Archives of Environmental Contamination and Toxicology (2022) 82:48–61

https://doi.org/10.1007/s00244-021-00893-5

ORIGINAL PAPER

Phytotoxic Effects of Antibiotics on Terrestrial Crop Plants and Wild

Plants: A Systematic Review
Matilde Carballo1 · Antonio Rodríguez1 · Ana de la Torre1

Received: 16 April 2021 / Accepted: 21 September 2021 / Published online: 20 October 2021
© The Author(s) 2021

Abstract
This review examines the state of knowledge on the phytotoxic effects of antibiotics on terrestrial crop plants and wild
(non-crop) plants with the goal of evaluating differences in their sensitivity. This is important because environmental risk
assessments of antibiotics currently consider their potential effects only on crop species but not wild species. Overall, we
analysed 275 datasets consisting of antibiotic-plant species-endpoint combinations for germination (mg/L) and 169 datasets
for plant growth (elongation and biomass) (mg/kg). EC10 and EC50 of each parameter were compared using a quotient
approach, in which the geometric mean and the 5th percentile of the crop data were divided by wild data. Quotients were > 1
for elongation growth, suggesting that wild species were more sensitive than crops, while they were < 1 for biomass growth,
suggesting quite the contrary. However, < 1% of the data in each dataset came from wild species, preventing definitive con-
clusions. Merging crop and wild data to evaluate differences in sensitivity among classes of antibiotics and plant families,
we found using a linear mixed effect model and post hoc test that plants were most sensitive to phenicol and least sensitive
to macrolides and tetracyclines. Further work must be conducted to gain a better understanding of the phytotoxic effects of
antibiotics on terrestrial wild plants and subsequently assess whether the current approach to environmental risk assessment
of antibiotics is sufficient to protect plant biodiversity.

Antibiotics play a major role in the maintenance of public The accumulation of antibiotics in the soil can alter the
and animal health. However, excessive use of antibiotics has structure and activity of microbial communities, increase the
resulted in the accumulation of micro-contaminants in soil abundance of resistance genes in soils (Llor and Bjerrum,
and water ecosystems over the last 20 years (Grenni et al. 2014; Carvalho et al., 2014), as well as inhibit the growth
2018). In 2017, the European Union (EU) reported the use of and performance of plants (Cycon and Piotrowska-Seget
nearly 5930 types of antibiotics in livestock farming (EMA 2019; Kumar et al. 2012). Antibiotics can exert phytotoxic
2019). These antibiotics are poorly absorbed in the gut of effects directly, for example, by decreasing the rate of res-
livestock animals and as much as 90% of certain antibiotics piration or synthesis of chlorophyll, as well as indirectly by
may be excreted in manure, resulting in the accumulation disbalancing plant–microbe symbiotic relationships (Kumar
of micro-contaminants in agro-ecosystems (Kumar et al. et al. 2005; Dolliver et al., 2008; Grote et al. 2007; Kuchta
2005). In the last decade, antibiotics have been found in soil et al. 2009; Carter et al. 2014; Carvalho et al. 2014).
matrices of areas fertilised with manure and areas used for Phytotoxicity of antibiotics can be observed in crop spe-
grazing (0.4 ng to 25 mg per kg of soil) (Cycon et al. 2019). cies, as well as in wild (non-crop) species present in pas-
tureland and adjacent habitats such as field margins. Such
non-crop species are important since they provide a wide
range of ecosystem services to agro-ecosystems, including
Matilde Carballo and Ana de la Torre have contributed equally to provisioning, regulating, and supporting services (Arts et al.
this work 2015; Boutin et al. 2014). These diverse floral resources
(e.g. forbs, legumes) can support pollinator services by pro-
* Ana de la Torre
[email protected] viding habitats to bumblebees, hoverflies, butterflies, and
honey bees that pollinate native plants in grasslands, thereby
1
Animal Health Research Centre, National Institute enhancing the pollination of agricultural crops (Hendrick-
for Agricultural and Food Research and Technology (INIA), son and Sanderson 2017; Kaluza et al. 2017). Therefore, the
Valdeolmos, Madrid, Spain

13
Vol:.(1234567890)
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 49

protection of wild (non-crop) species is critical to preserv- This systematic review was performed based on the
ing biodiversity, as stated in the recommendations of the guidelines recommended in the Joanna Briggs Institute
European Green Deal, which aims to protect, conserve, and Reviewer’s Manual (2017). The aim of this review was to
enhance the natural capital of the EU (European Commis- gain a better understanding of the sensitivity of crop and
sion 2019). wild plant species by assessing the number of papers pub-
In 2010, the European Food Safety Authority published lished on this subject, the most commonly studied antibiotics
a framework to identify specific protection goals for the and plant species, the different assay methods used to quan-
biological community based on ecosystem services that tify toxicity, the endpoints of those assays, the time periods
can be affected by plant protection products (PPP), such as during which the toxic effects were measured, and the type
conserving biodiversity (European Food Safety Authority of samples used for analysis.
2010, 2014; European Food Safety Authority 2016). Fur- Based on Peters et al. (2020), we used a four-step strat-
thermore, stakeholders at a workshop of the Society of Envi- egy to select articles for the review (Fig. 1). We identified
ronmental Toxicology and Chemistry (SETAC) in Europe relevant articles indexed in the electronic databases based
concurred that wild (non-crop) species need to be protected on the search terms “antibiotic” and “phytotoxicity” in com-
at the level of the population or higher, and that species bination with Boolean operators. After screening titles and
abundance, biomass, and cover are important attributes asso- abstracts, we removed duplicate records and articles whose
ciated with maintenance of ecosystem services (Arts et al. scope did not match the theme of interest. Reviews were also
2015). During that workshop, several important knowledge excluded. We included only articles published in English
gaps were identified to address these goals. For example, that reported experimental data. After conducting a full-text
only crop species, not wild plants, are typically used in labo- screening of the articles identified, we retained only those
ratory and greenhouse experiments to test phytotoxicity of that reported data on the following characteristics: name
plant protection products (PPPs), and these tests form the of the first author, year of publication, type of study, assay
basis of legally mandated environmental risk assessments
(ERAs). Stakeholders have expressed concern about the lack
of information about wild species, leading to doubts about
whether ERAs can protect biodiversity. A literature review
of studies on the phytotoxicity of PPPs towards crop and
wild plant species (Christl et al. 2019) found no consistent
sensitivity differences between crop and wild plant species,
implying that ERAs of PPPs can adequately protect plant
species biodiversity.
Although there is sufficient information on phytotoxicity
caused by plant protection products, very few studies have
focussed on the potential phytotoxic effects of antibiotics on
plants. In this study, we conducted a systematic review of the
information available on the phytotoxic effects of antibiot-
ics on terrestrial crop and wild plant species. Our goal was
to gain a better understanding of the sensitivity of crop and
wild plant species to antibiotics and thereby assess whether
ERAs of veterinary medicines are robust enough to protect
plant species biodiversity.

Methods

For this descriptive, cross-sectional study, we systematically

examined electronic databases, including PubMed, Scopus,
Web of Science, and Google Scholar, to identify studies pub-
lished between January 1980 and March 2020 that examined
the phytotoxic effects of antibiotics used in veterinary medi-
cine on terrestrial plants. Data retrieval was conducted using
the direct query and access method. Fig. 1  Flow diagram of the literature screening

13
50 Archives of Environmental Contamination and Toxicology (2022) 82:48–61

characteristics, assay duration, medium, assay conditions, Studies were classified into two, non-overlapping groups
endpoint unit, substance application method, as well as the based on the type of data collected: one group consisted of
results and units for all antibiotics and plant species that germination and growth studies that were performed on soil
were assayed (Table 1). samples and reported results as mg/kg, while the other con-
sisted of germination studies that were performed on other
substrates and reported results as mg/L.
Table 1  Data extracted during full-text screening of relevant articles Data were included in the two groups using an approach
identified for the systematic review
similar to that of Christl et al. (2019). Data were included
Characteristic on seed germination (radicle, hypocotyl or cotyledon emer-
Type of study Experimental gence), elongation growth (root, shoot and total length),
and biomass growth (root, shoot and total weight) (Fig. 2).
Type of assay Standardised, non-standardised Biomass data were included without differentiating between
Medium Soil, other wet or dry weight. For endpoint data reported as “greater
Assay conditions Temperature, light, duration, no. con- than” the highest rate or “less than” the lowest rate, “greater
centrations, no. replicates, no. seeds
than” values were multiplied by 2 and “less than” values
Endpoints Germination, length, growth
were divided by 2, based on the approach of Christl et al.
Units mg/kg, mg/L, fresh weight, dry weight
(2019). Based on the same approach, non-observed effect
Substance application Water, solvent, other
concentrations (NOECs) were converted into effect concen-
Results EC50, EC10, NOEC
tration 10 (EC10) values by assuming that EC10 > NOEC.
Units mg/L, mg/kg
NOEC values ≥ EC10 were multiplied by 2, and NOEC val-
Antibiotic tested Name and class
ues < EC10 were divided by 2. Endpoints from multiple tests
Plant species assayed Latin and common name
on the same plant species and antibiotic were merged as their
EC (effect concentration) 50 = concentration at which 50% of effect geometric means in order to avoid bias due to more frequent
(e.g. inhibition of germination or growth) is observed compared to testing of certain species.
the control group; EC 10 = concentration at which 10% of effect is After merging all the available data, we initially com-
observed compared to the control group; NOEC (no observed effect
concentration) = is the highest tested concentration that failed to give pared the sensitivity of crop and wild species using the ECx
a result significantly different from that in the control

Fig. 2  Illustration of the ecotoxicological endpoints of seed germination and plant

13
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 51

endpoint (EC50, EC10) for each measured variable (seed The characteristics of the studies included in this sys-
germination, elongation growth, and biomass growth). tematic review are listed in Table 2. Overall, these stud-
For this purpose, we used the quotient approach proposed ies were classified into two groups: those evaluating seed
by Christl et al. (2019), which uses two reference points emergence, and those evaluating plant growth. In the first
(RPs) recommended for risk assessment in the “Guideline group, seed emergence was evaluated using standardised
on the plant testing strategy for veterinary medicinal prod- guidelines developed by international organisations such as
ucts” (EMA/CVMP/ERA/689041/2015): (a) RPgeo, which the Environmental Protection Agency (EPA), the American
is reported as the geometric mean and can protect 50% of Society for Testing and Materials (ASTM) and the Interna-
the species; and (b) RPmin, which is reported as the haz- tional Seed Testing Association (ISTA). In these studies, all
ardous concentration for 5% of the population (HC5) or ­5th assays were performed in a Petri dish with filter paper, and
percentile of the species sensitivity distribution (SSD), cor- seed growth occurred mainly in the dark in culture media
responding to protection of 95% of the species. For those other than soil. Seed emergence and seed growth (radicle,
groups or variables with at least three different points on the hypocotyledon, and cotyledon length; mg/L) were recorded
SSD, namely three EC values from three different plant spe- within 14 days after the start of the assay, mostly in the first
cies-antibiotic combinations, calculations were performed week (Fig. 2). In five studies, we found further informa-
using ETX 2.0 software (Van Vlaardingen et al. 2004). tion on plant growth after 14 days using sand as a culture
Each resulting RP value for crop species was divided by the medium. The second group of studies evaluated plant growth
corresponding RP value for wild species. In this approach, on the basis of the OECD 208 standardised test. Here, all
quotients above 1 indicate that wild species are more sensi- assays were performed in the soil, plant growth occurred
tive than crop species, while quotients below 1 indicate the mainly under light/dark conditions, and seed emergence and
opposite. plant growth (length and fresh/dry biomass; mg/kg) were
Although we would have preferred to compare endpoints recorded at 28 days after the start of the assay (Fig. 2).
across different classes of antibiotics and plant families, we The first group had a larger number of studies (n = 20)
were unable to do this for lack of sufficient data: rarely were and more data on toxicity, but their results did not resem-
data on a given antibiotic available for at least three crop and ble in vivo conditions. The principle of the seed emergence
three wild species. Therefore, differences in toxicity among assay is to determine seed vigour, which can reliably predict
classes of antibiotics and plant families were explored for field performance. This assay is usually applied to monitor
the merging crop and wild data from studies on plant growth the viability of stored seed collections, but it has also been
(mg/kg), elongation growth and biomass growth, which are recommended for obtaining information on the germination
more sensitive parameters than seed germination (Ghava requirements of threatened species (Clemente 2017). Seed-
et al. 2015; Pan and Chu 2016; Bellino et al. 2018; Liu et al. ing is a conservative process, and the seed coat acts as a bar-
2009a; Wang et al. 2019). A linear mixed effects (LME) rier to protect the plant embryo from the negative impacts of
model (Lindstrom and Bates 1988) was used in which ECx environmental contaminants such as pharmaceuticals (Hillis
were considered as random factors in order to control the et al. 2011; Rede et al. 2019).
differences in the incidence values due to intrinsic features In contrast, the second group had fewer studies (n = 14),
of each antibiotic class or plant family. When the effects but was more representative of field conditions since the
were significant based on 95% confidence intervals, a post studies used soil as the medium. It is widely accepted that
hoc Tukey test (HSD) was performed using the emmeans R elongation and vegetative parameters are sensitive endpoints
package (Lenth et al. 2019). to evaluate phytotoxic effects caused by the physical inter-
action of roots with antibiotics and other soil contaminants
(Minden et al. 2017).

Results and Discussion Plant Species and Antibiotics

Characteristics of Included Studies We collected 169 data records on plant species, antibi-
otics, and toxicity endpoints from studies performed in
A total of 644 studies were identified from the databases soil (mg/kg) and 275 data records from studies performed
examined, including 206 from PubMed, 253 from Scopus, in other media (mg/L). This is one of the limitations of
and 185 from Web of Science (Fig. 1). We were unable to our study, since each of these groups accounted for < 10%
identify any additional studies from Google Scholar. After of the data on PPPs that were analysed by Christl et al.
a detailed assessment based on the eligibility criteria and (2019). Furthermore, most of the data analysed in the pre-
availability of data, 34 unique studies were selected for fur- sent study were from crop species: the data from wild spe-
ther analysis. cies accounted for < 1% of the data in each group, much

13
 52

Table 2  Characteristics of studies included in the systematic review on the phytotoxic effects of antibiotics on plant species
Reference Sudy id Assay id Method Duration (d) Medium Light Temp (ºC) No. Seeds Substance application No. and range Replicates Unit
of concentra-

13
tions

Timmerer et al. 2020 1 1 Phytobiotest MBT 5 Filter paper Dark 23 9 Citric acid buffer 5–11 4 mg/L
Pino et al. 2016 2 1 OECD 1984 5 Filter paper Dark 22 20 Water 5 3 mg/L
Hillis et al. 2011 3 1 ASTM 2003 5–7 Filter paper Dark 24 10 Water 6 5 mg/L
Tasho et al. 2020 4 1 ISTA 1985 6 Soil Dark 25 5 Water 9 3 mg/kg
2 Non- standardised 15 Soil Light/Dark 25 5 Manure 9 3 mg/kg
Luo et al. 2019a 5 1 Non-standardised 2 Filter paper Dark 25 20 Water 7 4 mg/L
2 Non- standardised 2 Filter paper Dark 25 160 Water 7 0 mg/L
Luo et al. 2019b 6 1 Non- standardised 2–3 Filter paper Dark 25 160 Water 7 0 mg/L
Rede et al. 2019 7 1 EPA 2012 5 Soil Light/Dark 24 20 Water 9 9 mg/kg
Litskas et al. 2019 8 1 OECD 1984 21 Soil Light/Dark 25 20 Water 5 3 mg/kg
Parente et al. 2018 9 1 OECD 1984 16 Soil Light/Dark 25 5 Water 7 4 mg/kg
Elezz et al. 2019 10 1 Non- standardised 6 Filter paper Light/Dark 10 Water 5 4 mg/L
Wieczerzak et al. 2018 11 1 Phytobiotest MBT 3 Cotton wool Dark 23 10 Water 5 3 mg/L
Menezes-Oliveira et al. 12 1 ISO 2012 21 Soil Light/Dark 20 10 Acetone 6 4 mg/kg
2018
Dipshika and Mehta, 13 1 Non- standardised 7 Filter paper Light/Dark 25 30 Water 6 3 mg/L
2018
Bellino et al. 2018 14 1 Non- standardised 10 Filter paper Dark 25 20 Water 5 5 mg/L
2 Non- standardised 7 Filter paper Dark 25 20 Water 5 0 mg/L
Litskas et al. 2019 15 1 OECD 1984 21 Soil Light/Dark 25 5 Water 5 4 mg/kg
Pan and Chu. 2016 16 1 ASTM 2003 5–7 Filter paper Dark 25 20 Water 6 5 mg/L
Orzoł and Piotrowicz- 17 1 Phytobiotest MBT 7 Filter paper Dark 23 10 Water 8 4 mg/L
Cieślak 2017 2 Phytobiotest MBT 12 Filter paper Dark 23 10 Water 8 4 mg/L
Rydzyński et al. 2017 18 1 Non- standardised 30 Soil Light/Dark 19_23 300 Water 5 1 mg/kg
Riaz et al. 2017 19 1 Non- standardised 2 Filter paper Dark 26 Water 8 3 mg/L
2 Non- standardised 20 Sand Light/Dark 25_21 Water 3 3 mg/L
Minden et al. 2017 20 1 Non-standardised 14 Filter paper Dark 24 100 Water 3 9 mg/L
2 Non- standardised 56 Filter paper Light/Dark 24 10 Water 3 9 mg/L
Richter et al. 2016 21 1 OECD 1984 28 Soil Light/Dark 22 20 Acetone 4 mg/kg
Eluk et al., 2016 22 1 ASTM 2003 7 Filter paper Dark 25 10 Water 4 5 mg/L
Ghava et al. 2015 23 1 Non- standardised 12 Filter paper Dark 24 5 Water 6 3 mg/L
Furtula et al. 2012 24 1 EC 2005 14 Soil Light/Dark 24 10 Water 8 6 mg/kg
Xie et al., 2011 25 1 Non- standardised 3 Water Dark 25 600 Water 10 0 mg/L
Wang et al. 2019 26 1 Non- standardised 4 Filter paper Dark 25 10 Water 5 3 mg/L
Pannu et al. 2012 27 1 Non- standardised 10 Soil Light/Dark 25 30 Methanol 3 4 mg/kg
Archives of Environmental Contamination and Toxicology (2022) 82:48–61
 Archives of Environmental Contamination and Toxicology (2022) 82:48–61 53

less than the 60% in the analysis by Christl et al. (2019).

mg/kg
mg/kg
mg/kg
mg/kg
mg/kg

mg/L
mg/L
mg/L
mg/L
mg/L
mg/L
Replicates Unit It is clear that the effects of antibiotics on plants, particu-
larly non-crop species, have received very little attention
(Minden et al 2017).
Data records were available for 12 antibiotic classes

10
(aminoglycosides, bisphenols, diaminopiridines, fluoroqui-

6
6
6
3
3
3
3
3

?
nolones, ionophoric, lincosamides, macrolides, penicillines,
Temp (ºC) No. Seeds Substance application No. and range
of concentra-

phenicol, quinolones, sulfonamides and tetracyclines) and

eight plant families (Apiaceae, Asteraceae, Brassicaceae,
tions

Cucurbitaceae, Fabaceae, Liliaceae, Poaceae and Solan-

7–8
7–8

5
5
5
3
3
7
7
7

aceae) (Table 3). The most frequently assayed antibiotics

with endpoint data (ECx) from crop and wild species were
Sodium hydroxide

tetracyclines (total n / crop n / wild n = 99 / 96 / 3), sulphona-

mides (75 / 73 / 2), quinolones (45 / 44 / 1), macrolides (66
Methanol / 60 / 6), and penicillins (29 / 26 / 3). Nearly all these anti-
Methanol
Methanol
acetone

biotic classes are top-sellers in the EU, with tetracyclines

Water
Water
Water
Water
Water
Water

accounting for 32.6% of antibiotic sales; penicillins, 28.8%;

sulphonamides, 9.8%; and macrolides, 7.9% (EMA 2019).
144_206

The most frequently evaluated plant families with data on

30_60
15–20
8–10

crop and wild species were Poaceae (total n / crop n / wild

2_5
1_8

15
15

6
6
6

n = 100 / 193 / 7), Fabaceae (71 / 66 / 5) and Brassicaceae

(56 / 53 / 3) (Table 4). There were no data on wild spe-
cies of any of the other plant families. The most common
26
26
26
25
20
20
25
25
25
25
25

crop species observed were the two cereals Oryza sativa and
Light/Dark
Light/Dark
Light/Dark

Triticum aestivum (Poaceae), as well as Brassica campes-

tris and Brassica napus (Brassicaceae), and Lupinus luteus
Light
Light
Light

Dark
Dark
Dark
Dark
Dark
Dark

and Phaseolus vulgaris (Fabaceae). Most of these crops are

listed in Annex 2 of the OECD 208 Terrestrial Plant Test,
Filter paper

M medium
M medium
M medium

which is the assay recommended in the “Guideline on the

Duration (d) Medium

plant testing strategy for veterinary medicinal products”

agar
agar

Soil
Soil
Soil
Soil
Soil

(EMA/CVMP/ERA/689041/2015). These species are com-

mon crop species in the EU, except Lupinus luteus, which
is a forage crop whose cultivation has decreased greatly in
recent decades. Poaceae cereals, including rice, are the main
17–27
17–37
2–5
4–5

crops grown in the EU-28 (Eurostat 2017), and they occupy

28
21
14
15
20
20

32.3% of the total arable land. Among these species, rice

Non- standardised
Non- standardised
Non- standardised
Non- standardised
Non- standardised
Non- standardised
Non- standardised
Non- standardised

(Oryza sativa) accounts for > 3% of cropland, while wheat

OECD 1984
OECD 1984

(Triticum aestivum) accounts for 46%. Pulses (Fabaceae) and

ISTA 1985

vegetables (Brassicaceae) are grown, respectively, on 1.2%

Sudy id Assay id Method

and 1.1% of EU cropland.

The wild species analysed were Apera spicaventi, Fes-
tuca arundinacea, and Lolium perenne (Poaceae), Cap-
sella bursa-pastoris (Brassicaceae), and Trifolium pratense
3
2
1
1
1
1
2
1
1
2
1

(Fabaceae). They are common weed species, or species

found in the margins of fields in Europe; in some cases, they
are native (or cultivated) forage crops, meadow, grassland, or
34
33
32
31
30
29
28

pasture species (Polunin 1977; Gómez 2008). Floral diver-

sity in crop margins can play a relevant ecological role in the
Table 2  (continued)

Migliore et al. 1995

Migliore et al. 2003

agricultural landscape by providing a niche for invertebrates

Sidhu et al. 2019
Hillis et al. 2008
Liu et al. 2009b
Liu et al. 2009a

and serving as an important food source for birds (Vickery

Jin et al. 2009

et al. 2009). None of the wild species analysed in the present

Reference

study, except Trifolium pratense, is listed in Annex 3 of the

OECD 208 Terrestrial Plant Test.

13
54 Archives of Environmental Contamination and Toxicology (2022) 82:48–61

Table 3  Antibiotics assayed in the germination studies (mg/L) and growth studies (mg/kg) included in the systematic review on the phytotoxic
effects of antibiotics on plant species
Crop data (mg/L) Crop data (mg/kg) Wild data (mg/L) Wild data (mg/kg)

Class Antibiotic Study ID Study ID Study ID Study ID

Aminoglycosides Kanamycin 22
Spectinomycin 14 4
Bisphenols Triclosan 27, 29
Diaminopiridines Trimethoprim 2, 3, 28 28
Fluoroquinolones Enrofloxacin 1, 10, 19, 22, 26, 31 30
Ionophoric Monensin 34 12
Salinomycin 24
Lincosamides Lincomycin 3
Macrolides Azithromycin 33 33
Erythromycin 16
Spiramycin 14
Tylosin 3, 10, 28, 34 21, 28 21
Penicillines Amoxicillin 3, 13, 23 15, 7 15
Penicillin 20 20
Phenicol Chloramphenicol 11, 14, 16
Florfenicol 21
Quinolones Ciprofloxacin 9, 18, 33 33
Levofloxacin 3, 17, 19, 23, 34
Norfloxacin 16
Ofloxacin 26
Sulfonamides Sulfadiazine 1, 20 30 20
Sulfadimethoxine 4
Sulfamethazine 3, 16, 28 28
Sulfamethoxazole 3, 28 28
Sulfamonomethoxine 30
Sulphadimethoxine 32
Tetracyclines Chlortetracycline 3, 28, 34 28
Doxycycline 26, 36 8
Oxytetracycline 3, 11, 26, 34 4, 9 9
Tetracycline 1, 2, 3, 5, 6, 13, 16, 20, 18, 28 20
23, 25, 28, 34

Native species are expected to show more variation in include at least three different EC50 and three different
sensitivity than crop species (Olszyk et al. 2008). Based on EC10 values from wild plant species. In contrast, we found
the endpoint data (ECx) collected from the plant growth differences in sensitivity when we assessed the datasets from
studies performed on soil (mg/kg), wild plant toxicity data the studies on plant growth (mg/kg). When we compared
fell within the range of crop plant toxicity data (Fig. 3). endpoints for elongation, we found that wild species were
However, the ranges plotted for crop species were broader more sensitive (Q > 1) but when we compared endpoints
than those for wild species, which may reflect the lack of for biomass, we found that wild species were less sensitive
data on wild species. (Q < 1). However, due to the lack of data on wild species
(n = 3), we could not detect reliable differences in sensitivity
Quotient Approach between crops and wild species.

Based on the quotient approach, we calculated the differ- Wild Species Sensitivity
ences in sensitivity between crop and wild plant species
(Table 5). We were unable to calculate average quotients Several studies comparing the effects of antibiotics on crop
for the data on seed emergence (mg/L), since they did not and wild species from the same plant family have reported

13
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 55

Table 4  Plant species assayed in the germination (mg/L) and growth studies (mg/kg) included in the systematic review on the phytotoxic effects
of antibiotics on plant species
Family Specie Common Study Id Crop Study Id Crop Specie Common Study Id Study Id Wild
Name Data (mg/L) Data (mg/kg) Name Wild Data Data (mg/kg)
(mg/L)

Apiaceae Daucus carota Carrot 3, 16, 34 4

Lactuca sativa Lettuce 33, 27, 4, 7,
15
Asteraceae Cichaorium Sweet oat 28
endivia
Lactuca sativa Lettuce 2, 3, 16, 31
Brassicaceae Raphanus Radish 27, 9 Capsella Shepherd’s 20
sativus bursa-pas- purse
toris
Brassica Cabbage 26 30
campestris
Brassica rapa Cabbage 5, 6 24, 30, 12
Brassica Cabbage 6
oleracea
Brassica Oilseed rape 20, 26 21
napus
Sinapis alba Mustard 1 21
Raphanus Radish 31 33
sativus
Cucurbitaceae Cucurbita Pumpkin 8, 15
pepo
Cucumis Cucumber 16, 26, 28, 31 29, 28
sativus
Fabaceae Lupinus luteus Yellow lupin 17 Trifolium Red cover 21
pratense
Medicago Alfalfa 3 18
sativa
Phaseolus Common bean 31 21, 8
vulgaris
Pisum sativum Pea 32 8, 15
Liliaceae Allium cepa Onion 21, 9
Poaceae Avena sativa Oat 21 Apera spi- Loose silky- 20
caventi bent
Hordeum Barley 10 Festuca arun- Grass 33, 15
vulgare dinacea
Panicum mili- Proso millet 32 Lolium per- Ryegrass 9
aceum enne
Paspalum Bahia grass 27
notatum
Oryza sativa Rice 13, 28 28, 29
Sorghum Sorghum 11
bicolor
Triticum Wheat 19, 20, 22, 30, 12
aestivum 23, 25
Zea mays Corn 32 8, 15
Solanaceae Solanum lyco- Tomato 14, 16 21, 8, 30, 15
persicum
Capsicum Pepper 4
annum

13
56 Archives of Environmental Contamination and Toxicology (2022) 82:48–61

Fig. 3  Endpoints (ECx) for each variable for a crop species (mg/kg soil), b wild species (mg/kg soil) and c crop species (mg/L solution)

that antibiotics may be equally or more harmful to wild similar to those detected in the soil did not adversely affect
plant species than to crop species. One study on Poaceae the germination rate of crop or wild species (Minden et al.
species reported no significant differences in sensitivity to 2017). Nevertheless, exposure to those antibiotics did delay
amoxicillin between crop species (Zea mays) and wild spe- germination and affected plant growth at later stages (e.g.
cies (Festuca arundinacea) (Litskas et al. 2019). However, canopy and chlorophyll production). These effects were
the authors of that study highlighted that amoxicillin can stronger in non-crop species (Capsella bursa-pastoris; Bras-
degrade rapidly in soil, decreasing the risk of acute toxic- sicaceae and Apera spicaventi; Poaceae) than in crop spe-
ity in plants. Another study reported that tylosin negatively cies (Brassica napus; Brassicaceae and Triticum aestivum;
affected emergence and growth of Fabaceae species, and that Poaceae). The results of that study indicate that antibiot-
non-crop species (Trifolium pratense) were more sensitive ics can affect the growth of wild plant species to a larger
than crop species (Phaseolus vulgaris) in terms of EC10 extent than they affect the growth of crop species. This can
(7.7 vs. 9.1 mg/kg) and EC50 (23.5 vs. 107 mg/kg) (Richter affect the composition of plant communities at field margins,
et al. 2016). which may trigger changes in species composition and affect
A study on plant species from the Poaceae and Brassi- biodiversity in the region (Minden et al. 2017).
caceae families found that exposure to different antibiotics The hypothesis that wild species are intrinsically more
(penicillin, sulfadiazine, and tetracycline) at concentrations sensitive to PPPs than crop species has been tested (Christl

13
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 57

Table 5  Sensitivity of crop and Group or variable Seed germination Growth (elongation) Growth (bio-
wild species to antibiotics based mass)
on quotients (Q) calculated
from reference points (RF) of EC50 EC10 EC50 EC10 EC50 EC10
toxicity data (ECx) on plant
growth. Quotients above 1 CROP n 20 21 58 27 14 120
indicated that wild species RPgeo(a) mg/kg 42.36 3.19 110.39 15.58 8.56 3.08
were more sensitive than crop RPmin(b) mg/kg 1.21 0.012 4.12 0.213 0.14 0.06
species, while quotients below 1
indicated the opposite WILD n 0 1 3 1 1 3
RPgeo(a) mg/kg – – 107.70 – – 3.30
RPmin(b) mg/kg – – 0.25 – – 0.25
QUOTIENT Qgeo(c) – – 1.6 – – 0.9
Qmin(d) – – 16.36 – – 0.21

(a) RPgeo, geometric mean and can protect 50% of the species
(b) RPmin, hazardous concentration for 5% of the population (HC5) or ­5th percentile of the species sensi-
tivity distribution (SSD), corresponding to protection of 95% of the species
(c) Qgeo, Quotient value based on geometric mean values
(d) Qmin, Quotient value based on 5th percentile of the species sensitivity distribution (SSD) values

et al. 2019). After conducting a critical review of available florfenicol (phenicol) and tylosin (macrolide). Liu et al
data on wild and crop species and statistically analysing the (2009a) also found lower toxicity for tylosin (macrolide),
differences in their intrinsic sensitivity to such products, chlortetracycline and tetracycline than for trimethoprim
those authors found no consistent differences between the (diaminopiridine), sulfamethoxazole and sulfamethazine
two groups of plants. In fact, crop species were found to be (sulfonamide) in two plant species, Oryza sativa (Poaceae)
slightly more sensitive than wild plant species. Our review and Cucumis sativus (Cucurbitaceae).
used a similar approach to analyse the effects of antibiot- Comparison of plant families did not reveal sig-
ics on crop and wild species, but it could not arrive at a nificant results except for EC50 elongation values,
clear. One major constraint was the lack of published data which showed the following trend in sensitivity: Bras-
on wild plant species. ERAs of veterinary medicines can sicaceae > Liliaceae > Apiaceae, Fabaceae, Solan-
contain additional sources of data, but we were unable to aceae > Poaceae > Cucurbitaceae > Asteraceae. Similar
access such data. Moreover, a majority of pharmaceutical to our results, Liu et al (2009b) reported Oryza sativa
veterinary medicine products (> 95%) are considered to have (Poaceae) to be more sensitive to triclosan than Cucumis
limited environmental release, resulting in low tier (Phase I) sativus (Cucurbitaceae). Conversely, Tasho et al. (2020)
risk assessments that do not require the analysis of ecotoxi- showed Daucus carota (Apiaceae) to be the most sensitive
cological data (Fabrega and Carapeto 2020). to sulfadiazine, oxytetracycline and streptomycin, followed
by Lactuca sativa (Asteraceae) and Capsicum annuum
Plant Families and Antibiotic Class Sensitivity (Solanaceae). Litskas et al. (2019) evaluated the effect of
doxycycline at concentrations up to 110 mg/kg on five
Data did show significant differences among classes of anti- plant species: Pisum sativum (Fabaceae), Cucurbita pepo
biotics based on the EC50 and EC10 values of elongation (Cucurbitaceae), Solanum lycopersicum (Solanaceae),
growth and biomass growth (Fig. 4). However, such data Phaseolus vulgaris (Fabaceae) and Zea mays (Poaceae).
often came from different antibiotic classes, and data for a That study reported Solanum lycopersicum (Solanaceae) to
given class were often lacking (n < 3). Nevertheless, analysis be the only sensitive plant species. Species differences in
based on elongation showed that phenicol was the most toxic sensitivity to antibiotics depend on the antibiotic assayed
class of antibiotics, whereas macrolides and tetracyclines (Richter et al. 2016; Parente et al., 2019), so more research
were the least toxic. Analysis based on biomass was similar is needed to explore such differences.
to that based on elongation, except for tetracyclines, due to Even though we were unable to arrive at a clear con-
the lack of data for this antibiotic class. Previous studies clusion in this review, the findings can contribute to the
have reported variability in antibiotic toxicity to plants. For current state of knowledge concerning the environmental
example, Richter et al. (2016) observed that six plant spe- risk assessment of antibiotics. Further work must be con-
cies (Allium cepa, Avena sativa, Brassica napus, Synapsis ducted to gain a better understanding of the effects of tox-
alba and Solanum lycopersicum and Phaseolus vulgaris) icity on wild plants, antibiotic classes and plant families.
differed by approximately two orders of magnitude between This is especially important for preserving biodiversity and

13
58 Archives of Environmental Contamination and Toxicology (2022) 82:48–61

Fig. 4  Differences in toxicity among classes of antibiotics: a elongation EC10 (mg/kg), b elongation EC50 (mg/kg), c biomass

enhancing natural capital in the EU, given the requirements taxonomic groups and antibiotic classes with sufficient data,
of the European Green Deal (European Commission 2019). wild species were more sensitive to antibiotics than crop spe-
cies in terms of elongation growth, yet less sensitive in terms
of biomass growth. Previous studies on potential sensitiv-
ity differences between wild and crop species have revealed
Conclusions similar results, so further work is required to explore such
differences. Understanding these differences is important for
Owing to the lack of data on wild species, we were una- ascertaining whether the current approach of basing ERAs
ble to evaluate the differences in sensitivity to antibiotics solely on crop plants is sufficient to protect plant biodiversity
between crop and wild plant species. We found that for plant from antibiotic contamination.

13
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 59

Among the different classes of antibiotics evaluated, Environ Sci Pollut Res 22:2350–2355. https://​doi.​org/​10.​1007/​
phenicol was the most toxic class of antibiotics, whereas s11356-​014-​3637-6
Bellino A, Lofrano G, Carotenuto M, Libralato G, Baldantoni D (2018)
macrolides and tetracyclines were the least toxic. However, Antibiotic effects on seed germination and root development
no significant results were found in the comparison across of tomato (Solanum lycopersicum L.). Ecotoxicol Environ Saf
plant families, except for elongation. We found that Bras- 148:135–141. https://​doi.​org/​10.​1016/j.​ecoenv.​2017.​10.​006
sicaceae and Liliaceae were the most sensitive families, Boutin VPC, Strandberg B, Carpenter D, Mathiassen SK, Thomas PJ
(2014) Herbicide impact on non-target plant reproduction: what
whereas Asteraceae was the least sensitive. Further studies are the toxicological and ecological implications? Environ Pollut
should verify and extend our findings. 185:295–306. https://​doi.​org/​10.​1016/j.​envpol.​2013.​10.​009
More data on plant sensitivity to antibiotics, including Carter LJ, Harris E, Williams M, Ryan JJ, Kookana RS, Boxall ABA
the sensitivity of wild species, may become available when (2014) Fate and uptake of pharmaceuticals in soil-plant systems.
J Agric Food Chem 62(4):816–825. https://​doi.​org/​10.​1021/​jf404​
the new Regulation (EU) 2019/6 comes into force in Janu- 282y
ary 2022, which will allow the publication of toxicity data Carvalho PN, Basto MCP, Almeida CMR et al (2014) A review of
for veterinary medicinal products. Currently those submit- plant–pharmaceutical interactions: from uptake and effects in
ting environmental risk assessments for veterinary medici- crop plants to phytoremediation in constructed wetlands. Envi-
ron Sci Pollut Res 21:11729–11763. https://​doi.​org/​10.​1007/​
nal products are not required to publish such data (Oelkers s11356-​014-​2550-3
2021), which in fact remain the property of the applicants Christl H, Morilla J, Hoen T, Zumkier U (2019) Comparative assess-
and cannot be used without corresponding commercial or ment of the intrinsic sensitivity of crop species and wild plant
confidentiality agreements (de la Casa-Resino et al. 2021). species to plant protection products and their active substances
and potential implications for the risk assessment: a literature
review. Integr Environ Assess Manag 15:176–189. https://​doi.​
Author contributions MC and AT designed and conceptualised the org/​10.​1002/​ieam.​4115
study. MC collected the data and performed the systematic review. AT Clemente AS, Müller JV, Almeida E, Costa CA, Dias SL, Brehm JM,
analysed the data and wrote the manuscript. AR facilitated the curation Rebelo R, Martins-Loução MA (2017) What can routine germina-
of data and provided software resources. All authors read and approved tion tests in seed banks tell us about the germination ecology of
the final manuscript. endemic and protected species? Botany 95(7):673–684. https://​
doi.​org/​10.​1139/​cjb-​2017-​0003
Funding This study was supported by the Spanish Ministry of Science Cycon M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil
and Innovation (RTI208_095586_B_C21). environment—degradation and their impact on microbial activity
and diversity. Front Microbiol 10:338
Data Availability We are unable to provide access to the datasets ana- de la Casa-Resino I, Haro Castuera A, Casimiro Elena R, Rubio
lysed in this study since many of them are not publicly available and Montejano C,Carapeto García R (2021) European legislation for
have been published in journals without open access. veterinary medicines: Would a monograph system improve the
environmental risk assessment? Integr Environ Assess Manag.
https://​doi.​org/​10.​1002/​ieam.​4431
Declarations Dipshika N, Mehta P (2018) Effect of veterinary antibiotics on the seed
germination of indica rice varieties. Ann Plant Sci 7(6):2321–
Conflict of interest The authors declare no conflicts of interest. 2327. https://​doi.​org/​10.​21746/​aps.​2018.7.​6.4
Dolliver H, Gupta S, Noll S (2008) Antibiotic degradation during
Open Access This article is licensed under a Creative Commons Attri- manure composting. J Environ Qual 37(3):1245–1253. https://​
bution 4.0 International License, which permits use, sharing, adapta- doi.​org/​10.​2134/​jeq20​07.​0399
tion, distribution and reproduction in any medium or format, as long EMA European Medicines Agency (2019) European Surveillance of
as you give appropriate credit to the original author(s) and the source, Veterinary Antimicrobial Consumption, 2019.‘Sales of veterinary
provide a link to the Creative Commons licence, and indicate if changes antimicrobial agents in 31 European countries in 2017’. Ninth
were made. The images or other third party material in this article are ESVAC report. (EMA/294674/2019)
included in the article's Creative Commons licence, unless indicated Elezz AA, Easa A, Atia F, Ahmed T (2019) The potential impact data
otherwise in a credit line to the material. If material is not included in of Tylosin and Enrofloxacin veterinary antibiotics on germination
the article's Creative Commons licence and your intended use is not and accumulation in barley seed as a forage crop and good dietary
permitted by statutory regulation or exceeds the permitted use, you will sources using LC/MS-MS. Data Brief 25:104326. https://​doi.​org/​
need to obtain permission directly from the copyright holder. To view a 10.​1016/j.​dib.​2019.​104326
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. Eluk D, Nagel OG, Zimmermann J, Molina MP, Althaus RL (2016)
Effect of antibiotics on the germination and root elongation of
argentine intensive crops. Int J Environ Res 10(4):471–480.
https://​doi.​org/​10.​22059/​IJER.​2016.​59521
References European Commission (2019) Communication from the commission
to the European parliament, the European council, the council,
Arts GHP, Dollinger M, Kohlschmid E, Maltby L, Ochoa-Acuña H, the European economic and social committee and the committee
Poulsen V (2015) An ecosystem services approach to pesticide of the regions. The European Green Deal. Brussels, 11.12.2019 ,
risk assessment and risk management of non-target terrestrial COM/2019/640 final
plants: recommendations from a SETAC Europe workshop. European Food Safety Authority (2010) Scientific Opinion on the
development of specific protection goal options for environmen-
tal risk assessment of pesticides, in particular in relation to the

13
60 Archives of Environmental Contamination and Toxicology (2022) 82:48–61

revision of the Guidance Documents on Aquatic and Terrestrial frommanure-amended cropland. J Environ Qual 38:1719–1729.
Ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002. https://​doi.​org/​10.​2134/​jeq20​08.​0365
EFSA Journal, 8(10):1821. https://​doi.​org/​10.​2903/j.​efsa.​2010.​ Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005) Anti-
1821 biotic uptake by plants fromsoil fertilized with animal manure.
European Food Safety Authority (2014) Scientific Opinion addressing J Environ Qual 34:2082–2085. https://​doi.​org/​10.​2134/​jeq20​05.​
the state of the science on risk assessment of plant protection 0026
products for non-target terrestrial plants. EFSA J 12(7):3800. Kumar RR, Lee JT, Cho JY (2012) Fate, occurrence, and toxicity of vet-
https://​doi.​org/​10.​2903/j.​efsa.​2014.​3800 erinary antibiotics in environment. J Korean Soc Appl Biol Chem
European Food Safety Authority Scientific Committee (2016) Guid- 55:701–709. https://​doi.​org/​10.​1007/​s13765-​012-​2220-4
ance to develop specific protection goals options for environ- Lenth R, Singmann H, Love J, Buerkner P, Herve, M (2019) Package
mental risk assessment at EFSA in relation to biodiversity and "emmeans. https://​doi.​org/​10.​1080/​00031​305.​1980.​10483​031
ecosystem services. EFSA J 14(6):4499. https://d​ oi.o​ rg/1​ 0.2​ 903/j.​ Lindstrom M, Bates D (1988) Newton—Raphson and EM algorithms
efsa.​2016.​4499 for linear mixed-effects models for repeated-measures data. J Am
Eurostat (2017) Archive: Main annual crop statistics. Statistics Stat Assoc 83(404):1014–1022. https://​doi.​org/​10.​1080/​01621​459.​
Explained. URL https://​ec.​europa.​eu/​euros​t at/​stati​stics-​expla​ 1988.​10478​693
ined/​index.​php?​title=​Archi​ve:​Main_​annual_​crop_​stati​stics& Litskas VD, Karamanlis XN, Prousali SP, Koveos DS (2019) The xenobi-
oldid=332968#Main_statistical_findings (accessed 2.25.21) otic doxycycline affects nitrogen transformations in soil and impacts
Fabrega J, Carapeto R (2020) Regulatory review of the environmental earthworms and cultivated plants. J Environ Sci Health Part A
risk assessment of veterinary medicinal products in the Euro- 54(14):1441–1447. https://​doi.​org/​10.​1080/​10934​529.​2019.​16553​68
pean Union, with particular focus on the centralised authorisa- Liu F, Guang-Guo YG, Ran T, Jian-Liang Z, Ji-Feng Y, Lan-Feng Z
tion procedure. Environ Sci Eur 32:99. https://​doi.​org/​10.​1186/​ (2009a) Effects of six selected antibiotics on plant growth and soil
s12302-​020-​00374-x microbial and enzymatic activities. Environ Pollut 157:1636–1642.
Furtula V, Stephenson GL, Olaveson KM, Chambers PA (2012) Effects https://​doi.​org/​10.​1016/j.​envpol.​2008.​12.​021
of the veterinary pharmaceutical salinomycin and its formula- Liu F, Ying GG, Yang LH, Zhou QX (2009b) Terrestrial ecotoxicologi-
tion on the plant Brassica rapa. Arch Environ Contam Toxicol cal effects of the antimicrobial agent triclosan. Ecotoxicol Environ
63(4):513–522. https://​doi.​org/​10.​1007/​s00244-​012-​9807-y Safety 72(1):86–92. https://​doi.​org/​10.​1016/j.​ecoenv.​2008.​06.​009
Ghava K, Rathod MC, Dhale DA (2015) Effect of antibiotics on seed Llor C, Bjerrum L (2014) Antimicrobial resistance: risk associated with
germination and root elongation of wheat. Int J Curr Microbiol antibiotic overuse and initiatives to reduce the problem. Ther Adv
App Sci 4(1):516–527 Drug Saf 5(6):229–241. https://​doi.​org/​10.​1177/​20420​98614​554919
Grenni P, Ancona V, Caracciolo AB (2018) Ecological effects of anti- Luo Y, Liang J, Zeng G et al (2019b) Responses of seeds of typical Bras-
biotics on natural ecosystems: a review. Microchem J 136:25–39. sica crops to tetracycline stress: sensitivity difference and source
https://​doi.​org/​10.​1016/j.​microc.​2017.​02.​006 analysis. Ecotoxicol Environ Saf 184:109597. https://​doi.​org/​10.​
Grote M, Schwake-Anduschus C, Michel R, Stevens H, Heyser W, 1016/j.​ecoenv.​2019.​109597
Langenkämper G, Betsche T, Freitaget M (2007) Incorporation Luo Y, Liang J, Zeng G, Li X, Chen M, Jiang L, Xing W, Tang N, Fang
of veterinary antibiotics into crops from manured soil. Landbau- Y, Chen X (2019) Evaluation of tetracycline phytotoxicity by seed
forschung Völkenrode 57:25–32 germination stage and radicle elongation stage tests: a comparison
Gómez D (2008) Pastos del Pirineo: Breve descripción ecológica y of two typical methods for analysis. Environ Pollut 251:257–263.
florística. In: Fillat F, García-González R, Gómez Garcia D, Reiné https://​doi.​org/​10.​1016/j.​envpol.​2019.​05.​005
R. (Eds.) Pastos del Pirineo. Madrid, Spain, pp. 111–140. ISBN Menezes-Oliveira V, Loureiro S, Amorim MJB et al (2018) Hazard
978–84–00–08614–5. http://​hdl.​handle.​net/​10261/​100492 assessment of the veterinary pharmaceuticals monensin and nicar-
Hendrickson JR, Sanderson M (2017) Perennial-Based agricultural bazin using a soil test battery. Environ Toxicol Chem 37(12):3145–
systems and livestock impact on soil and ecological services. In: 3153. https://​doi.​org/​10.​1002/​etc.​4265
Al-Kaisi MM, Lowery B (eds) Soil Health and Intensification of Migliore L, Brambilla G, Cozzolino S, Gaudio L (1995) Effect on plants
Agroecosytems. Academic Press, USA, pp 151–171. https://​doi.​ of sulphadimethoxine used in intensive farming (Panicum milia-
org/​10.​1016/​B978-0-​12-​805317-​1.​00007-5 ceum, Pisum sativum and Zea mays). Agr Ecosyst Environ 52:103–
Hillis DG, Antunes P, Sibley PK, Klironomos JN, Solomon K (2008) 110. https://​doi.​org/​10.​1016/​0167-​8809(94)​00549-T
Structural responses of Daucus carota root-organ cultures and Migliore L, Cozzolino S, Fiori M (2003) Phytotoxicity to and uptake of
the arbuscular mycorrhizal fungus, Glomus intraradices, to 12 enrofloxacin in crop plants. Chemosphere 52(7):1233–1244. https://​
pharmaceuticals. Chemosphere 73:344–352. https://​doi.​org/​10.​ doi.​org/​10.​1016/​S0045-​6535(03)​00272-8
1016/j.​chemo​sphere.​2008.​05.​063 Minden V, Deloy A, Volkert AM, Leonhardt SD, Pufal G (2017) Antibi-
Hillis DG, Fletcher J, Solomo KR et al (2011) Effects of ten antibiotics otics impact plant traits, even at small concentrations. AoB Plants.
on seed germination and root elongation in three plant species. https://​doi.​org/​10.​1093/​aobpla/​plx010
Arch Environ Contam Toxicol 60:220–232. https://​doi.​org/​10.​ Oelkers K (2021) Transparency in product authorisation – The han-
1007/​s00244-​010-​9624-0 dling of commercially confidential information in environmental
Jin C, Chen Q, Sun R, Zhou Q, Liu J (2009) Eco-toxic effects of sul- risk assessments of industrial chemicals, biocidal products, plant
fadiazine sodium, sulfamonomethoxine sodium and enrofloxacin protection products and pharmaceuticals. Sustain Chem Pharm
o wheat. Chin Cabbage Tomato Ecotoxicol 18(7):878–885. https://​ 20:100399. https://​doi.​org/​10.​1016/j.​scp.​2021.​100399
doi.​org/​10.​1007/​s10646-​009-​0349-7 Olszyk D, Pfleeger T, Lee E, Burdick C, King G, Plocher M, Kern J
Kaluza BF, Wallace H, Keller A, Heard TA, Jeffers B, Drescher N, (2008) Selecting and evaluating native plants for region-specific
Bluthgen N, Leonhardt SD (2017) Generalist social bees maxi- phytotoxicity testing. Integr Environ Assess Manag 4:105–117.
mize diversity intake in plant species-rich and resource-abundant https://​doi.​org/​10.​1897/​IEAM_​2007-​044
environments. Ecosphere 8(3):e01758. https://​doi.​org/​10.​1002/​ Orzoł A, Piotrowicz-Cieślak AI (2017) Levofloxacin is phytotoxic and
ecs2.​1758 modifies the protein profile of lupin seedlings. Environ Sci Pollut Res
Kuchta SL, Cessna AJ, Elliott JA, Peru KM, Headley JV (2009) 24(28):22226–22240. https://​doi.​org/​10.​1007/​s11356-​017-​9845-0
Transport of lincomycin to surface and ground water

13
Archives of Environmental Contamination and Toxicology (2022) 82:48–61 61

Pan M, Chu LM (2016) Phytotoxicity of veterinary antibiotics to seed Rydzyński D, Piotrowicz-Cieślak AI, Grajek H (2017) Instability of chlo-
germination and root elongation of crops. Ecotoxicol Environ Saf rophyll in yellow lupin seedlings grown in soil contaminated with
126:228–237. https://​doi.​org/​10.​1016/j.​ecoenv.​2015.​12.​027 ciprofloxacin and tetracycline. Chemosphere 184:62–73. https://​doi.​
Pannu MW, Toor GS, Wilson P (2012) Toxicity and bioaccumulation org/​10.​1016/j.​chemo​sphere.​2017.​05.​147
of biosolids-borne triclosan in food crops. Environ Toxicol Chem Sidhu H, O’Connor G, Kruse J (2019) Plant toxicity and accumulation of
31(9):2130–2137. https://​doi.​org/​10.​1002/​etc.​1930 biosolids-borne ciprofloxacin and azithromycin. Sci Total Environ
Parente CET, Sierra J, Martì E (2018) Ecotoxicity and biodegradability 648:1219–1226. https://​doi.​org/​10.​1016/j.​scito​tenv.​2018.​08.​218
of oxytetracycline and ciprofloxacin on terrestrial and aquatic media. Tasho RS, Ryu SH, Cho JY (2020) Effect of Sulfadimethoxine, Oxy-
Orbital Electron J. Chem 10(4):262–271. https://​doi.​org/​10.​17807/​ tetracycline, and Streptomycin antibiotics in three types of crop
orbit​al.​v10i4.​1063 plants—root, leafy, and fruit. Appl Sci 10:1111. https://​doi.​org/​10.​
Peters MDJ, Godfrey C, McInerney P, Munn Z, Tricco AC, Khalil H 3390/​app10​031111
(2020) Scoping Reviews. In: Aromataris. E, Munn Z (Editors). Timmerer U, Lehmann L, Schnug E, Bloem E (2020) Toxic effects of
Joanna Briggs Institute Manual for Evidence Synthesis. https://​ single antibiotics and antibiotics in combination on germination and
synth​esism​anual.​jbi.​global. https://​doi.​org/​10.​46658/​JBIMES-​20-​12 growth of Sinapis alba L. Plants 9(1):E107. https://​doi.​org/​10.​3390/​
Pino MR, Muñiz S, Val J et al (2016) Phytotoxicity of 15 common plant​s9010​107
pharmaceuticals on the germination of Lactuca sativa and photo- Van Vlaardingen P, Traas TP, Wintersen A, Aldenberg T (2004) ETX2.0.
synthesis of Chlamydomonas reinhardtii. Environ Sci Pollut Res A program to calculate hazardous concentrations and fraction
23:22530–22541. https://​doi.​org/​10.​1007/​s11356-​016-​7446-y affected, based on normally distributed toxicity data. RIVM Report
Polunin O (1977) Flowers of Europe: a field guide. Oxford University no. 601501028/2004, 68 pp.
Press, London Vickery JA, Feber RE, Fuller RJ (2009) Arable field margins managed
Rede D, Santos L, Ramos S, Oliva-Teles F, Antão C, Sousa SR, Delerue- for biodiversity conservation: a review of food resource provision
Matos C (2019) Individual and mixture toxicity evaluation of three for farmland birds. Agr Ecosyst Environ 133(1–2):1–13. https://​doi.​
pharmaceuticals to the germination and growth of Lactuca sativa org/​10.​1016/j.​agee.​2009.​05.​012
seeds. Sci Total Environ 673:102–109. https://​doi.​org/​10.​1016/j.​ Wang R, Wang J, Zhu L et al (2019) Growth inhibiting effects of four
scito​tenv.​2019.​03.​432 antibiotics on Cucumber, Rape and Chinese cabbage. Bull Envi-
Riaz L, Mahmood T, Coyne MS, Khalid AL, Rashid A, Hayat MT, ron Contam Toxicol 103:187–192. https://​doi.​org/​10.​1007/​
Gulzar A, Amjad M (2017) Physiological and antioxidant response s00128-​019-​02582-5
of wheat (Triticum aestivum) seedlings to fluoroquinolone antibi- Wieczerzak M, Kudłak B, Namieśnik J (2018) Impact of selected drugs
otics. Chemosphere 177:250–257. https://​doi.​org/​10.​1016/j.​chemo​ and their binary mixtures on the germination of Sorghum bicolor
sphere.​2017.​03.​033 (sorgo) seeds. Environ Sci Pollut Res Int 25(19):18717–18727.
Richter E, Berkner S, Ebert I, Förster B, Graf N, Herrchen M, Kühnen https://​doi.​org/​10.​1007/​s11356-​018-​2049-4
U, Römbke J, Simon M (2016) Results of extended plant tests using Xie X, Zhou Q, Lin D, Guo J, Bao Y (2011) Toxic effect of tetracy-
more realistic exposure scenarios for improving environmental risk cline exposure on growth, antioxidative and genetic indices of
assessment of veterinary pharmaceuticals. Environ Sci Eur 28(1):22. wheat (Triticum aestivum L.). Environ Sci Pollut Res 18:566–575.
https://​doi.​org/​10.​1186/​s12302-​016-​0089-2 https://​doi.​org/​10.​1007/​s11356-​010-​0398-8

13