Vol.:(0123456789)
1 3
En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
h ps://doi.o g/10.1007/s11356-023-30182-8
RESEARCH ARTICLE
Po en ial oxici y o Schisand a chinensis owa e en i onmen : acu e
oxici y es s wi hwa e c us aceans
JanaValíčko á1 · Š ěpánZezulka2· EliškaMa šálko á2· Jose Ko lík1· Blahosla Ma šálek2· RadkaOpa řilo á3
Recei ed: 12 June 2023 / Accep ed: 26 Sep embe 2023 / Published online: 14 Oc obe 2023
© The Au ho (s) 2023
Abs ac
F ui s o Schisand a chinensis, an Eas Asian liana plan , a e cu en ly mo e and mo e used o p oduce nu ien supplemen s
ha posi i ely a ec human heal h due o he con en o a ious seconda y me aboli es. On he o he hand, hese subs ances
because o hei bioac i i y can cause possible allelopa hic o oxic e ec s conce ning o he o ganisms (algae, plan s, ani-
mals). Bu he eco oxicological p ope ies o S. chinensis ou side i s a ea o o igin ha e ye o be su icien ly e i ied. Two
c us aceans, Daphnia magna and Thamnocephalus pla yu us, we e selec ed as model aqua ic o ganisms o es he po en ial
impac o S. chinensis ac i e compounds on he aqua ic en i onmen . C ude wa e ex ac om S. chinensis ui s, simula -
ing he na u al leakage o ac i e subs ances in wa e , was es ed in ea men s om 0.0045 o 45 mg/L (acco ding o he
con en o schisand in as he domina ing lignan). E ec i e concen a ion (EC50) causing 50% le hal e ec o D. magna was
es ablished o 0.0448 mg/L a e 24 h and 0.0152 mg/L a e 48 h. EC50 o T. pla yu us eached 0.4572 mg/L a e 24 h, i.e.
mo e han en imes highe han o D. magna. This s udy showed ha he po en ial en i onmen ally ele an concen a ions
o S. chinensis bioac i e compounds could ep esen a se e e isk o aqua ic ecosys ems.
Keywo ds Adap ogen· Lignan· Schisand in· Zooplank on· Acu e oxici y
In oduc ion
Schisand a chinensis (known as magnolia ine o
wuweizi) is a liana used as a na u al he bal medicine o
ea many human diseases. This plan g ows wild and is
cul i a ed in he Fa Eas , like no heas e n China, Japan
and Ko ea (Panossian and Wikman 2008). A wo k by Li
Shih-Chen, “Pên T'shao Kang Mu”, on Chinese medicine
published in 1596, con ains he i s w i en men ion o
he Schisand a species (Szopa e al. 2017). Howe e , he
seeds o Schisand a plan s we e also disco e ed in Eu ope,
as con i med (Teodo idis 2005) in a mo phological and
ana omical s udy o he holo ype o S. mo a ica om
Ša o and addi ionally seeds o he same species om he
Cheb, Sokolo and Mos Basins (Czech Republic) whe e
he assignmen o he seeds o he genus Schisand a MICH
was con i med.
As con i med by many s udies, S. chinensis is a p om-
ising plan wi h a posi i e e ec on human heal h and is
classi ied as an adap ogen. Hancke e al. (1999) desc ibe
he p o en posi i e impac o S. chinensis on human heal h
and ocus on an i-hepa o oxic, an ioxidan and an i- umou
e ec s and on imp o ing physical pe o mance and e ec s
on he cen al ne ous sys em. Ma e al. (2023) ha e shown
in he s udy ha S. chinensis has p omising clinical e i-
cacy in ea ing diabe es melli us as one o he mos com-
mon diseases in ou cu en ci ilisa ion. S. chinensis and
i s compounds a ec he endoc ine sys em, e.g. co isol
and es os e one le els, and he me abolism o lipids and
muscles (Leis e al. 2020). Ano he ad an age o S. chin-
ensis and i s de i a i es is ha i can be a sou ce o na u al
an ioxidan s (Wang and Wang 2013).
Responsible Edi o : Lo i Aleya
* Jana Valíčko á
xc alicko [email p o ec ed]
1 Ins i u e o Chemis y andTechnology o En i onmen al
P o ec ion, Facul y o Chemis y, B no Uni e si y
o Technology, Pu kyňo a 464/118, 61200B no,
CzechRepublic
2 Depa men o Expe imen al Phycology andEco oxicology,
Ins i u e o Bo any, Czech Academy o Sciences, Lidická
25/27, 60200B no, CzechRepublic
3 Depa men o Chemical D ugs, Facul y o Pha macy,
Masa yk Uni e si y, Palackého řída 1946/1, 61200B no,
CzechRepublic
112626 En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
1 3
Plan s om Schisand aceae amily con ain many pha -
macologically usable subs ances including schisand in,
deoxyschisand in, gomisin A, gomisin O and gamma-
schisand in (Smejkal e al. 2010; Wang e al. 2018). Mos
o he bioac i e compounds can be ound in ui s and
seeds, lowe con en s a e in lea es and s em (Lee e al.
2022). The eal con en o schisand in as he dominan
compound and o he lignans ound in he ui s o mag-
nolia ine is highly a iable. I depends on many ac-
o s, such as he me hod and place o cul i a ion o he
ui ipening s age. Acco ding o he li e a u e sou ces,
he con en o schisand in can be om 2.1 mg/g (Kohda
e al. 2012) o 5.0 mg/g o d y ui weigh (Slanina e al.
1997).
G owing demands o he p oduc ion o ood supple-
men s con aining bioac i e subs ances om his plan
p omo e i s a ming in la ge a eas ou side i s place o
o igin. I e okes a ques ion i S. chinensis can in luence
he en i onmen in such si es. Schisand in and o he
ac i e compounds om S. chinensis belong o lignans,
seconda y plan me aboli es known as allelochemicals
(Cos as-Gil e al. 2018; Sca o e al. 2019a; Sca o e al.
2019b) which can be oxic no only o plan s bu e en
o o he o ganisms in he ecosys em. Cu en ly, he da a
abou he allelopa hic e ec o schisand in a e sca ce.
S. chinensis g ows wild in Eas Asia, bu in some
a eas, i is a med. Fo example, he a e age size o he
a mland o S. chinensis cul i a ion in Sou h Ko ea was
0.5 ha pe a m (Choi e al. 2015) and he scale o cul i-
a ion a eas is s ill ising. In Eu opean a ea, S. chinensis
is o en plan ed only as an indi idual plan nea by ga den
ponds bu because o he inc easing inqui y on he ui s,
i is conside ed i s a ming on la ge a eas. Howe e , any
s udy does no add ess he possible impac o S. chinensis
a ming on he su ounding en i onmen .
Delica e wa e ecosys ems can be a ec ed by he
e ec s o lignans leaking om ui s acciden ally all-
ing in o he wa e body as p o ed on Lemna mino (Val-
icko a e al. 2023). The e ec s o bioac i e subs ances
om Schisand a chinensis on aqua ic animals a e insu -
icien ly esea ched and his lack o eco oxicological da a
should be add essed.
An in eg al pa o aqua ic ecosys ems and ood webs
is also in e eb a e zooplank on species like Daphnia
magna and Thamnocephalus pla yu us. Because o hei
high sensi i i y o en i onmen al pollu ion, hese species
a e included in s anda dised acu e oxici y es s (Ke -
be o a e al. 2022; Szkla ek e al. 2022).
This s udy a ge s o assess he possible acu e oxic-
i y o aqueous ex ac om S. chinensis ui s o indica-
o zooplank on species Daphnia magna and Thamno-
cephalus pla yu us o enhance he knowledge abou he
possible eco oxicological isks o S. chinensis a ming
ou side i s a eas o o igin.
Ma e ials andme hods
Plan ma e ial andex ac ion
The ipe ui s o S. chinensis we e ha es ed om a
plan g own in he a ea o V aco , Czech Republic. The
whole ui s (including seeds) we e eed om impu i-
ies, de ached om he s alks and le o d y na u ally
in he ai . The a e age po ion o hei d y mass was
es ablished a 20% o he esh weigh .
C ude aqueous ex ac om S. chinensis ui s (SCE)
was ob ained by a Soxhle ex ac ion wi h dis illed wa e
as desc ibed in Valicko a e al. (2023). I s composi ion
was analysed using high-pe o mance liquid ch oma og-
aphy. HPLC (Agilen 1100 Se ies, Agilen Technolo-
gies, USA) was equipped wi h C18 column (Kine ex®
2.6 μm C18 100Å, LC Column 150 × 2.1 mm). Mobile
phases we e MilliQ wa e and me hanol (70 o 100 %).
Diode a ay de ec o was se o 225 nm. Calib a ion was
done using ex e nal s anda d (CAS 7432-28-2, pu i y ≥
98%, Me ck). The con en o he domina ing compound
schisand in was de e mined o be 45 mg/L.
Acu e oxici y es s
Daph oxki F® and Thamno oxki F® (Mic obio es s, Bel-
gium) we e used o es he acu e oxici y o SCE o esh-
wa e c us aceans Daphnia magna and Thamnocephalus
pla yu us. Acco ding o p oduce ’s guides, es ing s ages
o bo h o ganisms (D. magna ephippia and T. pla yu us cys s
included in he ki s) we e e-ac i a ed in a s anda d eshwa-
e and cul i a ed on Pe i dishes unde con inuous ligh o
ob aining a popula ion o adul animals (D. magna o 72 h,
T. pla yu us o 20–22 h).
The SCE was dilu ed wi h s anda d eshwa e o he
concen a ions 0.0045 mg/L, 0.009 mg/L, 0.045 mg/L,
0.09 mg/L, 0.45 mg/L, 0.9 mg/L, 4.5 mg/L and 9 mg/L.
Undilu ed SCE (45 mg/L) was included in bo h es s
oo. Tes ed solu ions and animals we e ans e ed o
es pla es (4 wells pe each ea men wi h 5 indi iduals
pe well o D. magna; 3 wells wi h 10 indi iduals pe
well o T. pla yu us) and he cul i a ion con inued in he
da kness and con olled empe a u e (D. magna 20 ± 2
°C, T. pla yu us 25 °C). Acco ding o p oduce ’s guides
and ISO s anda ds (ISO 6341: 2012; ISO 14380: 2011),
he mobili y o D. magna was e alua ed a e 24 and 48
h and he mo ali y o T. pla yu us was assessed a e 24
h. The es s we e un in iplica es.
112627En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
1 3
S a is ics
The e ec o SCE on bo h species was e alua ed as he pe -
cen age o immobilised/dead indi iduals in each ea men
acco ding o he ollowing equa ion:
whe e NL is he numbe o li ing indi iduals and NT is he
numbe o o al indi iduals in each ea men .
The so wa e STATISTICA (S a So Inc.®) was used o
e alua e he ob ained esul s s a is ically. The signi icance o
he di e ences in he a e age alues be ween he ea men s
was assessed by he non-pa ame ic K uskal-Wallis es and
mul iple compa ison me hod (P < 0.05). The e ec i e con-
cen a ions EC50/LC50 o bo h species we e e alua ed using
G aphPad P ism® so wa e (Do ma ics) by a dose- esponse
cu e and non-linea eg ession analysis.
Resul s
Acu e oxici y oDaphnia magna
In acco dance wi h he s anda ds ISO 6341: 2012 and
OECD Guidelines Tes No. 202, daphnids we e exposed
o SCE in an acu e oxici y es . The numbe o dead and
immobilised indi iduals was assessed a e 24 and 48 h
Inhibi ion
(%)=
(
1−
(
NL∕NT
))
×100
%
(Fig.1). The lowes es ed ea men (0.0045 mg/L SCE)
did no in luence he i ali y o daphnids ei he a e 24 h
o 48 h as compa ed o he un ea ed con ol. The numbe
o su i ing indi iduals dec eased in 0.009 mg/L SCE
ea men a e 24 h by 25% and a e 48 h by 50%. Highe
ea men s o 0.045 and 0.09 mg/L SCE caused mo e han
50% mo ali y on bo h days. F om 0.45 mg/L SCE, all
ea men s exhibi ed 100% mo ali y. Undilu ed SCE 45
mg/L caused e en he des uc ion o he daphnid’s bodies.
The e ec i e concen a ion (EC50) o Daphnia magna
was es ablished a 0.0448 mg/L a e 24 h and 0.0152 mg/L
a e 48 h (Table1), showing high acu e oxici y o SCE o
his in e eb a e.
Acu e oxici y oThamnocephalus pla yu us
Following he ISO s anda d 14380: 2011, T. pla yu us
la ae we e exposed o SCE in an acu e 24 h oxici y es
(Fig.2). The lowes es ed ea men s (0.0045 and 0.009
mg/L SCE) did no in luence he i ali y o T. pla yu us
la ae a e 24 h as compa ed o un ea ed con ol. T ea -
men s 0.045, 0.09 and 0.45 mg/L SCE caused a dec ease
o su i ing indi iduals’ numbe by 3, 10 and 36%,
espec i ely. In highe ea men s (0.9 o 45 mg/L SCE),
he mo ali y eached 100%.
The e ec i e concen a ion (EC50) o T. pla yu us was
es ablished a 0.4572 mg/L a e 24 h (Table1).
Fig. 1 Acu e oxici y es o SCE on Daphnia magna a e 24 and 48
h. Da a poin s ep esen he mean o e wel e eplica es, and s anda d
de ia ions a e indica ed by e o ba s. Di e en le e s ma k signi i-
can di e ences be ween ea men s wi hin he ime poin (K uskal-
Wallis es , P < 0.05)
Table 1 E alua ion o SCE
acu e oxici y in es s wi h
eshwa e c us aceans
O ganism EC50/LC50 (mg/L) S d. e o R2Con iden ial in e als
D. magna (24 h) 0.0448 0.0022 0.9313 0.032–0.062
D. magna (48 h) 0.0152 0.0008 0.8921 0.011–0.023
T. pla yu us (24 h) 0.4572 0.0274 0.9849 0.319–0.594
Fig. 2 Acu e oxici y es o SCE on Thamnocephalus pla yu us a e
24 h. Da a poin s ep esen he mean o e nine eplica es, and s anda d
de ia ions a e indica ed by e o ba s. Di e en le e s ma k signi ican
di e ences be ween ea men s (K uskal-Wallis es , P < 0.05)
112628 En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
1 3
Discussion
Biologically ac i e subs ances con ained in plan s, ui s
o seeds ep esen a wide ange o chemicals which can
be help ul o humans bu oxic o o he o ganisms in he
en i onmen . One g oup o hese seconda y me aboli es is
lignans, compounds wi h allelopa hic po en ial. Schisand in
and o he lignans in S. chinensis ui s a e highly bene i-
cial o human heal h. S ill, hey can ep esen a se e e isk
o o he o ganisms, as al eady p o ed o he aqua ic plan
Lemna mino (Valicko a e al. 2023). Cu en ly, he eco-
oxicological da a on he e ec s o plan lignans in a wa e
en i onmen on o he o ganisms, including zooplank on,
a e sca ce, and schisand in s ill needs o be e alua ed. Bu
as Mayo ga e al. (2010) and o he s s a ed, using complex
whole plan ex ac s in eco oxicological s udies can be mo e
sui able and signi ican han s udying ac ions because he
indi idual cons i uen s can lose hei speci ic bioac i i y
when isola ed om he c ude ex ac .
C us aceans ep esen an essen ial pa o he zooplank-
on. D. magna and T. pla yu us belong o he common spe-
cies known o hei sensi i i y o pollu ion in he aqua ic
en i onmen and a e, he e o e, o en used as model o gan-
isms (Al a enga e al. 2016; Szkla ek e al. 2022). The e o e,
his pape aimed o simula e he condi ions when he ex ac-
ion o compounds con ained in S. chinensis ui s occu s
acciden ally in a wa e body and zooplank on species ge in
con ac wi h i .
Bo h es ed species exhibi ed conside able sensi i i y
when exposed o S. chinensis ui ex ac . As shown in
Table1, a e 24 h, he EC50 alue o D. magna (0.0448
mg/L) was en imes lowe han o T. pla yu us (0.4572
mg/L), and a e 48 h, he s anda d es pe iod o D. magna,
he EC50 alue dec eased e en o 0.0152 mg/L. The exac
mechanism o SCE oxici y o he c us aceans is cu en ly
unknown.
Acco ding o he li e a u e sou ces (Slanina e al. 1997;
Kohda e al. 2012), he con en o schisand in in S. chin-
ensis ui s can each 0.2 o 0.5% o hei d y weigh , i.e.
one S. chinensis be y (a e age d y weigh app ox. 30 mg)
can con ain 0.06 o 0.15 mg o schisand in. Hypo he ically,
when conside ing his schisand in con en , o eaching he
schisand in concen a ion in a wa e body close o he EC50
alue o D. magna, only dozens o Schisand a be ies could
be su icien o con amina e hund eds o li es o wa e .
The suscep ibili y o hese species o a ious chemicals,
including na u al compounds, is di e en . In his case, T.
pla yu us seems o be less sensi i e o SCE as compa ed o
D. magna, simila o he esul s published on o he o ganic
pollu ion, like oli e oil mill was ewa e (Paixao e al.
1999), a ious o ganic ma e s like compos , diges a e o
sludge eluen s (Al a enga e al. 2016) o u ban was ewa-
e con amina ed by a i icial swee ene s (Ke be o a e al.
2022). Opposingly, in he case o ino ganic de-icing sal s,
D. magna was less sensi i e han T. pla yu us (Szkla ek
e al. 2022). Some examples o hei di e ences in sensi-
i i y o o he con aminan s a e gi en in Table2.
The e ec i e concen a ion (EC50) o T apa japonica
lea es ex ac o D. magna was om 4 o 22 g we mass
pe li e (Ishimo a e al. 2019), and in con as o his, EC50
o SCE o D. magna is 0.0152 mg/L (Table1) co espond-
ing o 15 o 37.5 mg esh weigh pe li e o S.chinensis
be ies. Simila ly, he ex ac om Hedychium co ona ium
hizomes exhibi ed a 50% mo ali y a e o Daphnia similis
in concen a ion app ox. 1.3 g esh weigh pe li e (Cos a
e al. 2021). Bo h hese esul s show ha S. chinensis ui
ex ac is mo e oxic o daphnids han ex ac s om o he
plan s.
In he case o T. pla yu us, Mayo ga e al. (2010) s a ed
highe sensi i i y o his species as compa ed o ano he
c us acean A emia salina when exposed o an ex ac o
di e en Gua emalan plan s. The le hal concen a ion (LC50)
ange was om 10 o 500 mg/L. Cangiano e al. (2002)
desc ibed he oxic e ec o di e penes om Ruppia ma -
i ima and Po amoge on na ans on g een algae and a ew
zooplank on species, including D. magna and T. pla yu us.
In his case, T. pla yu us was mo e sensi i e han D. magna,
and he LC50 alue o he mos oxic compound eached
0.84 μM, a lowe alue han in SCE 0.4572 mg/L (co e-
sponding o 1 μM schisand in).
Ji e al. (2014) desc ibed ha only he mino i y o S.
chinensis bioac i e compounds (unme abolised o ms) we e
Table 2 Acu e oxici y (EC50/
LC50) o selec ed con aminan s
o eshwa e c us aceans D.
magna and T. pla yu us. EC50
alues a e exp essed as means
Con aminan EC50 (mg/L; 48 h) LC50 (mg/L; 24 h) Re e ence
D. magna T. pla yu us
Tebuconazole Fungicide 2.37 0.115 To an e al. (2023)
Nico ine Alkaloid 0.789 Insensi i e O opesa e al. (2017)
Amidine polys y ene Nanoplas ics 36.2 194.8 Saa ed a e al. (2019)
Ca boxyl polys y ene 111.4 318.2
A azine Pes icide 35.5 36.7 Palma e al. (2008)
Endosul an sulpha e 0.92 0.58
Chlo py i os 0.74 × 10−3 0.53 × 10−3
112629En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
1 3
exc e ed ia bile, u ine and aeces in a s ed wi h S. chinen-
sis ex ac . Simila ly, Kim e al. (2014) s a ed only negligi-
ble exc e ion o Schisand a lignans ia u ine a e o al and
in a enous adminis a ion o S. chinensis ex ac s o a s.
I can be hypo hesised ha he was e wa e con amina ed
by schisand in used by humans as ood supplemen s would
be a negligible sou ce o con amina ion, and he p ima y
sou ce o con amina ion would be S. chinensis a ming in
la ge a eas due o ui o o he plan pa s allou .
Conclusion
Al hough S. chinensis p o ides many bene icial e ec s o
human heal h, i can ha m aqua ic ecosys ems. C us aceans
D. magna and T. pla yu us exhibi ed sensi i i y o wa e -
ex ac able bioac i e compounds om S. chinensis ui s
al eady in po en ially en i onmen ally ele an concen a ion.
Reac ion o o he zooplank on species o SCE is unp edic a-
ble; ne e heless, he acciden al con amina ion o wa e by S.
chinensis bioac i e compounds can dis u b agile ood webs.
Acknowledgemen s Au ho s would like o hank he Facul y o Chem-
is y, B no Uni e si y o Technology, and he Ins i u e o Bo any, Czech
Academy o Sciences, o acili a ing his esea ch.
Au ho s con ibu ion JV: concep ualiza ion, in es iga ion, me hodol-
ogy, w i ing—o iginal d a , w i ing— e iew and edi ing. ŠZ: da a
cu a ion, o mal analysis, w i ing— e iew and edi ing. EM: concep-
ualiza ion, me hodology, supe ision, w i ing— e iew and edi ing.
JK: supe ision, w i ing— e iew and edi ing. BM: supe ision, w i -
ing— e iew and edi ing. RO: supe ision
Funding Open access publishing suppo ed by he Na ional Technical
Lib a y in P ague. This wo k was suppo ed by he Minis y o Educa-
ion o he Czech Republic g an No. FCH-S-22-8001 and Resea ch
Ins i u e De elopmen P og amme No. RVO67985939.
Da a a ailabili y Da a will be made a ailable on a easonable eques .
Decla a ions
E hical app o al No applicable. This s udy does no in ol e human
pa icipan s no animals eques ing an e hical app o al.
Consen o pa icipa e All lis ed au ho s ha e pa icipa ed on he
ese ch conduc ed and/o manusc ip p epa a ion.
Consen o publica ion All lis ed au ho s ha e app o ed he manu-
sc ip be o e submission, including hei names and o de o au ho s.
Compe ing in e es s The au ho s decla e no compe ing in e es s.
Open Access This a icle is licensed unde a C ea i e Commons A i-
bu ion 4.0 In e na ional License, which pe mi s use, sha ing, adap a-
ion, dis ibu ion and ep oduc ion in any medium o o ma , as long
as you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce,
p o ide a link o he C ea i e Commons licence, and indica e i changes
we e made. The images o o he hi d pa y ma e ial in his a icle a e
included in he a icle’s C ea i e Commons licence, unless indica ed
o he wise in a c edi line o he ma e ial. I ma e ial is no included in
he a icle’s C ea i e Commons licence and you in ended use is no
pe mi ed by s a u o y egula ion o exceeds he pe mi ed use, you will
need o ob ain pe mission di ec ly om he copy igh holde . To iew a
copy o his licence, isi h p://c ea i ecommons.o g/licenses/by/4.0/.
Re e ences
Al a enga P, Mou inha C, Fa o M, Palma P, Sengo J, Mo ais MC,
Cunha-Queda C (2016) Eco oxicological assessmen o he po en-
ial impac on soil po ewa e , su ace and g oundwa e om he
use o o ganic was es as soil amendmen s. Eco ox En i on Sa e
126:102–110. h ps:// doi. o g/ 10. 1016/j. ecoen . 2015. 12. 019
Cangiano T, Dellag eca M, Fio en ino A, Isido i M, Monaco P, Za elli
A (2002) E ec o en -labdane di e penes om Po amoge onaceae
on Selenas um cap ico nu um and o he aqua ic o ganisms. J Chem
Ecol 28:1091–1102. h ps:// doi. o g/ 10. 1023/A: 10162 13630 957
Choi SI, Kang HM, Sa o N (2015) A s udy o he Schisand a p oduc-
ion s uc u e in Ko ea. J Fac Ag Kyushu U 60:553–561
Cos a RO, Viei a BH, Espindola ELG, Ribei o AI, Fe o JLR, Fe -
nandes JB, Ma os D.D (2021) Toxici y o hizomes o he
in asi e Hedychium co ona ium (Zingibe aceae) on aqua ic
species. Biol In asions 23:2221-2231. h ps:// doi. o g/ 10. 1007/
s10530- 021- 02501-y
Cos as-Gil A, Reigosa MJ, Sanchez-Mo ei as AM (2018) The na u-
al compound podophyllo oxin induces g ow h inhibi ion and
mic o ubule condensa ion on A abidopsis oo s. Allelopa hy J
45:255–262. h ps:// doi. o g/ 10. 26651/ allelo. j./ 2018- 45-2- 1191
Hancke JL, Bu gos RA, Ahumada F (1999) Schisand a chinensis
(Tu cz.) Baill. Fi o e apia 70:451–471. h ps:// doi. o g/ 10. 1016/
S0367- 326X(99) 00102-1
Ishimo a M, Nakajima D, Sakamo o M, Miyaba a Y (2019) Wa e -sol-
uble bioac i e na u al compounds in T apa japonica lea es: em-
po al changes in chemical composi ion and e ec s on cladoce ans.
Ecol Res 34:328–335. h ps:// doi. o g/ 10. 1111/ 1440- 1703. 1274
ISO 14380:2011 Wa e quali y — De e mina ion o he acu e oxici y
o Thamnocephalus pla yu us (C us acea, Anos aca)
ISO 6341:2012 Wa e quali y — De e mina ion o he inhibi ion o
he mobili y o Daphnia magna S aus (Cladoce a, C us acea)
— acu e oxici y es
Ji D, Liu J, Li L, Mao CQ, Yin FZ, Lu TL (2014) Simul aneous quan-
i ica ion o schisand in, deoxyschisand in and schisand in B in
a bile, u ine, and eces and applica ion o exc e ion s udy. La
Am J Pha m 33:797–803
Ke be o a V, Ga goso a HZ, Casla sky J (2022) Occu ence and eco-
oxici y o selec ed a i icial swee ene s in he B no ci y was e
wa e . In J En i on Sci Te 19:9055–9066. h ps:// doi. o g/ 10. 1007/
s13762- 021- 03771-8
Kim YJ, Lee HJ, Kim CY, Han SY, Chin YW, Choi YH (2014) Simul ane-
ous de e mina ion o nine lignans om Schisand a chinensis ex ac
using ul a-pe o mance liquid ch oma og aphy wi h andem mass
spec ome y in a plasma, u ine, and gas oin es inal ac samples:
applica ion o he pha macokine ic s udy o Schisand a chinensis. J
Sep Sci 37:2851–2863. h ps:// doi. o g/ 10. 1002/ jssc. 20140 0451
Kohda H, Ozaki M, Name a A (2012) P oduc ion o lignans in calluses
o Schisand a chinensis. J Na Med 66:373–376. h ps:// doi. o g/
10. 1007/ s11418- 011- 0586-y
Lee S, Yeon SW, Tu k A, Ryu SH, Seo J, Lee KY, Hwang BY, Shin H,
Lee MK (2022) Va ia ion o lignan con en and alpha-glucosidase
inhibi o y ac i i y o Schisand a chinensis ui a di e en ma u a ion
s ages: compa ison wi h s em, lea and seed. Sci Ho ic - Ams e dam
293:110679. h ps:// doi. o g/ 10. 1016/j. scien a. 2021. 110679

112630 En i onmen al Science and Pollu ion Resea ch (2023) 30:112625–112630
1 3
Leis K, Baska A, Mazu E, Kaczo P, Racinowski M, Galazka P (2020)
Schisand ins impac on he e iciency o human body: a e iew.
Sci Spo 35:271–278. h ps:// doi. o g/ 10. 1016/j. scispo. 2019. 12. 009
Ma Y, Deng YY, Li N, Dong A, Li HD, Chen S, Zhang S, Zhang
MZ (2023) Ne wo k pha macology analysis combined wi h
expe imen al alida ion o explo e he he apeu ic mechanism o
Schisand a Chinensis Mix u e on diabe ic neph opa hy. J E hnop-
ha macol 302:115768. h ps:// doi. o g/ 10. 1016/j. jep. 2022. 115768
Mayo ga P, Pe ez KR, C uz SM, Cace es A (2010) Compa ison o
bioassays using he anos acan c us aceans A emia salina and
Thamnocephalus pla yu us o plan ex ac oxici y sc eening.
Re is a B asilei a De Fa macognosia-B azilian Jou nal o Pha -
macognosy 20:897–903. h ps:// doi. o g/ 10. 1590/ S0102- 695X2
01000 50000 29
OECD Guidelines Tes No. 202: (n.d.) Daphnia sp. acu e immobilisa-
ion es h ps:// doi. o g/ 10. 1787/ 97892 64069 947- en
O opesa AL, Flo o AM, Palma P (2017) Toxic po en ial o he
eme ging con aminan nico ine o he aqua ic ecosys em. En i-
on Sci Pollu R 24:16605–16616. h ps:// doi. o g/ 10. 1007/
s11356- 017- 9084-4
Paixao SM, Mendonca E, Picado A, Anselmo AM (1999) Acu e oxici y
e alua ion o oli e oil mill was ewa e s: a compa a i e s udy o h ee
aqua ic o ganisms. En i on Toxicol 14:263–269. h ps:// doi. o g/ 10.
1002/ (SICI) 1522- 7278(199905) 14: 2< 263:: AID- TO X7>3. 0. C O;2-D
Palma P, Palma VL, Fe nandes RM, Soa es A, Ba bosa IR (2008)
Acu e oxici y o a azine, endosul an sulpha e and chlo py i os o
Vib io ische i, Thamnocephalus pla yu us and Daphnia magna,
ela i e o hei concen a ions in su ace wa e s om he Alen ejo
egion o Po ugal. B En i on Con amin Tox 81:485–489. h ps://
doi. o g/ 10. 1007/ s00128- 008- 9517-3
Panossian A, Wikman G (2008) Pha macology o Schisand a
chinensis Bail.: an o e iew o Russian esea ch and uses in
medicine. J E hnopha macol 118:183–212. h ps:// doi. o g/ 10.
1016/j. jep. 2008. 04. 020
Saa ed a J, S oll S, Sla eyko a VI (2019) In luence o nanoplas ic
su ace cha ge on eco-co ona o ma ion, agg ega ion and oxici y
o eshwa e zooplank on. En i on Pollu 252:715–722. h ps://
doi. o g/ 10. 1016/j. en pol. 2019. 05. 135
Sca o A, Pandino G, Res uccia A, Lomba do S, Pesce GR, Mau o-
micale G (2019a) Allelopa hic po en ial o lea aqueous ex ac s
om Cyna a ca dunculus L. on he seedling g ow h o wo cos-
mopoli an weed species. I al J Ag on 14:78–83. h ps:// doi. o g/
10. 4081/ ija. 2019. 1373
Sca o A, Rial C, Molinillo JMG, Va ela RM, Mau omicale G, Macias
FA (2019b) The ex ac ion p ocedu e imp o es he allelopa hic
ac i i y o ca doon (Cyna a ca dunculus a . al ilis) lea allelo-
chemicals. Ind C op P od 128:479–487. h ps:// doi. o g/ 10. 1016/j.
indc op. 2018. 11. 053
Slanina J, Tabo ska E, Lojko a L (1997) Lignans in he seeds and
ui s o Schisand a chinensis cul u ed in Eu ope. Plan a Med
63:277–280. h ps:// doi. o g/ 10. 1055/s- 2006- 957676
Smejkal K, Slape o a T, K mencik P, Babula P, Dall'Acqua S,
Innocen i G, Vanco J, Casa in E, Ca a a M, Kal a o a K,
D o ska M, Slanina J, K ama o a E, Julinek O, U bano a M
(2010) E alua ion o cy o oxic ac i i y o Schisand a chin-
ensis lignans. Plan a Med 76:1672–1677. h ps:// doi. o g/ 10.
1055/s- 0030- 12498 61
Szkla ek S, Go ecka A, Salabe B, Woj al-F ankiewicz A (2022)
Acu e oxici y o se en de-icing sal s on ou zooplank on species-
is he e an “eco- iendly” al e na i e? Ecohyd ology & Hyd obi-
ology 22:589–597. h ps:// doi. o g/ 10. 1016/j. ecohyd. 2022. 08. 005
Szopa A, Ekie R, Ekie H (2017) Cu en knowledge o Schisan-
d a chinensis (Tu cz.) Baill. (Chinese magnolia ine) as a
medicinal plan species: a e iew on he bioac i e componen s,
pha macological p ope ies, analy ical and bio echnological
s udies. Phy ochem Re 16:195–218. h ps:// doi. o g/ 10. 1007/
s11101- 016- 9470-4
Teodo idis V (2005) Ea ly Miocene seeds o Schisand a mo a ica
(MAI) GREGOR om he Czech Republic. Neues Jah buch Fu
Geologie Und Palaon ologie-Mona she e 11:663–682. h ps:// doi.
o g/ 10. 1127/ njgpm/ 2005/ 2005/ 663
To an L, Ni a V, Nenciu M, Coa u V, Laza L, Dami N, Vasile D,
Popo iciu DR, B o ea AG, Cu ean-Banaduc AM, A amescu S,
Aono iesei F (2023) Mul iple assays on non- a ge o ganisms o
de e mine he isk o acu e en i onmen al oxici y in ebucona-
zole-based ungicides widely used in he black sea coas al a ea.
Toxics 11:597. h ps:// doi. o g/ 10. 3390/ oxic s1107 0597
Valicko a J, Zezulka S, Ma salko a E, Ko lik J, Ma salek B, Opa ilo a
R (2023) Bioac i e compounds om Schisand a chinensis - isk
o aqua ic plan s? Aqua Toxicol 254:106365. h ps:// doi. o g/ 10.
1016/j. aqua ox. 2022. 106365
Wang JC, Wang BQ (2013) An ioxidan ac i i y o Schisand a chin-
ensis ex ac and de i a i es. 2nd In e na ional Con e ence on
Ene gy, En i onmen and Sus ainable De elopmen (EESD 2012).
Ad Ma e Res-Swi z 610-613:3549–3551. h ps:// doi. o g/ 10.
4028/ www. scien i ic. ne / AMR. 610- 613. 3549
Wang XT, Yu JH, Li W, Wang CM, Li H, Ju WB, Chen JG, Sun JH
(2018) Cha ac e is ics and an ioxidan ac i i y o lignans in
Schisand a chinensis and Schisand a sphenan he a om di e -
en loca ions. Chem Biodi e s 15:e1800030. h ps:// doi. o g/ 10.
1002/ cbd . 20180 0030
Publishe ’s No e Sp inge Na u e emains neu al wi h ega d o
ju isdic ional claims in published maps and ins i u ional a ilia ions.