Weil, 2001; Kästner and
Gode, 1983; Gledhill and Feijtel, 1992; Huber, 1975; Maise, 1984;
Metzner and Nägerl, 1982; Schöberl and Huber, 1988; Jaworska et al.,
1186 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
2002). Such high concentrations do not occur in natural waters
(Section 6.1). However, the lethal concentration (LC) does not have
any direct correlation to potential chronic effects that may already
occur at much lower concentrations.
Steber and Wierich (1986, 1987) observed bioconcentration factors
(concentration of the test substance in the fish in relation to the concen-
tration of the test substance in the test water) between 15 and 25 in
zebrafish for HEDP and NTMP. These values are unexpectedly high for
hydrophilic compounds with n-octanol/water distribution coefficients
log KOW b − 1.3 (Table 1), but much lower than the bioconcentration
factors of lipophilic compounds such as 1,2,4-trichlorobenzene or γ-
hexachlorocyclohexane (lindane), which can be several orders of mag-
nitude higher (Geyer et al., 1985, 1997). At the end of several weeks of
exposure, immediately a rapid elimination of the phosphonate in the
fish body occurred. These results showed that the accumulation of the
phosphonate is not a result of lipophilicity, but caused by its general
high adsorption affinity or other not known uptake pathways or elimi-
nation kinetics.
Phosphonates were also tested in common Daphnia assays with
Daphnia magna (the large water flea), where they, however, did not
show any acute toxicity with EC0 values N 100 mg/L (the endpoint of
these tests was the unability of the individuals to swim (immobiliza-
tion) after 24 h or 48 h of exposition) (Knepper and Weil, 2001;
Schöberl and Huber, 1988; Kästner and Gode, 1983; Gledhill and
Feijtel, 1992; Grohmann and Horstmann, 1989). Of the invertebrates
tested, oysters were most sensitive with mean effect concentrations
(EC50) after 96 h of b 100 mg/L (e.g., EDTMP: EC50 = 67 mg/L)
(Gledhill and Feijtel, 1992). The shell formation of oysters requires the
precipitation of calcium carbonate, which is prevented by complex for-
mation (Gledhill and Feijtel, 1992). It has to be noted that the measured
mean effect concentrations (≥ 67 mg/L phosphonate) were very high
compared to the naturally occuring phosphonate concentrations in the
aqueous environment (Section 6.1), so that it is questionable if this ad-
verse effect of phosphonates on oysters also occurs at these lower natu-
ral concentrations.
Gledhill and Feijtel (1992) reported on studies on the algal toxicity
(Selenastrum capricornutum, latterly: Raphidocelis subcapitata) of
polyphosphonates. Mixtures of 10,000 algae cells/mL were exposed to
various concentrations of the polyphosphonates at a light intensity of
4300 lx in algae growth medium. The chlorophyll content was analyzed
via the determination of chlorophyll fluorescence. After an exposure
time of 4 days, average effect concentrations between 0.4 and 20 mg/L
were obtained. After 14 days, equal or significantly higher effect concen-
trations (i.e., lower algae toxicity) were measured for all phosphonates
tested. The authors hypothesized that a photolytic degradation of the
phosphonates might have occurred over the longer test period, causing
that on the one hand important elements for algae growth, e.g., Ca and
Mg, would be available again due to the absence of complex formation.
On the other hand, additional biologically available phosphate might
have been released from degraded phosphonates stimulating the
algae growth.
Up to phosphonate concentrations of 2.5 g/L, no clear inhibitory ef-
fect on Photobacterium phosphoreum, a light-emitting, halophilic, non-
spore-forming, Gram-negative, and facultative anaerobic rod-shaped
bacterium was observed (Grohmann and Horstmann, 1989). Huber
(1975) investigated potential inhibitory effects of HEDP and NTMP on
the aerobic biodegradation of peptone, glucose and municipal wastewa-
ter by activated sludge. NTMP had no significant effect up to the highest
concentration tested (100 mg/L). HEDP had no inhibitory effect up to a
concentration of 50 mg/L.
In some studies, also the influence of phosphonates on the toxicity of
heavy metals was investigated. Gledhill and Feijtel (1992) compared
the acute toxicity (LC50) of CdII, CuII, PbII and ZnII (LC50: 0.81–73 mg/L)
with the toxicity of their 1:1-phosphonate-complexes with the blue
sunfish as test organism. They determined LC50 values above 100 mg/L
for each of the tested metal-polyphosphonate complex. Hanstveit and
Oldersma (1996), cited by Jaworska et al. (2002), also observed no
growth inhibition by complexation of heavy metals for the algae
Raphidocelis subcapitata. Koch (1995) analyzed the inhibitory effect of
PbII, CdII and CuII as well as their 1:1-complexes with HEDP and NTMP
on the heterotrophic biocenosis of sludge of a WWTP (addition of N-
allylthiourea to inhibit the nitrificants) by means of a respirometer.
NTMP had no influence on the inhibitory effect of CuII. HEDP was able
to reduce the effect, but not to zero. The inhibitory effect of PbII and
CdII was not significantly affected by complex formation with HEDP
and NTMP.
In a comprehensive risk assessment study of HEDP, NTMP and
DTPMP on humans and the environment (HERA, 2004), phosphonates
were characterized to have low to moderate acute oral toxicity and
low acute dermal toxicity. No genotoxic, mutagenic, carcinogenic nor
a teratogenic effect could be detected for any of the phosphonates.
Phosphonates are therefore classified as being toxicologically harmless
for a wide range of aquatic species (Gledhill and Feijtel, 1992; Maise,
1984; Metzner and Nägerl, 1982; Kästner and Gode, 1983; HERA, 2004).
From the mass of the degradation products of aminophosphonates,
in particular, N-(phosphonomethyl)glycine (glyphosate) and
aminomethylphosphonic acid (AMPA) are prominent (Klinger et al.,
2000; Grandcoin et al., 2017). Glyphosate is a broad-spectrum herbi-
cide, whereas AMPA is the main degradation product of glyphosate.
AMPA is considered to have genotoxic effects (Mañas et al., 2009).
Both compounds are controversially discussed in the scientific commu-
nity with regard to their potential environmental relevance (de Roos
et al., 2003; Eriksson et al., 2008; Hardell et al., 2011).
6.4. Contribution to eutrophication
Eutrophication is the enrichment of water bodies with mineral nu-
trients (P and N) resulting in an excessive production of autotrophic or-
ganisms (phytoplankton) predominantly in the form of green algae and
cyanobacteria (blue algae). The excessive growth of these organisms re-
sults in less light reaching the depths of the water body. The absence of
light leads to the dying of the macrophytes growing on the sediment.
Furthermore, phytoplankton sinks down to the sediment and is
decomposed there by destruents, causing further nutrient release and
phosphate mobilization from the sediment. The increased respiratory
rate of the bacteria on the bottom results in oxygen deficiency (hypox-
ia), the increased activity of anaerobic microorganisms and the associat-
ed release of reduced toxic compounds such as hydrogen sulfide and
ammonia. This self-reinforcement of eutrophication ultimately acceler-
ates the dying of aquatic organisms. Phosphorus is the minimum factor
for plant growth and eutrophication. Autotrophic organisms are only
able to assimilate phosphorus in the form of ortho-phosphate (Correll,
1998).
Only in very few publications, phosphonates are linked with the
topic of eutrophication (Boels et al., 2010; Reichert, 1996; Horstmann
and Grohmann, 1986; Studnik et al., 2015). The hypothesis that
phosphonates do not contribute to eutrophication is generally attribut-
ed to the high stability of phosphonates against biodegradation by mi-
croorganisms (Metzner and Nägerl, 1982; Huber, 1975). However,
studies on the biodegradability of phosphonates have so far been car-
ried out predominantly with heterotrophic bacteria (Schowanek and
Verstraete, 1990; Raschke et al., 1994) rather than with autotrophic
organisms which actually are responsible for eutrophication. Further-
more, phosphonates are subject to natural abiotic degradation process-
es that contribute to the release of biologically available phosphate from
phosphonates (Section 6.2).
Gledhill and Feijtel (1992) exposed the algal species Selenastrum,
Chlorella and Anabaena (cyanobacterium) (10,000 cells/mL) to different
concentrations of the phosphonates NTMP, HEDP, EDTMP and HDTMP
(0.1, 1.0, 10, 100 mg/L) in algae growth medium at a light intensity of
4300 lx. The chlorophyll determination by fluorescence measurement
after eight days showed that NTMP stimulated the growth of
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191 1187

Selenastrum and Chlorella at concentrations between 0.1 and 10 mg/L concentration (Gledhill and Feijtel, 1992). This is relevant since even a
and stimulated the growth of Anabaena at concentrations between 0.1 total P concentration of as low as 20 μg/L can cause eutrophication
and 1.0 mg/L. Higher NTMP concentrations caused growth inhibition (Correll, 1998).
of all three species. The growth of Chlorella was also stimulated by Despite the many factors influencing their field trials, Grohmann and
HEDP, EDTMP and HDTMP in the concentration range between 0.1 Horstmann (1989) have clearly shown that, due to its photolytic de-
and 10 mg/L. HDTMP in all tested concentrations up to 100 mg/L caused composition, the phosphonate HEDP should be considered as a nutrient
an increased growth of the cyanobacterium Anabaena. During the first resource in a slowly flowing surface water. The growth of Spirulina
days of these tests, no growth stimulation occurred, rather the growth platensis based on phosphonic acids (Forlani et al., 2011) as well as
of the three species were inhibited. The authors ascribed the initial inhi- the growth stimulation of algae and the cyanobacterium Anabaena by
bition to the shortage of essential nutrients caused by phosphonate HDTMP at a wide range of concentrations (Gledhill and Feijtel, 1992)
complexation. In the course of the experiments, these phosphonates speak for the transformation of phosphonates in the environment by
were photolytically cleaved, which resulted in both the release of the some autotrophic organisms. Consequently, the contribution of
beforehand complexed nutrients and of newly formed biologically phosphonates to eutrophication, although the process may be only
available phosphate. slow, should not be underestimated.
Forlani et al. (2008) have shown that the cyanobacterium Spirulina
platensis can catalytically cleave the C\\P bond in glyphosate. Conse- 6.5. Remobilization of heavy metals
quently, Forlani et al. (2011) exposed Spirulina platensis to HDTMP as
the sole phosphorus source and also observed a partial degradation of Complexing agents are capable of dissolving metals bound in the
this phosphonate. Grohmann and Horstmann (1989), on the other sediment. Consequently, remobilized metals can potentially reach
hand, ruled out the bioavailability of the phosphonates PBTC, HEDP toxic concentrations for aquatic organisms in water, may enter the
and NTMP for Scenedesmus (green algae) and Nostoc (cyanobacteria). drinking water via bank filtrate or contribute to algal bloom (HERA,
The only previously known field trials investigating the bioavailabil- 2004). Table 5 summarizes the minimum concentrations of various
ity of phosphonates in water bodies were carried out by Grohmann and phosphonates at which a metal-remobilizing effect could be detected
Horstmann (1989). Six square concrete tanks of 10 m3 were filled in in batch extraction tests. The numbers in brackets correspond to the
parallel with groundwater from a large storage tank mixed with 2% ef- highest phosphonate concentration tested in the test for the case
fluent from a WWTP as source of nutrients (20 L/h flow rate, 21 days when no metal remobilization was observed. As a result of differences
theoretical residence time, 49 days test duration). Three different con- in the experimental conditions (pH, temperature, test duration) as
centrations of ortho-phosphate-P (approx. 20, 55 and 190 μg/L P) and well as in the kinds of sediments used, observed effect concentrations
HEDP-P (likewise) were adjusted in the tanks. Nitrate-N was dosed to differed significantly from one another. In principle, however, it can be
each tank at the same concentration of 10 mg/L. Compressed air intro- concluded that phosphonates have tendencies to preferably remobilize
duced via perforated PVC pipes on the bottoms of the tanks was used the transition metals iron, chromium and zinc. However, their remobi-
for continuous mixing, which, however, was only achievable to an un- lization only occurs at quite high phosphonate concentrations N50
satisfactory extent. In the course of the experiment, a strong dominance μg/L which are higher than those usually found in natural waters
of filamentous green algae of the genus Cladophora spec. developed. At (Section 6.1). Remobilization of the highly toxic heavy metals cadmium,
the end of the experiment, its dry mass was approximately proportional lead and mercury by phosphonates occurred only at high phosphonate
to the P concentration adjusted with ortho-phosphate in the tanks (50, concentrations of N 1 mg/L and is therefore not likely to occur in water
205 and 271 g of dry mass). Accordingly, the readily available phosphate bodies (Gledhill and Feijtel, 1992; Bordas and Bourg, 1998; Nowack,
was quasi completely incorporated into the biomass. In the basins with 2003). The comparatively weak remobilizing effect of phosphonates
HEDP feed, to some extent also the genus Cladophora spec. developed on metals was explained by their high adsorption affinity for sediment
(0, 5 and 67 g of dry mass), which was attributed to a partial uptake (Gledhill and Feijtel, 1992). Accordingly, the phosphonates become ef-
of the phosphorus from the phosphonate into biomass. The authors at- fective only when the adsorption capacity of the sediment is exceeded.
tributed this to the photolysis of the phosphonate and the successive re- The comparison of the phosphonate concentrations necessary for remo-
lease of biologically available ortho-phosphate. bilization of heavy metals found in batch extraction tests (N 50 μg/L) in-
The results of such field trials are influenced by many factors. Thus, dicated in Table 5 with the likely concentrations in surface waters,
in one basin, the formation of algae biomass exceeded the theoretically which are lower than 50 μg/L (see Section 6.1), therefore allows the as-
possible amount (55 μg/L P: 205 g of dry mass determined, 90 g of dry sessment that the risk of remobilization of heavy metals from sediment
mass theoretically possible). An influence of surrounding flora and by phosphonates can be considered to be very low.
fauna or an erroneous calculation of the theoretically possible algae bio-
mass cannot be ruled out. The authors themselves found no explanation Table 5
for this fact. The use of concrete tanks was also insufficient to simulate Phosphonate concentrations with remobilizing effect of metals from sediment (in mg/L).
Data in brackets: Maximum concentration tested in the complete absence of metal
the presence of sediments or suspended matter in water bodies.
remobilization.
Phosphonates have a high adsorption affinity for mineral surfaces
such as soils and sediments (Steber and Wierich, 1986, 1987). Substance Fe Cr Zn Cd Ni Pb Cu Hg Tl Ref.
Zaranyika and Nyandoro (1993) found for glyphosate that it is degraded PBTC (1) (1) (1) (1) – (1) (1) – – 1
more slowly in the adsorbed state than in dissolved form. According to HEDP 0.05 0.05 0.05 (5) (5) (5) (5) (5) – 2
Nowack (2003), a similar behavior can also be assumed for (1) (1) (1) (1) – (1) (1) – – 1
2.4 (2.4) (2.4) (2.4) (2.4) (2.4) (2.4) – – 3
polyphosphonates.
– – – 20 – 20 2 – – 4
The adsorption on sediment and suspended matter is considered to – – – (100) – – – – (100) 5
lead to concentrations of dissolved phosphonates in surface water gen- NTMP 0.05 0.05 0.05 (5) (5) (5) (5) (5) – 2
erally in the lower μg/L-range (Section 6.1). The total phosphorus con- EDTMP 0.05 0.05 (0.05) (5) (5) (5) (5) (5) – 2
– – 0.3–1 0.3–1 0.3–1 – – – – 6
tent of phosphonates is 10 to 30% (Table 1). However, not for all water
DTPMP 0.05 0.05 (0.05) (5) (5) (5) (5) (5) – 2
bodies a standard value can be assumed for the phosphonate concentra- – – 0.3–1 0.3–1 0.3–1 – – – – 6
tion. The discharge of untreated cooling water or membrane concen-
Ref.: reference, 1 Knepper and Weil (2001), 2 internal report from Monsanto cited by
trate contaminated with phosphonates as well as insufficiently Gledhill and Feijtel (1992), 3 Müller et al. (1984), 4 Bordas and Bourg (1998), 5 Günther
purified municipal wastewater can contribute to phosphonate concen- et al. (1987), 6 internal report from Procter and Gamble cited by Gledhill and Feijtel
trations in water that deviate strongly from the predicted average (1992).
1188 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
Müller et al. (1984) carried out laboratory experiments to examine
the remobilization of metals from suspended activated sludge by
HEDP. The metals zinc, chromium, nickel, copper, lead and cadmium
were not remobilized by 2.4 mg/L HEDP. On the other hand, an increase
of the solute concentration of iron was observed. Müller et al. (1984)
also made a similar observation on a WWTP. The addition of 2 mg/L of
HEDP to the feed of the WWTP caused significantly higher concentra-
tions of iron in the discharge of the primary clarifier compared to the
regular operation situation. However, due to the adsorptive removal of
the phosphonate in the subsequent activated sludge stage, the com-
plexed iron was removed with the adsorbed phosphonate, so that no re-
sidual concentration of iron in the wastewater was detectable. Zinc,
chromium, nickel, copper, lead and cadmium did not show any unusual
behavior. These findings indicate that there is no metal remobilization
to be expected from activated sludge due to phosphonates, however,
still more investigations are needed in order to make a sure statement.
7. Summary
Articles on phosphonates with respect to their environmental rele-
vance and degradability were published mainly in the periods
1985–1995 and 1998–2005. In the last 10 years, this subject has been
rarely addressed. However, with the significant increase in phospho-
nate production and consumption over the last few years also the inter-
est in their environmental behavior increased causing an increasing
need for research. In the following, the findings on the state of knowl-
edge regarding the environmental relevance of phosphonates and
their removal from wastewater are summarized.
Biodegradability and removal in municipal WWTPs:
• Only a very small proportion of classes of microorganisms in the envi-
ronment (including those constituting activated sludge) is capable of
degrading PBTC and polyphosphonates (Raschke et al., 1994;
Schowanek and Verstraete, 1990).
• The microbial degradation of phosphonates takes place preferably in a
phosphate-free environment in the presence of other carbon sources
(Raschke et al., 1994; Schowanek and Verstraete, 1990).
• In aerobic OECD tests, phosphonates were usually only partially min-
eralized, even after several weeks. At the same time, relatively high
DOC removal rates, which were attributed to adsorption onto activat-
ed sludge, were also occasionally observed (Table 2).
• Phosphonates were not significantly converted to digester gas (CO2,
CH4) under anaerobic conditions (Steber and Wierich, 1986, 1987;
Nowack, 1998).
• With the exception of PBTC, which adsorbed poorest of all
phosphonates, polyphosphonates adsorbed well on activated and
digested sludge (Table 3).
• Phosphonates adsorbed stronger in an acidic pH milieu than between
pH 6 and 9 (Nowack, 2002b).
• Water hardness improved the adsorption of phosphonates onto acti-
vated sludge (Nowack, 2002b).
• With the exception of PBTC, phosphonates, once adsorbed onto acti-
vated sludge, no longer desorbed under anaerobic conditions
(Reichert, 1996).
• In the literature, largely high removal rates of polyphosphonates in
WWTPs (N80%) are described mostly with effluent concentrations
below the LOQ/LOD, except for the publication of Metzner (1990) (re-
moval rates of 25–70%) (Table 4). However, the LODs are in such a
high range (e.g., 0.057 mg/L in the case of DTPMP (Nowack, 1998))
that a contribution of phosphonates to the eutrophication of water
cannot be excluded. Furthermore, no studies exist so far about the be-
havior of PBTC in WWTPs.
• In some aerobic degradation tests, only very low adsorption rates of
phosphonates onto activated sludge were observed. In particular,
nitrogen-free phosphonates, such as PBTC, seem to be subject to a
smaller extent of removal (Reichert, 1996).
• Already phosphonate concentrations b 1 mg/L can have a negative ef-
fect on phosphate precipitation in WWTPs. The effect can, however,
be overcome by an increased precipitant concentration (Horstmann
and Grohmann, 1984, 1986).
• Phosphonates can cause the need of high precipitant excesses
(Horstmann and Grohmann, 1984, 1986), a deficiency of phosphorus
as nutrient in the biological treatment (Wenger-Oehn et al., 2005) and
can lead to problems with the compliance with phosphorus limit
values (König et al., 2002).
Environmental relevance of phosphonates:
• Calculations (Gledhill and Feijtel, 1992; Jaworska et al., 2002) and first
measurements (Schmidt et al., 2014) suggest that phosphonates are
present in water in concentrations in the lower μg/L range. However,
currently there are no more detailed investigations.
• Phosphonates accumulate in sewage sludge in concentrations of ca.
1.2–1.5 g/kg dry substance.
• The contamination of groundwater with phosphonates has been
assessed to be low, but a comprehensive risk assessment is missing
(Knepper, 2003).
• Phosphonates are present in surface waters mainly in the form of
Ca2+ and Fe2+ complexes (Nowack, 2003; Jaworska et al., 2002) as
well as adsorbed to sediment particles and suspended matter
(Steber and Wierich, 1986, 1987; Fischer, 1992).
• Phosphonates are subject to a variety of transformation and degrada-
tion mechanisms in the aquatic environment resulting in the release
of bioavailable phosphate: degradation by MnII and O2 (Nowack and
Stone, 2000), hydrolysis (Schowanek and Verstraete, 1990, 1991)
and metal-catalyzed photolysis (Matthijs et al., 1989; Grohmann
and Horstmann, 1989).
• The phosphonates investigated so far are neither mutagenic, carcino-
genic nor teratogenic, and are classified as harmless for a wide range
of aquatic organisms (Gledhill and Feijtel, 1992; Maise, 1984;
Metzner and Nägerl, 1982; Kästner and Gode, 1983; HERA, 2004).
Their degradation products AMPA and glyphosate, however, are clas-
sified as critical from a toxicological point of view (Mañas et al., 2009;
de Roos et al., 2003; Eriksson et al., 2008; Hardell et al., 2011).
• The contribution of phosphonates to the eutrophication of water
should not be underestimated since phosphonates are subject to nat-
ural degradation mechanisms (Matthijs et al., 1989; Grohmann and
Horstmann, 1989; Nowack and Stone, 2000). In some experiments,
phosphonates were even stimulating the growth of green algae and
cyanobacteria (Gledhill and Feijtel, 1992; Forlani et al., 2011).
• Phosphonates are discussed in context with the remobilization of
metals bound to sediments and activated sludge, however, the con-
centrations measured in surface waters so far are considered to be
too low for remobilization of significant amounts of metal (Gledhill
and Feijtel, 1992; Bordas and Bourg, 1998; Müller et al., 1984).
8. Conclusions
Phosphonates are very stable against biological degradation. In the
literature, however, predominantly good removal efficiencies on
WWTPs (80–95% removal) are mentioned, which are attributed to the
high tendency of phosphonates to adsorb onto sewage sludge. On the
other hand, it is questionable whether phosphonates can be adequately
removed in WWTPs operating with enhanced biological phosphorus re-
moval instead of phosphate precipitation, so that there is still demand
for research in this area. The LOQs of analytical methods applied for
the quantification of phosphonates were relatively high. Thus, despite
the removal efficiencies in WWTPs determined by these methods ap-
pear to be high, there is a risk that phosphonates contribute to a certain
degree to the eutrophication of water, particularly as phosphonates un-
dergo natural degradation such as metal-catalyzed photolysis, weak
 E. Rott et al. / Science of the Total Environment 615 (2018) 1176–1191
hydrolysis and catalytic degradation by MnII and O2. It can be assumed
that at least 9000–18,600 t/a of phosphonates reach European surface
waters via direct discharge and WWTPs. Phosphonate concentrations
of 0.5–2.9 μg/L have been measured in some German rivers, but higher
concentrations can occur locally. Moreover, at least 7300 t/a of
phosphonates are discharged via sewage sludge used in agriculture in
Europe. It is assumed that the concentrations of phosphonates in
water bodies are currently too low for a significant heavy metal
remobilizing effect by complex formation. However, if the phosphonate
concentration will increase in future, remobilized metals may reach
toxic concentrations for aquatic organisms or get into the drinking
water via bank filtrate. Although, phosphonates are classified as harm-
less for a wide variety of aquatic organisms, some degradation products
of aminophosphonates, such as N-(phosphonomethyl)glycine and
aminomethylphosphonic acid (AMPA), have to be seen very critical
from an ecotoxicological point of view. Particularly, it is strongly recom-
mended not to discharge wastewater containing phosphonates without
pretreatment, since the contribution of phosphonates to eutrophication
of weak receiving waters, in particular, cannot be excluded. In the case
of indirect discharges, it has to be assured that very high concentrations
of phosphonates are not present in the inflow of WWTPs. Otherwise in-
creased precipitant dosing quantities are necessary for P removal, which
then might cause a deficiency of this essential nutrient in the biological
treatment step. Thus, in any case there should be a pretreatment of
phosphonate containing industrial partial stream wastewaters prior to
discharging them into the receiving water or WWTPs. For this purpose,
several physicochemical treatment methods are presented in various
scientific articles. In particular, processes using metal salts or metal-
containing materials such as the precipitation/flocculation method
(Rott et al., 2017a; Fettig et al., 2000; Klinger et al., 1998), Photo-
Fenton method (Rott et al., 2017b), UV/FeII treatment (Lesueur et al.,
2005; Rott et al., 2017b) or filtration using iron-containing materials
(Chen et al., 2017; Boels et al., 2010) are very promising. Whereas the
use of activated carbon is not recommended for the targeted removal
of phosphonates from wastewater (Klinger et al., 1998).
Acknowledgements
The authors are grateful for the financial support by the Willy-
Hager-Stiftung, Stuttgart.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2017.09.223.
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