Eco oxicology and En i onmen al Sa e y 216 (2021) 112226
A ailable online 10 Ap il 2021
0147-6513/© 2021 The Au ho (s). Published by Else ie Inc. This is an open access a icle unde he CC BY-NC-ND license
(h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/).
High sensi i i y o in e eb a e de i i o es om opical s eams o
di e en pes icides
Ayde´
e Co nejo
a
,
*
,
1
, F ancisco Encina-Mon oya
b
, F ancisco Co ea-A aneda
c
, Dalys Ro i a
d
,
Gab iela Ga cía
a
, Ca los Nie o
a
, Víc o Villa eal
d
, Nicomedes Ja amillo
e
, Edga P´
e ez
a
,
Anayansi Valde ama
a
, Ja ie P´
e ez
, Luz Boye o
,
g
a
Aqua ic Ecology and Eco oxicology Labo a o y, Zoological Collec ion Eus o gio Mendez, Go gas Memo ial Ins i u e o Heal h S udies, (COZEM-ICGES), A e. Jus o
A osemena and Calle 35, 0816-02593 Panama Ci y, Panama
b
Núcleo de Es udios Ambien ales, Depa amen o de Ciencias Ambien ales, Facul ad de Recu sos Na u ales, Uni e sidad Ca ´
olica de Temuco, 4780000 Temuco, Chile
c
Unidad de Cambio Clim´
a ico y Medio Ambien e (UCCMA), Ins i u o Ibe oame icano de Desa ollo Sos enible (IIDS), Uni e sidad Au ´
onoma de Chile, Temuco, Chile
d
Wa e Labo a o y and Physicochemical Se ices (LASEF), Au onomous Uni e si y o Chi iqui, Da id Ci y, Panama
e
Resea ch Cen e o Na u al P oduc s and Bio echnology (CIPNABIOT), Au onomous Uni e si y o Chi iqui, Da id Ci y, Panama
Depa men o Plan Biology and Ecology, Facul y o Science and Technology, Uni e si y o he Basque Coun y (UPV/EHU), Leioa, Spain
g
IKERBASQUE, Bilbao, Spain
ARTICLE INFO
Edi ed by: D Yong Liang
Keywo ds:
Ag icul u e
De i i o es
F eshwa e
Fungicides
Insec icides
Toxici y bioassays
The opics
ABSTRACT
F eshwa e o ganisms a e o en sensi i e o pes icides, bu hei sensi i i y a ies ac oss di e en axa and wi h
pes icide ype and ac ion mode, as shown by mul iple acu e oxici y es s. Such a iabili y hampe s p edic ions
abou how eshwa e ecosys ems may be al e ed by pes icide oxici y, which is especially c i ical o unde -
s udied a eas o he wo ld such as he opics. Fu he mo e, he e is li le in o ma ion abou he sensi i i y o
some o ganisms ha a e key componen s o s eam ood webs; his is he case o li e - eeding de i i o ous
in e eb a es, which con ibu e o he undamen al p ocess o li e decomposi ion. He e, we examined he
sensi i i y o h ee common de i i o es [Anchy a sus sp. (Coleop e a: P ilodac ylidae), Hyalella sp. (Amphipoda:
Hyalellidae) and Lepidos oma sp. (T ichop e a: Lepidos oma idae)] o h ee pes icides commonly used ( he in-
sec icides bi en h in and chlo py i os and he ungicide chlo o halonil) using acu e (48 o 96 h) oxici y es s.
Ou s udy demons a es ha common-use pes icides p o oke he mo ali y o hal hei popula ions a concen-
a ions o 0.04–2.7
μ
g L
-1
. We ound ha all species we e sensi i e o he h ee pes icides, wi h he highes
sensi i i y ound o chlo py i os. Addi ionally, we used he app oach o species sensi i i y dis ibu ions (SSD) o
compa e ou s udy species wi h Daphnia magna and o he empe a e and opical in e eb a es. We ound ha
he s udy species we e among he mos sensi i e species o chlo py i os and chlo o halonil. Ou esul s sugges
ha opical de i i o es me i special a en ion in ecological isk assessmen o pes icides and highligh he need
o accu a e eco oxicological in o ma ion om ecologically ele an species in he opics.
1. In oduc ion
T opical o es s a e declining a unp eceden ed a es in a o o
ag icul u e (Gibbs e al., 2010), and such eplacemen causes se e e
impac s on s eam ecosys ems ha a e associa ed o mul iple s esso s
(Rasmussen e al., 2016; Co nejo e al., 2019). Among hese s esso s,
pes icides a e o g ea impo ance as hey a e o en oxic o eshwa e
o ganisms (Sch¨
a e e al., 2011), causing suble hal and le hal e ec s and
subsequen al e a ions in ecosys ems (Bighiu e al., 2020; Bundschuh
e al., 2020; Co nejo e al., 2020b). Many s udies ha e examined he
oxici y o di e en pes icides on a a ie y o eshwa e in e eb a es
h ough acu e and ch onic oxici y es s, bu he g ea majo i y o hese
s udies ha e been conduc ed wi h species om empe a e a eas, mos ly
Eu ope and No h Ame ica (Rico e al., 2011). Because o his pauci y o
da a, wa e quali y c i e ia in mos opical egions ely on ex apola-
ions o eco oxicological da a om empe a e zones using s anda d
empe a e species, assuming ha hei sensi i i ies a e simila (Kwok
e al., 2007; Sch¨
a e e al., 2013), e en hough he a e and e ec s o
* Co esponding au ho .
E-mail add ess: [email p o ec ed] (A. Co nejo).
1
ORCID-ID: 0000-0001-6789-5847.
Con en s lis s a ailable a ScienceDi ec
Eco oxicology and En i onmen al Sa e y
jou nal homepage: www.else ie .com/loca e/ecoen
h ps://doi.o g/10.1016/j.ecoen .2021.112226
Recei ed 28 Decembe 2020; Recei ed in e ised o m 27 Ma ch 2021; Accep ed 31 Ma ch 2021
Eco oxicology and En i onmen al Sa e y 216 (2021) 112226
2
pes icides may be di e en be ween clima ic egions (Daam and Rico,
2018). This is an impo an esea ch gap ha hinde s accu a e assess-
men s o he en i onmen al isk o pes icides in opical s eams.
Addi ionally, he e is li le in o ma ion abou how some g oups o
o ganisms a e a ec ed by pes icides, and his includes li e - eeding
de i i o ous in e eb a es (he ea e de i i o es), which a e majo
componen s o s eam ood webs (Cummins e al., 1989), especially in
o es ed headwa e s (Vanno e e al., 1980). Li e decomposi ion is a key
p ocess and a undamen al componen o s eam ecosys em unc ioning,
media ed by mic obial decompose s and de i i o es (G aça, 2001).
These in e eb a es eed on li e and hus con ibu e o i s agmen a-
ion, he p oduc ion o ine pa icula e o ganic ma e ha se es as ood
o collec o s (Cummins and Klug, 1979), and nu ien ecycling
(L´
opez-Rojo e al., 2019). E en i de i i o es a e less abundan and
species ich in he opics han in empe a e a eas (Boye o e al., 2011),
hey s ill play an impo an ecological ole (Boye o e al., 2012; Cheshi e
e al., 2005; Yule e al., 2010). Fo his eason, and because hey o en
belong o sensi i e axa (e.g., T ichop e a, Amphipoda; Boye o e al.,
2020), i becomes c ucial o assess how de i i o es a e a ec ed by he
p esence and concen a ion o pes icides in s eams.
He e, we examined he sensi i i y o h ee common opical de i-
i o es [Anchy a sus sp. (Coleop e a: P ilodac ylidae), Hyalella sp.
(Amphipoda: Hyalellidae) and Lepidos oma sp. (T ichop e a: Lep-
idos oma idae)] o h ee pes icides commonly used in ag icul u al land
in Cen al Ame ica and wes e n Panama: he insec icides bi en h in and
chlo py i os and he ungicide chlo o halonil. We pe o med acu e (48
o 96 h) oxici y es s o assess he mo ali y and o calcula e he mean
le hal concen a ion (LC
50
) o each pes icide o each species (wi h he
only excep ion o he Lepidos oma – bi en h in combina ion). We hen
used he app oach o species sensi i i y dis ibu ions (SSDs) o in eg a e
acu e oxici y da a o mul iple aqua ic o ganisms om di e en ophic
le els and geog aphic egions. SSDs a e used o es ima e haza dous
concen a ions (HC
p
) ha a ec p% o species (Pos huma e al., 2002).
We p edic ed ha (1) ou s udy species would be sensi i e o he h ee
pes icides es ed, despi e he exis ence o (2) di e ences among species
and (3) di e ences among pes icides, wi h he insec icides being mo e
ha m ul han he ungicide; and (4) ou s udy species would be mo e
sensi i e han empe a e species, including he s anda d species
D. magna.
2. Ma e ials and me hods
2.1. S udy a ea
Ou s udy a ea was he uppe ca chmen o he Chi iquí Viejo i e ,
loca ed on he Paci ic coas o wes e n Panama (8.25 – 9.00 ºN, 82.25 –
83.00 ºW). Ca chmen a ea is 1376 km
2
, he leng h o he main i e is
161 km and he highes al i ude is 3474 m a.s.l. a he Ba ú Volcano
(ETESA, 2008). The clima e is opical, wi h minimum, a e age and
maximum ai empe a u es o 17.8, 28.0 and 35.5 ºC, espec i ely
(ANAM and CATIE, 2014). To al annual p ecipi a ion is 3400 mm on
a e age, wi h a maximum o 7000 mm a high al i udes, 87.7% occu -
ing in he we season om May o Decembe (ETESA, 2008). We con-
duc ed he s udy a he ou doo acili ies o he Minis y o he
En i onmen S a ion in he La Amis ad In e na ional Pa k (PILA; 8.894
ºN, 82.615 ºW; MS Fig. S1), loca ed ca. 400 m away om one o he
s eams whe e in e eb a es we e collec ed. This acili a ed he collec-
ion and anspo o in e eb a es and wa e , and ensu ed simila
empe a u e condi ions be ween he collec ion si es and expe imen al
loca ion.
2.2. Pes icide selec ion
A o al o 29 pes icides ha e been epo ed in he uppe ca chmen o
he Chi iquí Viejo i e (Co nejo e al., 2019). We selec ed h ee o he
p esen s udy based on hei epo ed concen a ions, pe sis ence in he
en i onmen , physical p ope ies, mechanisms o ac ion and haza d
(Table S1): he insec icides bi en h in and chlo py i os and he ungicide
chlo o halonil. Bi en h in (C
23
, H
22
ClF
3
O
2
) is a py e h oid insec icide
commonly used in he con ol o oliage, which in e e es wi h he so-
dium channel; in ou s udy a ea i has been epo ed in anges om 0.15
o 0.35 µg L
-1
(Co nejo e al., 2019). Chlo py i os (C
9
H
11
Cl
3
NO
3
PS) is an
o ganophospha e insec icide ha ac s as ace ylcholines e ase (AChE)
inhibi o i is widely used in ag icul u e and i has been epo ed in
anges om 0.14 o 15.24 µg L
-1
in ou s udy a ea (Co nejo e al., 2019).
Chlo o halonil (C
8
Cl
4
N
2
) is a polychlo ina ed a oma ic compound ha
has been epo ed in anges om 0.26 o 0.38 µg L
-1
in sedimen in he
s udy basin (MIDA, 2016), and i has been shown o be le hal o
empe a e de i i o ous caddis lies in mic ocosms (Co nejo e al.,
2020a).
The h ee pes icides we e pu chased a local ag icul u al s o es
au ho ized o he sale and dis ibu ion o ag ochemicals. The anges
p o ided o he h ee pes icides a e hose epo ed in a p e ious s udy
conduc ed in he same a ea (Co nejo e al., 2019; MIDA, 2016). The
dilu ions we e made using il e ed s eam wa e om he Chi iquí Viejo
i e collec ed wi hin he PILA, whe e no pes icides had been de ec ed
(Co nejo e al., 2020b). Two anges we e se o wo king solu ions: a i s
ange o low concen a ions (0.01, 0.1, 0.5 µg L
-1
), and a second ange o
high concen a ions (1.0, 1.5, 2.5, 5.0 and 10.0 µg L
-1
). The wo king
solu ions we e p epa ed om wo nominal o s ock solu ions: 100 mg L
-1
o he i s ange and 1000 mg L
-1
o he second ange. S ock solu ions
we e p epa ed based on he concen a ion o he ac i e p inciple indi-
ca ed in he comme cial p oduc s, using mic opipe es wi h plas ic ips
and glass olume ic lasks. Nominal concen a ions we e used because
we could no make measu emen s du ing he expe imen due o logis-
ical and inancial limi a ions. Thus, we acknowledge ha ou esul s
can be compa ed wi h o he s udies bu should no be used in egula o y
isk assessmen (Von Fume i and Blau ock, 2018).
2.3. Taxon selec ion, sampling and acclima ion
We ob ained a lis o common de i i o es and hei dis ibu ion in
he Chi iquí Viejo i e uppe ca chmen om p e ious s udies (Co nejo
e al., 2019, 2020b), and chose h ee axa ha we e dominan in he
a ea: Anchy a sus sp., Hyalella sp. and Lepidos oma sp. We did no iden-
i y he species, bu con i med ha all indi iduals belonged o he same
species (al hough we name hem as gene a he ea e o simplici y). We
collec ed hese de i i o es in 1s and 2nd o de independen ibu a ies
o he Chi iquí Viejo i e loca ed wi hin p o ec ed a eas o gua an ee
ha indi iduals had no been p e iously exposed o pes icides. These
a eas whe e he Ba ú Volcano Na ional Pa k (PNVB), whe e we collec ed
specimens o Lepidos oma, and he PILA, whe e we collec ed Anchy a sus
and Hyalella. We used wo sampling echniques: li e bags illed wi h
Alnus acumina a Kun h. (Be ulaceae) ha we e subme ged in he s eam
o 15 days, and mul ihabi a sampling using a 0.5 mm D-ne . A each
sampling si e we used a mul ipa ame e p obe (HACH; HQ40d) o
measu e pH, empe a u e (ºC), conduc i i y (
μ
S cm
-1
), u bidi y (NTU)
and dissol ed oxygen sa u a ion (%); and a lowme e (Flowa ch 12,
300) o measu e cu en eloci y m s
-1
(Table S2).
The collec ed in e eb a es we e placed in plas ic con aine s illed
wi h s eam wa e and li e and p o ided wi h cons an ae a ion, and
ans e ed o he expe imen al acili ies whe e hey we e coun ed and
iden i ied using a s e eoscope. They we e hen placed in aqua iums
con aining 1–2 L o s eam il e ed wa e , whe e hey we e acclima ed
o 96 h wi h cons an ae a ion (p o ided h ough sy inge ips connec ed
o a pump), a an ai empe a u e o 17.1 ±0.8 ◦C, wa e empe a u e o
14.4 ±0.2 ◦C, and ligh : da k egime o 12:12 h ( he na u al condi ions
a he ime o he expe imen ). They we e ed wi h agmen s o
A. acumina a li e o he i s 48 h o acclima ion and hen as ed o he
las 24 h be o e s a ing he acu e oxici y es s (Table S3).
A. Co nejo e al.
Eco oxicology and En i onmen al Sa e y 216 (2021) 112226
3
2.4. Toxici y es s
The es s we e conduc ed in 216 mic ocosms dis ibu ed in 67
ea men s, which co esponded o di e en combina ions o axa
(Anchy a sus, Hyalella and Lepidos oma), pes icide ypes (bi en h in,
chlo py i os and chlo o halonil) and pes icide concen a ions [0 (con-
ol), 0.01, 0.1, 0.5, 1.0, 1.5, 2.5, 5.0 and 10.0
μ
g L
-1
]; he only combi-
na ions ha we e absen , due o logis ical cons ain s, we e hose wi h
Lepidos oma and bi en h in. Thus, he e we e 24 mic ocosms pe com-
bina ion o axon and pes icide, and h ee eplica es pe concen a ion
(excep con ols, N =6–9; Table S4; Fig. S1). Each mic ocosm con ained
200 mL o il e ed (100 µm) s eam wa e , which was cons an ly ae a ed
h ough sy inge ips connec ed o an aqua ium pump, and ecei ed i e
indi iduals o a gi en species (wi h 1080 indi iduals es ed in o al: 405
Anchy a sus, 405 Hyalella and 270 Lepidos oma).
Tes me hods we e based on he En i onmen al P o ec ion Agency
s anda d p o ocol o oxici y es ing wi h eshwa e o ganisms (EPA,
2002). Howe e , some en i onmen al condi ions we e adap ed o he
ecological demands o he in e eb a es es ed. The expe imen was
pe o med in a s a ic exposu e egime wi h a single ini ial dose. Du ing
he expe imen he ai empe a u e was 17.1 ±0.8 ◦C, he wa e em-
pe a u e was 14.3 ±0.2 ◦C and he ligh : da k egime was 12:12 h
(which we e he condi ions in nea by s eams a he ime o he expe -
imen ). We assessed he e ec o pes icide exposu e using mo ali y as
he end poin . The es s las ed 48 (o 96 h in he case o Anchy a sus o
bi en h in and chlo o halonil) and le hal e ec s we e moni o ed 24 and
48 h (o 96 h) a e exposu e, wi h dead o ganisms being emo ed.
2.5. Da a analyses
Based on mo ali y a 48 o 96 h a e exposu e we calcula ed LC
50
alues (i.e., he concen a ion equi ed o kill 50% o he popula ion)
and associa ed 95% con idence in e als (CIs) o each species and
pes icide concen a ion, using he eco ox package [Hlina e al. (2019) in
R s a is ical so wa e (R Co e Team, 2020)]. We used he app oach o
SSD and HC
5
o compa e ou LC
50
alues wi h hose epo ed o aqua ic
o ganisms o di e en unc ional g oups [collec o s (Co); de i i o es
(De); he bi o es (Hb); omni o es (Om); p ima y p oduce s (Pp) and
p eda o s (P )], sepa a ed by pes icides and geog aphic dis ibu ion (see
summa y o da a used in Table S5-S7). Fo his, we used he da a
a ailable a he ECOTOX da abase o he Uni ed S a es En i onmen al
P o ec ion Agency (USEPA; h ps://c pub.epa.go /eco ox/sea ch.c m).
We selec ed da a om he ECOTOX da abase ollowing hese c i e ia
(pa ly as in Mal by e al., 2005): (1) endpoin s we e LC
50
o median
e ec concen a ion (EC
50
), ega ding mo ali y o immobili y o ani-
mals, and g ow h a e o algae; (2) es du a ion was 2–21 d o ish, and
1–7 d o in e eb a es and algae; (3) he lowes alue was selec ed when
se e al du a ion alues we e s udied in he same expe imen ; (4) he
geome ic mean was aken o da a o he same species (and end poin )
bu om di e en expe imen s; (5) da a epo ed as <o >we e no
used; (6) only s a ic es s ca ied ou in he labo a o y we e conside ed;
and (7) only alues published in scien i ic li e a u e we e used since
2000. We calcula ed he SSD using he ssd ools R package (Tho ley and
Schwa z, 2018), and buil di e en SSDs o LC
50
/EC
50
o he h ee
pes icides. The a ailable dis ibu ions included he log-no mal (lno m),
log-logis ic (llog), and gamma dis ibu ions. The compa ison be ween
he sensi i i y o opical and empe a e species o chlo py i os was
e i ied using he Kolmogo o -Smi no es .
3. Resul s
Mo ali y a e 48 o 96 h o exposu e was ≤10% in ou con ol
mic ocosms and co esponded o Hyallela. The esul s o he oxici y
es s, LC
50
alues (
μ
g L
-1
) and hei 95% con idence in e als (CI) a e
shown in Table 1. LC
50
alues indica ed ha chlo py i os was one o de
o magni ude mo e oxic han bi en h in and chlo o halonil o he
s udied species. Bo h Anchy a sus (LC
50–96 h
=1.54
μ
g L
-1
) and Hyalella
(LC
50–48 h
=1.77
μ
g L
-1
) had simila sensi i i ies o bi en h in exposu e.
In he case o chlo py i os, Hyalella (LC
50–48 h
=0.037
μ
g L
-1
) and Lep-
idos oma (LC
50–48 h
=0.038
μ
g L
-1
) we e he mos sensi i e species,
ollowed by Anchy a sus (LC
50–48 h
=0.079
μ
g L
-1
). Fo chlo o halonil,
Hyalella (LC
50–48 h
=0.57
μ
g L
-1
) was he mos sensi i e species, ol-
lowed by Lepidos oma (LC
50–48 h
=2.72
μ
g L
-1
) and Anchy a sus (LC
50–96
h
=1.96
μ
g L
-1
).
The bi en h in da ase used o he SSD analysis comp ised LC
50
/
EC
50
alues be ween 0.01 and 822 µg L
-1
o 16 eshwa e species (one
alga, ou c us aceans, eigh insec s and h ee ishes) om i e di e en
unc ional g oups (Co, De, Om, Pp and P ) o which only wo in e e-
b a e species co esponded o opical de i i o es ( om he p esen
s udy), wi h he es being empe a e de i i o es (Table S5). Chlo -
py i os was he pes icide wi h he highes a ailable in o ma ion; he
da ase comp ised LC
50
/EC
50
alues be ween 0.05 and 22,440 µg L
-1
o
49 eshwa e species ( ou algae, 16 c us aceans, 21 insec s and eigh
ishes) belonging o six di e en unc ional g oups (Co, De, Hb, Om, Pp
and P ) o which 18 species we e es ed in opical egions (including he
h ee species o his s udy) and he es in empe a e zones (Table S6).
Fo chlo o halonil, he da ase comp ised LC
50
/EC
50
alues be ween
0.57 and 8069.3 µg L
-1
o 10 eshwa e species ( ou algae, h ee
c us aceans, wo insec s and one ish) belonging o ou di e en unc-
ional g oups (Co, De, Om and Pp; Table S7).
The SSD cu es a e shown in Fig. 1 and he esul s a e summa ized in
Table 2. The log no mal model showed he bes i o he h ee pes i-
cides es ed (Table S8). Bi en h in (HC
5
o 0.009 µg L
-1
; Fig. 1A) and
chlo py i os (0.012
μ
g L
-1
; Fig. 1B) we e mo e oxic, compa ed o
chlo o halonil (HC
5
o 0.523
μ
g L
-1
; Fig. 1C). The compa ison be ween
he sensi i i y o opical and empe a e species o chlo py i os is p e-
sen ed in Fig. 2. We did no ind signi ican di e ences (p =0.59) be-
ween he HC
5
alues o opical species (n =18; HC
5
=0.009
μ
g L
-1
)
and hose o empe a e species (n =34; HC
5
=0.012
μ
g L
-1
), al hough
he HC
5
es ima es o opical species ended o be lowe .
4. Discussion
Ou s udy demons a es ha common-use pes icides can a ec
se e al species o opical s eam de i i o es, p o oking he mo ali y
o hal hei popula ions a concen a ions o 0.04–2.7
μ
g L
-1
. This is
Table 1
Resul s o he acu e oxici y es s (24–96 h) wi h bi en h in, chlo py i os and
chlo o halonil o h ee de i i o es, wi h mo ali y as endpoin ; we show he
LC
50
and R
2
o he es .
Pes icides Species Tes du a ion
(h)
LC
50
(95% CI;
μ
g L
-1
) R
2
Bi en h in Anchy a sus 24 10.7 (6.63–35.9) 0.54
48 2.86 (1.69–5.8) 0.63
96 1.54 (0.74–3.0) 0.67
Hyalella 24 4.30 (3.15–6.45) 0.49
48 1.77 (1.28–2.4) 0.74
Chlo py i os Anchy a sus 24 0.211 (0.106–0.345) 0.82
48 0.0799 (0.0333–0.148) 0.83
Hyalella 24 0.106 (0.04–0.22) 0.90
48 0.0370
(0.00671–0.0958)
0.88
Lepidos oma 24 0.0470
(0.0193–0.0898)
0.86
48 0.0384
(0.0147–0.0764)
0.86
Chlo o halonil Anchy a sus 24 –
48 4.62 (2.81–10.7) 0.41
96 1.96 (1.25–3.2) 0.85
Hyalella 24 2.61 (1.73–4.25) 0.76
48 0.57 (0.28–0.99) 0.84
Lepidos oma 24 5.08 (3.32–10.20) 0.62
48 2.72 (1.76–4.65) 0.69
A. Co nejo e al.
Eco oxicology and En i onmen al Sa e y 216 (2021) 112226
4
impo an because o he key ole o de i i o es in s eam ecosys ems as
main agen s ( oge he wi h aqua ic hyphomyce es) o lea li e
decomposi ion, a undamen al componen o s eam ecosys em unc-
ioning (G aça, 2001). In o ma ion abou he sensi i i y o hese o -
ganisms is sca ce because hey a e no s anda d o ganisms commonly
used in oxici y es s (F ei as and Rocha, 2010). Howe e , hey a e
highly ele an om an ecosys em pe spec i e, and likely o be s ongly
a ec ed by pes icides compa ed o o he o ganisms because hey can
inges pes icides no only om he wa e bu also while eeding on lea
li e , whe e pes icides can accumula e (Zub od e al., 2015; Co nejo
e al., 2020a).
The sca ci y o in o ma ion abou pes icide e ec s on s eam o -
ganisms is pa icula ly sca ce o opical egions (F ei as and Rocha,
2010), and ou cu en scien i ic knowledge in eco oxicology is based
mos ly on esea ch om empe a e sys ems (Gunna sson and Cas illo,
2018). This is pa ly due o he limi ed basic knowledge o ben hic auna
compa ed o ha o Eu ope, No h Ame ica and, o a lesse ex en ,
Aus alia and New Zealand (Boye o e al., 2009). Many opical insec
la al s ages ha e no been ela ed o adul s, so species canno be
iden i ied, and hei li e his o ies a e unknown (Boye o e al., 2009). Fo
his eason, opical s udies ha e o en used in o ma ion om
well-known, s anda d o ganisms such as D. magna, which a e no he
mos sensi i e (Sch¨
a e e al., 2013). Ou h ee s udy species we e mo e
sensi i e ha D. magna o chlo py i os and chlo o halonil (bu no o
bi en h in), so he consequences o hese pes icides in s eams whe e
hese de i i o es a e p esen would be unde es ima ed by conside ing
he esponses o D. magna.
Fig. 1. Species sensi i i y dis ibu ions (SSD) and haza dous concen a ions o 5% using he LC
50
/EC
50
alues o ou species and hose epo ed o eshwa e species
o di e en unc ional g oups. The solid line is he i ed Log No mal Model, he sec ion in g ay ep esen 95% con idence in e al, and he dashed line ed ep esen
haza dous concen a ions o 5%. A =Bi en h in (
μ
g L
-1
); B =Chlo py i os (
μ
g L
-1
); C =Chlo o halonil (
μ
g L
-1
). Colo ep esen s axonomic g oup as ollows:
=Algae; =C us aceans; =Fishes; =Insec s. Shape ep esen s unc ional g oup as ollows: •= Collec o s; ▴=De i i o es; ■=He ibo es; þ=Omni-
o es; =P ima y p oduce s; ✹=P eda o s.
Table 2
Haza dous concen a ion o 5% o species (HC
5
; µg L
-1
) and hei lowe (95%)
and uppe (5%) con idence limi s, calcula ed om species sensi i i y dis ibu-
ions cons uc ed o eshwa e species.
Pes icide name No. o species HC
5
(95% CI) R
2
Bi en h in All species 16 0.009 (0.001–0.114) 0.98
Chlo py i os All species 49 0.012 (0.003–0.0589) 0.98
T opical 18 0.009 (0.0005–0.469) 0.99
Tempe a e 34 0.012 (0.0027–0.0603) 0.98
Chlo o halonil All species 10 0.523 (0.0493–8.02) 0.97
Fig. 2. Tempe a e (blue cu e) and opical (g een cu e) species sensi i i y
(SSD) o chlo py i os (
μ
g L
-1
). The solid line is he i ed Log No mal Model
(blue o empe a e species and g een o opical), he g ey sec ions ep esen
he 95% con idence in e al. Colo ep esen s axonomic g oup as ollows:
=Algae; =C us aceans; =Fishes; =Insec s. Shape ep esen s
unc ional g oup as ollows: •= Collec o s; ▴=De i i o es; ■=He ibo es;
þ=Omni o es; =P ima y p oduce s; ✹=P eda o s.
A. Co nejo e al.
Eco oxicology and En i onmen al Sa e y 216 (2021) 112226
5
As in o he s udies, we ound no sys ema ic di e ences be ween he
sensi i i y o opical and empe a e species using he SSD app oach
(Diepens e al., 2014; Kha ika n e al., 2016; Kwok e al., 2007; Mal by
e al., 2005; Rico e al., 2010, 2011). O he s had hypo hesized ha
opical o ganisms would be mo e suscep ible o pes icide exposu e han
hei empe a e coun e pa s, due o he highe empe a u es in he
opics and hence he highe me abolic a es o opical o ganisms
(Cas illo e al., 1997; Pe e s e al., 1997). Howe e , a ailable e idence
sugges s ha sensi i i y o pes icides does no depend on he clima ic
condi ions (Daam e al., 2008), bu i is a he de e mined by
species-speci ic ai s and he oxicodynamics o he chemical (Van den
Be g e al., 2019). Fo example, Mal by e al. (2005) ound ha HC
5
alues o chlo py i os, eni o hion and ca bo u an ended o he lowe
in opical han empe a e o ganisms, bu he di e ences we e no s a-
is ically signi ican , and Kwok e al. (2007) ound ha empe a e spe-
cies we e mo e sensi i e o ca ba yl, DDT, and mala hion, whe eas
opical species we e mo e sensi i e o chlo py i os.
Despi e he lack o di e ences be ween he sensi i i y o opical and
empe a e species o pes icides, he use o hese pes icides mos likely
has di e en consequences in hese wo zones o he wo ld. This is
because he in ensi e ag icul u al p ac ices in opical coun ies lead o
highe inpu s o pes icides and sp ead o con amina ion o e wa e sheds
(Daam and Van den B ink, 2010), and egula ions o pes icide use a e
o en mo e pe missi e in opical han in empe a e coun ies (Cas illo
e al., 1997). Thus, opical s eams o en each pes icide concen a ions
ha a e much highe han hose in empe a e s eams, wi h mo e se ious
consequences o popula ions and ecosys ems. Un o una ely, opical
da a a e s ill sca ce in he li e a u e, and his p ecludes obus es s, so
ou esul s and hose o p e ious au ho s should be aken wi h cau ion
and be conside ed as p elimina y.
In conclusion, ou s udy demons a es a clea sensi i i y o se e al
in e eb a e species ha a e key o he unc ioning o he s eam
ecosys em o common-use pes icides in he s udy a ea. We also show
ha ex apola ion o esul s om eco oxicological es s wi h D. magna o
o he common es species would unde es ima e he eal e ec s o pes-
icides in opical s eam ecosys ems and communi ies. We highligh he
need o mo e eco oxicological s udies ha use opical aqua ic species
om di e en ophic le els in o de o assess he (Von Fume i and
Blau ock, 2018) ecological isk o pes icide pollu ion in s eam
ecosys ems.
Funding
This wo k was suppo ed by he Na ional Sec e a ia o Science,
Technology and Inno a ion o Panama (SENACYT; p ojec APY-GC-
2018B-052; con ac no. 259-2018) and he Minis y o Economy and
Finance o Panama (MEF; p ojec 019910.001). AC was suppo ed by a
ellowship om SENACYT (con ac no. 001-2015) and by he Na ional
Resea ch Sys em o Panama (SNI; Ph.D. ca ego y; con ac no. 186-
2018). GC was suppo ed by a ellowship om IFARHU-SENACYT
(con ac no. 270-2018-1011).
CRediT au ho ship con ibu ion s a emen
Ayde´
e Co nejo: Concep ualiza ion, Funding acquisi ion, P ojec
adminis a ion, In es iga ion, Supe ision, Me hodology, Da a cu a ion,
Fo mal analysis, W i ing - o iginal d a , W i ing - e iew & edi ing.
F ancisco Encina-Mon oya: Funding acquisi ion, In es iga ion, Me h-
odology, W i ing - e iew & edi ing. F ancisco Co ea-A aneda:
Funding acquisi ion, In es iga ion, Me hodology, W i ing - e iew &
edi ing. Dalys Ro i a: Funding acquisi ion, In es iga ion, Me hodol-
ogy, W i ing - e iew & edi ing. Gab iela Ga cía: In es iga ion, Me h-
odology, Da a cu a ion, Li e a u e e ision, W i ing - e iew & edi ing.
Ca los Nie o: In es iga ion, Da a cu a ion, Li e a u e e ision, W i ing -
e iew & edi ing. Víc o Villa eal: In es iga ion, Me hodology, Da a
cu a ion, Li e a u e e ision. Nicomedes Ja amillo: In es iga ion,
Me hodology, W i ing - e iew & edi ing. Edga P´
e ez: In es iga ion,
Da a cu a ion, Li e a u e e ision. Anayansi Valde ama: In es iga-
ion, Me hodology, Da a cu a ion, W i ing - e iew & edi ing. Ja ie
P´
e ez: Supe ision, In es iga ion, Me hodology, W i ing - e iew &
edi ing. Luz Boye o: Concep ualiza ion, Funding acquisi ion, Supe i-
sion, In es iga ion, Me hodology, W i ing - o iginal d a , W i ing - e-
iew & edi ing.
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Acknowledgemen s
We hank he Panamanian Minis y o En i onmen o hei
au ho iza ion o ca y ou he s udy a he PILA S a ion; B enda Checa
om he Minis y o Ag icul u al De elopmen (MIDA), who led he
RLA7019 P ojec , unded by he In e na ional A omic Ene gy Agency
(AIEA), which suppo ed aining wi h expe s; Anyi Tu˜
non, Be Kolh-
mann, F ancisco Quesada, Jenny Be múdez, Meye Gue a a, Milexi
Molina , Monika Sp inge , Sil ia Eche e ía-S´
aenz, Tom´
as A. Ríos
Gonz´
alez and Yusse Agui e o comple ing he su eys o in e e-
b a e selec ion; Allison Villa eal and Ka ina Co ea o assis ance wi h
in e eb a e sampling and labo a o y bioassays; Ja e h Roman, Rodol o
No elo, Jose Loaiza and Mileika San os o p o iding in o ma ion on
dis ibu ion o in e eb a e species; and wo anonymous e iewe s o
p o iding cons uc i e commen s on he manusc ip .
Appendix A. Suppo ing in o ma ion
Supplemen a y da a associa ed wi h his a icle can be ound in he
online e sion a doi:10.1016/j.ecoen .2021.112226.
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