9
Func ional ai esponses o eme gen and ee- loa ing
Al e nan he a philoxe oides o inc easing salini y wi h sea
le el ise: s ess ole ance, a oidance, and escape s a egies
B enda J. G ewell1, Blanca Gallego-Té a 2, Jesús M. Cas illo2, Ca yn J. Fu ell1, Rebecca E. D eno sky3,
Na han E. Ha ms4, Paul D. P a 5
1 USDA-ARS In asi e Species and Pollina o Heal h Resea ch Uni , Depa men o Plan Sciences MS-4, Uni e si y o Cali o nia, Da is, CA, 95616, USA
2 Depa amen o de Biología Vege al y Ecología, Uni e sidad de Se illa, Ap. 1095, 41080 Se illa, Spain
3 Biology Depa men , John Ca oll Uni e si y, 1 John Ca oll Boule a d, Uni e si y Heigh s, OH 44118-4581, USA
4 US A my Enginee Resea ch and De elopmen Cen e (ERDC), Aqua ic Ecology and In asi e Species B anch, 201 E. Jones S ., Lewis ille, Texas, 75057, USA
5 USDA-ARS In asi e Species and Pollina o Heal h Resea ch Uni , Wes e n Regional Resea ch Cen e , 800 Buchanan S ee , Albany, CA, 94710, USA
Co esponding au ho : B enda J. G ewell ([email p o ec ed])
Copy igh : © B enda J. G ewell e al.
This is an open access a icle dis ibu ed unde
e ms o he C ea i e Commons A ibu ion
License (A ibu ion 4.0 In e na ional – CC BY 4.0).
Resea ch A icle
Abs ac
Sea le el ise is ha ing majo impac s on es ua ies due o salini y in usion. These changes in s ess
p o iles ha e ipple e ec s in ecosys ems, including al e ing he in asibili y o hese we lands depend-
ing on he sal ole ance o he in ading species. Al e nan he a philoxe oides Ma . (G iseb.) (alliga o
weed), na i e o Sou h Ame ica and long ecognized as one o he wo ld’s wo s eshwa e aqua ic
weeds, ecen ly in aded idal we lands in Cali o nia’s San F ancisco Bay–Del a Es ua y. Gene ally
conside ed a eshwa e -limi ed glycophy e, obse a ions sugges ed his in asi e mac ophy e may ha e
some deg ee o salini y ole ance, hough i s deg ee o ole ance and capaci y o sp ead wi h inc eased
salini y in usion we e unknown. In wo ull- ac o ial g eenhouse expe imen s, we assessed esponses
o eme gen (soil- oo ed) and ee- loa ing g ow h o ms o A. philoxe oides o ou salini y concen a-
ions ( eshwa e o euhaline) a he whole-plan (g ow h, biomass p oduc ion and alloca ion, i ness),
physiological, and biochemical le els. We also conduc ed a hi d expe imen explo ing he eco e y po-
en ial o ee- loa ing A. philoxe oides in eshwa e ollowing ex ended exposu e o mesohaline o eu-
haline aqueous salini y. Al hough sensi i i y o A. philoxe oides o inc easing salini y was documen ed,
he su i al o bo h g ow h o ms in he ull ange o salini y ea men s was no able and unexpec ed.
Ou esul s indica e A. philoxe oides is a acul a i e halophy e well adap ed o oligohaline–mesohaline
salini y le els. Resul s also e ealed he in asi e weed’s mul iple s a egies o su i e salini y-induced
physiological s ess, suppo ing i s su i al e en a ele a ed polyhaline o euhaline condi ions. The
mac ophy e exp essed unc ional ai esponses spanning s ess ole ance, a oidance, and escape s a -
egies ha may sus ain i s sp ead as es ua ine salini y in usion inc eases wi h sea le el ise.
Key wo ds: Alliga o weed, Ama an haceae, aqua ic plan s, glycophy e, in asion ecology, in asi e
plan s, plan in asions, idal we lands
In oduc ion
Accele a ed clima e change, concomi an sea le el ise, and inc easing biological
in asions concu en ly a ec coas al species, biological di e si y, and we land eco-
sys em se ices (IPCC 2022; Ho ick e al. 2023). In his con ex , s ess g adien s
Academic edi o : Filipe Ribei o
Recei ed:
14 Feb ua y 2025
Accep ed:
7 Augus 2025
Published:
7 Oc obe 2025
Ci a ion: G ewell BJ, Gallego-Té a B,
Cas illo JM, Fu ell CJ, D eno sky RE,
Ha ms NE, P a PD (2025) Func ional
ai esponses o eme gen and ee-
loa ing Al e nan he a philoxe oides
o inc easing salini y wi h sea le el
ise: s ess ole ance, a oidance, and
escape s a egies. In: Anas ácio P,
Ribei o F, Chainho P (Eds) In asions
in Aqua ic Sys ems. NeoBio a 102:
9–36. h ps://doi.o g/10.3897/
neobio a.102.150325
NeoBio a 102: 9–36 (2025)
DOI: 10.3897/neobio a.102.150325
Ad ancing esea ch on alien species and biological in asions
A pee - e iewed open-access jou nal
NeoBio a
10
NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
in es ua ies a e apidly changing due o global wa ming and sea le el ise, esul ing
in spa ial and empo al shi s in salini y (He and Silliman 2019; Zhu e al. 2022).
In a ec ed a eas, hese no el condi ions can al e he dis ibu ion and sp ead o
es ua ine ege a ion and o he o ganisms, including non-na i e species, ul ima ely
yielding unp edic able ou comes o na i e species (Rubino and G osholz 2022).
The pe ennial aqua ic he b Al e nan he a philoxe oides Ma . (G iseb.) (alliga o
weed; Ama an haceae) is endemic o sou he n Sou h Ame ica (Vog e al. 1979; Sosa
e al. 2004). I is conside ed one o he ele en mos p oblema ic in asi e aqua ic
plan species in eshwa e habi a s globally (F ancis 2012), ha ing na u alized in
32 coun ies ac oss he Ame icas, Wes e n Eu ope, Asia, and Oceania (Tan ee e
al. 2018; EPPO 2024). Al hough gene ally ega ded as a glycophy e (i.e., a plan
species limi ed o eshwa e o low-sodium soils; Daubenmi e 1947), A. philoxe oi-
des has ecen ly been obse ed in mo e saline en i onmen s (Walden e al. 2019).
Glycophy es a e hough o ha e e ol ed in ecosys ems wi h low soil sodium – ye
some can de elop sal - ole an mechanisms h ough adap a ion unde na u al selec-
ion p essu es (Ho ie e al. 2012; Cheeseman 2015). Limi ed anecdo al epo s o A.
philoxe oides in saline habi a s (Gangs ad 1978; U.S. Fish and Wildli e Se ice 2018)
sugges ha a leas some lineages may ha e de eloped a deg ee o sal ole ance.
In 2017, he i s pa ches o A. philoxe oides we e de ec ed in idal we lands o
he b ackish Suisun Ma sh each o he San F ancisco Bay–Del a Es ua y, ollowed
by i s sp ead in o he inland idal eshwa e Del a (Walden e al. 2019). This un-
expec ed appea ance in b ackish a eas aised ques ions abou i s abili y o ole a e
changing salini y egimes associa ed wi h seawa e in usion. G ea e sal s ess
caused by seawa e in usion may hinde expansion o lead o die-back o esh-
wa e plan s in idal we lands (C a e al. 2009; Thou eno and Thiébau 2018),
al e ing na i e ege a ion pa e ns and c ea ing oppo uni ies o in asion by alien
plan species (Humph eys e al. 2021).
These plan in asions and hei ecological e ec s a ise om changing en i on-
men al condi ions and co esponding shi s in plan unc ional ai esponses
(D eno sky e al. 2012). A la ge me a-analysis sugges s ha aqua ic alien plan s al-
e hei unc ional ai s in esponse o global change ac o s mo e ac i ely han na-
i e species, which accele a es hei sp ead in o new a eas (So e e al. 2013; Wu and
Ding 2019). Imp o ed unde s anding o how plan unc ional ai s suppo he
s ess esponse s a egies o in asi e species is essen ial o mi iga ing hei impac s.
Plan esponses o sal s ess can be ca ego ized in o ou main s a egies: ole -
ance, a oidance, escape, and eco e y (Munns 2002; Slama e al. 2015; Shelake e
al. 2022). Tole ance may in ol e a slowe g ow h a e (Voesenek and Bailey-Se es
2015; Zhang e al. 2020), p oduc ion o compa ible solu es o main ain osmo ic bal-
ance, and gene a ion o an ioxidan enzymes (Pungin e al. 2023; Huang e al. 2024).
A oidance mechanisms educe sal up ake h ough s oma al closu e and lea wax ac-
cumula ion, while succulence inc eases lea hickness o cell size and p omo es wa e
s o age o dilu e and seques e oxic ion concen a ions o suble hal le els (Mann e
al. 2023; Pé ez-López e al. 2023). Escape mechanisms may include sho ened li e
cycles o enable ea ly ep oduc ion o ai s ha p omo e dispe sal away om s ess
(Ca o d and Jansson 2014), high pho osyn he ic capaci y, emobiliza ion o assimi-
la es o s o age o gans (Tang e al. 2022), and clonal plas ici y (Puijalon e al. 2008).
Reco e y mechanisms include cellula damage epai , s ess memo y o ma ion, p o-
line accumula ion, and es o a ion o hyd oly ic condi ions o enable plan s o egain
i ness and g ow h (Gup a and Huang 2014; Shelake e al. 2022).
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NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
To da e, esea ch in o he salini y esponses o A. philoxe oides has been limi ed.
Mos p e ious wo k ocused on pho osyn he ic me abolism and g ow h esponses in
cell-suspension cul u es (Longs e h e al. 1984; Mudalige and Longs e h 2006) o
on g ow h and gas exchange in in ac young plan s (Ja ed e al. 2019). A ecen expe -
imen e alua ing limi ed whole-plan esponses – g ow h a e and oo e sus shoo
biomass – a salini y le els anging om 0.2 o 20 pa s pe housand (pp ) ac oss 14
aqua ic species in Flo ida ound ha A. philoxe oides su i ed a 20 pp (Too oonchi
e al. 2023). He e, using h ee g eenhouse expe imen s, we assessed how unc ional
ai s a y in esponse o inc easing salini y in he in asi e plan A. philoxe oides and
how ai esponses di e be ween i s eme gen and ee- loa ing g ow h o ms. Ou
speci ic objec i e was o e alua e plan ai esponses o ou salini y le els ( esh-
wa e o seawa e ) a he biochemical, physiological, and whole-plan le els in wo
con as ing g ow h o ms – eme gen and ee- loa ing – in o de o unde s and how
hese ai s con ibu e o sal s ess s a egies anging om escape o ole ance (sensu
Neg ão e al. 2017). We hypo hesized ha inc easing salini y would lead o changes
in g ow h, physiological, and biochemical ai s ha suppo su i al and sus ained
in asi eness, and ha hese esponses would a y by g ow h o m. We p edic ed ha
belowg ound ca bon ese es in he soil-ancho ed eme gen o m would suppo
g ea e su i al h ough ole ance o a oidance s a egies, o bo h. In con as , we
p edic ed ha he ee- loa ing o m would lack he capaci y o su i e o main ain
igo unde high salini y, he eby a o ing a apid escape s a egy. Ou o e all aim
was o imp o e unde s anding o he unc ional ai s o each g ow h o m in ela ion
o he po en ial o ange expansion and pe sis ence o A. philoxe oides. This wo k is
pa icula ly ele an in he con ex o ising es ua ine salini y wi h sea le el ise and
has impo an implica ions o in asi e species managemen s a egies.
Ma e ials and me hods
Focal species
Al e nan he a philoxe oides is a c eeping eme gen aqua ic species (sensu Rejmánko á
1992) ha sp ou s and eme ges om belowg ound bud banks and g ows apidly o
o m long buoyan shoo s ha sp ead on he wa e su ace and wi hin he wa e col-
umn. A. philoxe oides ypically g ows as soil- oo ed eme gen plan s in well-d ained,
shallow aqua ic o e es ial eco ones (Julien and Bou ne 1988) and accumula es
ca bohyd a e s o age ese es in woody ap oo s suppo ing g ow h (Julien e al.
1992; Jia e al. 2009, 2010). In hese high in e idal zones, he eme gen g ow h
o m o A. philoxe oides g ows e ically (> 2 m), o en pa ially suppo ed by o he
all eme gen mac ophy es. High gene ic a iabili y suppo s i s success as a weed
in bo h i s na i e and na u alized anges (Jia e al. 2010). Al hough i s g ow h a e
and sp ead a e g ea es in aqua ic we land habi a s, he eme gen g ow h o m o A.
philoxe oides has also agg essi ely in aded adjacen e es ial a eas, including pas-
u es, o cha ds, and c ops (Shen e al. 2005; Xie e al. 2010; Tan ee e al. 2018).
Less common, ye ecologically signi ican , a e ee- loa ing plan s ha can o m la ge
pa ches o hick in e wo en ma s (Julien e al. 1992). F ee- loa ing clonal ame s a e
also hyd ocho ous dispe sal uni s, ep esen ing he p ima y mode o sp ead h ough-
ou i s na i e and na u alized anges (Sosa e al. 2004, 2008). The highly b anching
a chi ec u e o A. philoxe oides, leading o inc eased ma ing on he wa e su ace, can
esul in mo e clonal p opagules o dispe sal, as he hollow s ems o A. philoxe oides
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NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
a e p one o b eakage and dislodge om es ablished ma s in esponse o dis u bance
(Ha ms e al. 2023). Following agmen a ion, ca bohyd a e s o age in in e nodes and
lea es can suppo he su i al o ee- loa ing shoo s (Dong e al. 2010).
Expe imen al plan ma e ial
Al e nan he a philoxe oides plan s o a single haplo ype and ploidy le el (Ap2, hexa-
ploid; Williams e al. 2020) in ading no he n Cali o nia and he San F ancisco
Bay–Del a Es ua y (SFE) we e used o each expe imen . Visibly undamaged api-
cal shoo agmen s (50 cm long, n = 150) om eme gen loa ing-lea ed shoo s
g owing o e he wa e su ace we e andomly collec ed om widely sepa a ed
poin s along an in aded each o he Fea he Ri e (39.456505, –121.633851),
a eshwa e ibu a y o idelands o he SFE. Collec ed shoo agmen s we e
ca e ully placed in coole s illed wi h cold i e wa e and anspo ed o he US-
DA-ARS Aqua ic Weed Resea ch Facili y a he Uni e si y o Cali o nia, Da is.
A he labo a o y, shoo cu ings we e cleaned, insed in deionized (DI) wa e ,
and loa ed in shallow 190-li e anks (132 cm long × 39 cm wide × 30 cm deep;
Rubbe maid®, A lan a, Geo gia, USA) illed wi h DI wa e plus a nu ien solu ion
addi i e (10% Hoagland mac o/20% mic o/i on solu ion) o a 30-day eco e y
pe iod p io o expe imen al se up.
Expe imen al se ups
Two independen expe imen s (A: eme gen ; B: ee- loa ing g ow h o ms) we e
es ablished due o space equi emen di e ences o g owing he con as ing li e
o ms. Me hods s anda dized be ween he expe imen s ollow. To e alua e A.
philoxe oides esponses o salini y, mesocosms we e andomly assigned o one o
ou aqueous salini y ea men s (0.5 pp [ eshwa e /low oligohaline], 12 pp [me-
sohaline], 24 pp [polyhaline], and 36 pp [euhaline, “ma ine”]) using sea sal s
(Ins an Ocean®, Aqua ium Sys ems Inc., Men o , Ohio, USA). Each ea men
was es ablished in a 75.7-li e plas ic mesocosm (U ili ub Model 14, E. L. Mus ee
& Sons, B ook Pa k, Ohio, USA) illed wi h 45 li e s o DI wa e and sea sal s o
achie e a ge salini ies. Mesocosm posi ions we e andomly assigned on g een-
house benches. F eshwa e ea men s we e main ained a 0.5 pp salini y. T ea -
men s > 0.5 pp we e amped up g adually o e condi ioning in e als o a oid
osmo ic shock, wi h salini y adjus ed as needed. Sea sal s we e s i ed di ec ly in o
each ub, wi h inc emen al weekly inc eases un il he a ge mesohaline, polyhaline,
and euhaline salini ies we e achie ed ( h ee o ou weeks o euhaline). Salini y
o each ea men was moni o ed using a YSI P o30 Conduc i i y/Salini y Me e
(Yellow Sp ings Ins umen s, Inc., Yellow Sp ings, Ohio, USA). Speci ic conduc-
ance eadings we e aken weekly, and ocean sal s we e added as needed o main ain
le els. Ai bubble s wi h 5/32˝ ubing (Model 9720, Pen ai Aqua ic Eco-sys ems,
Ca y, No h Ca olina, USA) we e ins alled o ci cula e wa e , supp ess algal g ow h,
and homogenize gas concen a ions ac oss salini y ea men s, ensu ing alid com-
pa isons. Con olled glasshouse condi ions included 21–27 °C ai empe a u e and
app oxima ely 1300 μmol m−2 s−1 maximum pho on lux densi y a canopy le el
(LI-COR LI-250A ligh me e , LI-COR Inc., Lincoln, Neb aska, USA). A e ull
ea men es ablishmen , su i o ship o plan s was eco ded weekly un il ini ia ion
o inal p e- and pos -ha es measu emen s o plan unc ional ai s.
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NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
Expe imen A: eme gen g ow h o m
Fo he eme gen , soil-ancho ed g ow h o m ea men , single agmen s o equi a-
len mass ange, leng h, and numbe o s em nodes we e selec ed om cul u e s ock.
Shoo agmen s we e immed o 40 cm in leng h. The esh weigh o he ini ial
20 shoo agmen s was 10.5 ± 0.2 g (mean ± SE), wi h 5–7 s em nodes pe plan .
Each single agmen was ansplan ed in o a bulb pan (12.5 cm heigh × 25 cm di-
ame e ) illed wi h a cus om soil mix o mode a e nu ien a ailabili y, e lec ing soil
bulk densi y and nu ien concen a ions measu ed in 45 samples om 24 A. philox-
e oides in asion s udy si es in Suisun Ma sh, SFE. The soil mix was composed o
40% opsoil, 40% humus, and 20% sand, wi h 30 pp C, 1.9 pp N, and 305 ppm
P. In each expe imen al po , a single shoo agmen was plan ed wi h he lowe 10
cm – bea ing wo s em nodes – bu ied benea h he soil su ace o acili a e soil oo
de elopmen , and 30 cm o each agmen , wi h app oxima ely ou s em nodes,
was le eme gen abo e he soil. The po s we e ele a ed on small b icks (6 cm all)
wi hin each mesocosm (n = 5 eplica es pe salini y ea men ), so ha he soil su -
ace emained subme ged 4 cm below he wa e le el. Du ing he 5-day ansplan
adjus men pe iod, plan s we e e ilized wi h 10% Hoagland mac o/20% mic o/
i on nu ien solu ion. Eme gen plan s we e exposed o he inal salini y ea men s
o 42 days, and he en i e expe imen las ed 62 days be o e ha es .
Expe imen B: ee- loa ing li e o m
Shoo cu ings o equi alen mass ange, leng h, and numbe o s em nodes we e
selec ed om cul u e s ock, hen immed o 45 cm, weighed, and measu ed. The
esh weigh o he ini ial 72 cu ings was 11.6 ± 0.2 g (mean ± SE), wi h 5–9 s em
nodes and 0–3 small b anches pe shoo . Because loa ing ma s o alliga o weed
in na u e ypically include mo e han a single agmen , es ablishmen was s an-
da dized wi h h ee loa ing shoo agmen s in each mesocosm. Mesocosms (n =
24) we e andomly assigned o one o ou salini y ea men s (n = 6 eplica es pe
ea men ), and cu ings we e loa ed on he wa e su ace in 45 L o solu ion pe
mesocosm. Du ing he 5-day condi ioning pe iod be o e salini y amp-up, plan s
we e e ilized wi h 25% Hoagland mac o/50% mic o/i on nu ien solu ion. Ex-
pe imen al plan s we e hen exposed o one o ou aqueous salini y ea men s
(0.5, 12, 24, o 36 pp ) and e ilized wi h 50% Hoagland mac o/100% mic o/
i on nu ien solu ion added o he wa e . Plan s we e exposed o he inal salini y
ea men s o 25 days, and he en i e expe imen las ed 51 days be o e ha es .
Expe imen C: ee- loa ing salini y wi h eshwa e eco e y phase
Six y shoo cu ings we e collec ed wo weeks ollowing he ha es o Expe imen
B, om he same sou ce popula ion desc ibed o he ini ial wo expe imen s. Shoo
cu ings we e immed o 45 cm in leng h, weighed, and measu ed. The esh weigh
o he ini ial 36 cu ings was 18.5 ± 0.2 g (mean ± SE), wi h 6–7 s em nodes and
0–3 small b anches pe plan . Th ee cu ings we e andomly assigned o each ex-
pe imen al uni (mesocosm), using he p e iously desc ibed salini y amp-up me h-
ods. Gi en changes in day leng h, sola ligh was supplemen ed in he mo ning (6
a.m.–10 a.m.) using high-in ensi y discha ge ligh s (GE Lucalox LU1000/ECO
HPS 1000 W, PARsou ce, Pe aluma, Cali o nia, USA). Expe imen al eplica es
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NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
we e andomly assigned o one o h ee aqueous salini y ea men s (12, 24, o 36
pp ; n = 4 eplica es pe ea men ) and e ilized wi h 50% Hoagland mac o/100%
mic o/i on nu ien solu ion. Following a ou -week amp-up pe iod, salini y ea -
men s we e main ained o 21 days. F eshwa e eco e y was ini ia ed by g adually
amping down salini y o inal alues o 0.5, 3, and 4.5 pp (o e a h ee-week
amp-down pe iod). Plan s we e allowed o eco e unde eshwa e condi ions o
32 days, and he en i e expe imen las ed 80 days be o e ha es .
P e-ha es measu emen s: expe imen s A and B
Th ee days be o e ha es , pho osyn he ic a e (A) and s oma al conduc ance (gs)
we e measu ed using an LI-COR 6400 XT po able in a ed CO2 gas analyze
(LI-COR Biosciences, Lincoln, Neb aska, USA) in di e en ial mode and open
ci cui . Th ee subsamples we e eco ded a 10-second in e als o each plan and
a e aged be o e analysis. The LI-COR 6400 XT used a ed–blue LED ligh sou ce
gene a ing ac inic ligh , and chambe condi ions we e se a 1000 μmol m−2 s−1
pho on lux densi y, 400 μmol s−1 low a e, and 400 μmol mol−1 CO2. In insic
wa e use e iciency (iWUE) was calcula ed om simul aneous measu emen s o A
and gs. All measu es we e conduc ed on a sunny day wi hin 2 h o sola noon. Gas
exchange was measu ed on all plan s in he eme gen expe imen bu only on he
0.5 pp salini y ea men in he ee- loa ing expe imen . Measu emen s in he 12,
24, and 36 pp ea men s o he ee- loa ing expe imen could no be conduc ed
due o he absence o sui able li e lea es abo e he wa e su ace.
Pos -ha es measu emen s: expe imen s A and B
Biomass p oduc ion and alloca ion
All lowe s we e emo ed om he plan s and collec ed o d y weigh (DW) mea-
su emen . Li e lea es we e collec ed and quan i ied o o al lea a ea (m2) using
image analysis so wa e (WinFOLIA 2009). A subse o ully expanded lea es was
e alua ed wi h WinFOLIA and used o calcula e speci ic lea a ea (SLA; m2 kg−1).
Each expe imen al plan was ha es ed, sepa a ing he biomass in o ac ions: e-
p oduc i e pa s, lea es, p ima y s ems, b anch s ems, soil oo s, and ad en i ious
oo s. Fo he eme gen expe imen , he belowg ound biomass – including soil
oo s and he bu ied oo c own om which he s em a ises – was sie ed om he
soil mix, collec ed, and cleaned. Each biomass ac ion was d ied a 70 °C o 48
h, and biomass alloca ion and o al biomass we e calcula ed. Mass da a we e used
o calcula e ela i e g ow h a e (RGR; g day−1), lea mass a io (LMR), shoo mass
a io (SMR), and ad en i ious oo mass a io (ARMR). Belowg ound alloca ion
(%) was also calcula ed o he eme gen g ow h o m.
S em a chi ec u e and mo phology ai s
S em hollow pi h ca i y (SPC) diame e was measu ed as s em wall and pi h (spongy
ae enchyma cells) hickness ela i e o he wid h o he s em’s hollow cen e . Pi h
ca i y size is ecologically ele an as habi a and o pupal-s age su i al o po en ial
biological con ol insec s (Li and Ye 2006; Geng e al. 2007). SPC diame e s we e
measu ed on h ee s em sec ions om each plan and a e aged be o e analysis. Each
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sec ion was aken om a di e en shoo and cu a he in e node below he six h
node om he apical ip. Fo he eme gen g ow h o m, he p ima y s em leng h
was measu ed om he soil su ace. B anches we e sepa a ed om he p ima y s em,
d ied sepa a ely, and used o calcula e he b anch in ensi y index (BI; a io o b anch
d y weigh o s em d y weigh ; Liu e al. 2018). P ima y s em leng h was also used
o calcula e he shoo elonga ion a e (SER; cm day−1). P ima y s em leng h and BI
could no be measu ed in he ee- loa ing g ow h o m, as he h ee ini ial shoo s in
each expe imen al uni could no longe be isola ed om one ano he .
Plan chemis y ai s
A subsample o 2–6 esh lea es was collec ed and ozen a ha es . P oline concen a-
ion was de e mined ollowing Ba es e al. (1973). Lea samples we e ex ac ed in 80%
aqueous ace one, and supe na an s om cen i uged ex ac s we e used o de e mine
chlo ophyll (Chl) a, Chl b, and ca o enoid (Ca ) concen a ions using a spec opho-
ome e (Beckman DU-730, Beckman Coul e , B ea, Cali o nia, USA), ollowing
Lich en hale (1987). D y lea issue was g ound o pass h ough a No. 40 mesh sie e
p io o measu emen o o al ni ogen (N), sodium (Na), glycinebe aine, o al phe-
nolics, and lignin concen a ions. D y, g ound s em node issue om bo h g ow h
o ms and belowg ound oo s ex ac ed om he soil in he eme gen expe imen we e
analyzed o o al N, lignin, and o al non-s uc u al ca bohyd a e (TNC; e.g., soluble
suga s and s a ch) concen a ions. To al N concen a ion was measu ed using a Pe -
kin Elme 2400 CHNS/O analyze (Pe kin Elme , Wal ham, Massachuse s, USA).
Sodium concen a ion was de e mined using an O ion ROSS™ sodium ISE elec ode
(The mo Scien i ic, Be e ly, Massachuse s, USA) on d y-ashed samples dissol ed in
1 M hyd ochlo ic acid. Glycinebe aine was es ima ed as qua e na y ammonium com-
pounds ollowing G ie e and G a an (1983). To al phenolics we e measu ed using
spec opho ome ic de ec ion ollowing eac ion wi h Folin–Ciocal eu eagen and so-
dium ca bona e solu ion (Single on e al. 1999). Lea and s em lignin we e measu ed
only o he eme gen g ow h o m using he ace yl b omide assay (Ha ield e al.
1999). TNC concen a ion was de e mined using a phenol–sul u ic acid assay o e-
ducing suga s ollowing e hanol ex ac ion, wi h colo ime ic de e mina ion o s a ch
esidue a e enzyma ic diges ion (Chow and Landhäusse 2004; Quen in e al. 2015).
Pos -ha es measu emen s: expe imen C
Biomass p oduc ion and alloca ion
Each expe imen al plan was ha es ed, sepa a ing he biomass in o ac ions: e-
p oduc i e pa s, lea es, s ems, and ad en i ious oo s. Each biomass ac ion was
d ied a 70 °C o 48 h, and biomass alloca ion and o al biomass we e calcula ed.
Mass da a we e used o calcula e ela i e g ow h a e (RGR; g day−1), lea mass a io
(LMR), shoo mass a io (SMR), and ad en i ious oo mass a io (ARMR).
S em a chi ec u e and mo phology ai s
To al s em diame e and SPC diame e we e measu ed on h ee s em sec ions om
each plan and a e aged be o e analysis. S em sec ions we e selec ed using he same
p o ocol p e iously desc ibed.
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
Plan chemis y ai s
S em node issue was g ound o pass h ough a No. 40 mesh sie e p io o mea-
su emen o N and TNC concen a ions using p e iously desc ibed p o ocols.
S a is ical analysis
All analyses we e conduc ed in R so wa e (R-Co e Team 2021). Co ela ion anal-
ysis o mul iple independen esponse a iables was pe o med o iden i y and
elimina e highly co ela ed a iables ha could educe he s a is ical powe o sub-
sequen analyses. Thi een highly co ela ed a iables ( > 0.90) – including ela-
i e g ow h a e, shoo elonga ion a e, AGB, BGB, lea , s em, ep oduc i e and
ad en i ious oo biomasses, lea a ea, shoo mass a io, s em and SPC diame e ,
and s oma al conduc ance – we e conside ed edundan and emo ed om he
s a is ical models o eme gen plan s. Plan ai esponses o salini y ea men s in
eme gen plan s we e ca ego ized in o h ee unc ional g oups o subsequen s a-
is ical analysis: (1) biomass alloca ion and mo phology ( o al plan biomass, SLA,
LMR, ad en i ious oo mass a io, belowg ound mass a io, and BI); (2) lea gas
exchange and pho osyn he ic pigmen s (A, iWUE, Chl a, Chl b, and Ca concen-
a ions); and (3) plan issue chemis y ( olia N, Na, p oline, glycinebe aine, o al
phenolic compounds, and lignin concen a ions; s em lignin concen a ion; and
s em node and soil oo N and TNC concen a ions). Fo ee- loa ing plan s, en
highly co ela ed ai s – ela i e g ow h a e, lea , s em, ep oduc i e and ad en i-
ious oo biomasses, lea a ea, shoo mass a io, s em diame e , Ca concen a ion,
and lea Na concen a ion – we e excluded. The 13 selec ed ai s o ee- loa ing
plan s we e g ouped as ollows: (1) biomass alloca ion and mo phology ( o al plan
biomass, SLA, LMR, ad en i ious oo mass a io, and SPC diame e ); and (2)
plan issue chemis y ( olia Chl a, Chl b, N, p oline, glycinebe aine, and o al
phenolic compound concen a ions; and s em node N and TNC concen a ions).
Fo each expe imen , mul i a ia e analysis o a iance (MANOVA) and Ho-
elling–Lawley’s ace we e used o compa e mean alues o each g oup o plan
ai s in esponse o salini y ea men s. Mul i a ia e analysis o a iance p o ec s
agains ype I e o (Scheine 2001). Once mul i a ia e signi icance was con i med
ia MANOVA, main uni a ia e di e ences o each plan ai we e assessed using
Gene al Linea Models (GLMs), wi h Tukey’s es used as a pos hoc analysis. The
assump ions equi ed o pa ame ic es s we e analyzed by plo ing s anda dized
esiduals agains i ed alues and p edic o a iables using he DHaRMa package
(Ha ig 2022). To mee he assump ions, he a iable biomass o he ee- loa ing
plan s (Expe imen B) was squa e- oo ans o med.
Fo he expe imen al esul s o he eme gen and he ee- loa ing plan s, we
i ed piecewise s uc u al equa ion models (SEM) in R using he piecewise-SEM
package (Le check 2016) o es o di ec and indi ec e ec s o he mos im-
po an a iables, using salini y as he only exogenous a iable. S uc u al equa ion
models a e known o be da a demanding and ypically equi e la ge sample sizes o
s able and gene alizable es ima es (G ace e al. 2010). We selec ed piecewise SEM
o e adi ional SEM because i allows o he use o models wi h non-no mal e o
s uc u es – which a e common in ecological da a – and o e s g ea e lexibili y in
model speci ica ion. Mo eo e , piecewise SEM is gene ally mo e ole an o mod-
e a e sample sizes, which applies o ou design (n = 20; i e eplica es ac oss ou
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
salini y le els) (Le check 2016). This model can p o ide insigh s in o he causal
ela ionships among unc ional ai s unde salini y s ess, hough he mode a e
sample size should be conside ed when in e p e ing he s eng h and gene ali y o
some pa hway es ima es. Ne e heless, he applica ion o piecewise SEM enables
explo a ion o hese ela ionships wi hin he cons ain s o ou expe imen al de-
sign (Le check 2016). To cons uc he model, we combined 11 gene alized linea
models o expe imen A and 18 models o expe imen B, wi h he alidi y o
assump ions e alua ed using he DHARMa package (see abo e), and applied neces-
sa y ans o ma ions. The models, concep ually based on mul i-equa ional analyses
o dependency o co ela ion be ween a iables (G ace e al. 2010), we e used o
explo e how di e en unc ional plan ai s in e ela e, suppo plan esponses o
salini y s ess, e eal cascading e ec s o inc easing en i onmen al s ess on plan s
o he di e en g ow h o ms, and iden i y he ela i e impo ance o causal e-
la ionships among a iables. We de eloped ou causal models a p io i based on
heo e ical insigh s and p edic ed ela ionships (Suppl. ma e ial 1: ig. S1). Fo each
expe imen , he ini ial SEM was e alua ed using a D-sepa a ion es o iden i y
missing connec ions, and he o e all model was hen es ed wi h Fishe ’s C s a is ic,
whe e a non-signi ican p- alue implies a well- i ing model. Di ec , indi ec , and
o e all associa ions we e assessed as s anda dized pa ial eg ession coe icien s wi h
he semE package (Mu phy 2022). To cha ac e ize he s a egies used o deal wi h
sal s ess by bo h A. philoxe oides g ow h o ms, unc ional ai esponses included
in piecewise SEM models as di ec and indi ec e ec s ela ed o salini y we e clas-
si ied in o each o he main s a egies: ole ance, a oidance, and escape.
Resul s
All plan unc ional ai g oups e ealed signi ican esponses o salini y o bo h
eme gen and ee- loa ing A. philoxe oides plan s (MANOVA, Table 1; Suppl. ma-
e ial 1: able S1).
Table 1. Ho elling–Lawley’s ace, F-s a is ic, deg ees o eedom, and p- alues om MANOVAs
o ai esponse g oups om expe imen A: eme gen plan s and expe imen B: ee- loa ing plan s
o Al e nan he a philoxe oides exposed o ou aqueous salini y concen a ions (0.5, 12, 24, 36 pp ).
Signi ican alues (p < 0.05) a e ma ked in bold.
Fac o s Ho elling-Lawley’s T ace F DF p
Expe imen A: eme gen plan s
Biomass and mo phology 149.53 80.305 18 <0.0001
Gas exchange and pigmen s 25.556 18.173 15 <0.0001
Plan issue biochemis y 136.92 19.363 33 <0.0001
Expe imen B: ee- loa ing plan s
Biomass and mo phology 194.81 190.48 15 <0.0001
Plan issue biochemis y 145.1 70.536 24 <0.0001
S ess ole ance ai esponses o salini y
In esponse o salini y s ess, a ole ance s a egy was e lec ed in 12 ai esponses o
eme gen A. philoxe oides plan s. To al biomass o eme gen plan s in mesohaline sa-
lini y dec eased by 78% compa ed o he eshwa e con ol, whe eas plan s in poly-
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
he eme gen g ow h o m e lec a classic s ess ole ance s a egy (Shelake e al.
2022) ha was media ed in ou s udy by dec easing le els o pho osyn he ic pig-
men s (Ash a and Ha is 2013). Diminishing pho osyn he ic p o ein le els and
inc easing da k espi a ion a es also ha e been documen ed as unc ional ai
Figu e 5. Resul s om he s uc u al equa ion model (SEM) showing he main ela ionships be ween me ics o unc ional ai espons-
es and salini y o he ee- loa ing g ow h o m o Al e nan he a philoxe oides (Expe imen B; n = 20, i e eplica es ac oss ou salini y
le els). The a iable in g ey ep esen s he main explana o y a iable (salini y), and he esponse a iables a e enclosed in hollow boxes.
Black a ows indica e posi i e causal links, and ed a ows indica e nega i e causal links. Double-headed a ows ep esen co ela ions.
S anda dized pa ame e es ima es (β) a e shown nex o each a ow and a e p opo ional o he hickness o he lines. The coe icien o
de e mina ion (R2) is shown in pa en heses o each esponse a iable. S a is ical powe is indica ed by he Fishe ’s C s a is ic, p- alue (P),
and deg ees o eedom (d ). The able shows he indi ec e ec s o p edic o s on esponse a iables h ough media o s, along wi h hei
co esponding s anda dized es ima es. Sal s ess esponse s a egies included: ole ance (blue), a oidance (o ange), and escape (g een).
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
esponses ela ed o educed ne pho osyn he ic a es unde salini y s ess in A.
philoxe oides (Longs e h e al. 1984; Mudalige and Longs e h 2006). A sal - ol-
e an s a egy also was e lec ed in inc easing accumula ion o o ganic osmoly es
by bo h g ow h o ms. P oline and glycinebe aine accumula ion a e well-known
mechanisms plan s use o main ain osmo ic balance o alle ia ion o salini y s ess
(Gup a and Huang 2014), as p e iously epo ed o A. philoxe oides (Longs e h e
al. 2004; Islam e al. 2019). S em node TNC in eme gen plan s was no a ec ed
by salini y, bu i dec eased wi h inc easing salini y in ee- loa ing plan s, sugges -
ing mobiliza ion o s o age ese es o su i e in ha sh condi ions.
S ess a oidance ai s
Eme gen and ee- loa ing g ow h o ms o A. philoxe oides exp essed compa able
a oidance esponses o sal s ess. They p oduced hicke , succulen lea es o dilu e
sal concen a ions and alloca ed less biomass o ad en i ious oo s wi h inc eas-
ing salini y, po en ially educing sal up ake (Ka lo a e al. 2021). Mo eo e , we
eco ded inc easing s em lignin accumula ion o eme gen plan s in esponse o
inc easing sal s ess, yielding hicke , ha dened s ems wi h educed pi h ca i ies
mo e ypically obse ed in A. philoxe oides in e es ial habi a s (Vog 1973). Al-
hough inc eased s em lignin would p omo e issue impe meabili y and he eby
educe Na up ake and wa e loss (Du e al. 2024), i may educe success o biolog-
ical con ol, as plan s wi h hin, hollow s ems a e needed o success ul pupa ion
by he lea bee le, A. hyd ophila (Sosa e al. 2008).
S ess escape ai s
Func ional ai esponses o salini y suppo ed al e na i e s ess escape s a egies
o eme gen A. philoxe oides, whe eas he ee- loa ing g ow h o m had a much
mo e limi ed capaci y o coun e sal s ess. Roo in es men may suppo accu-
mula ion o non-s uc u al ca bohyd a e s o age ese es in esponse o sal s ess
(Gup a and Huang 2014). In ou s udy, oo ed plan s inc eased hei sub e anean
TNC ese es in esponse o sal s ess, a esponse no a ailable o ee- loa ing
plan s. Realloca ion o hese s o ed assimila es om belowg ound s o age o gans
p o ides ene gy o s ess escape and suppo s esp ou ing du ing eco e y om
salini y exposu e. TNC ese es may also be s o ed in s em node issues o loa -
ing s oloni e ous shoo s ha can in luence es ablishmen success o loa ing ame
agmen s (Dong e al. 2011; Suzuki and S ue e 1999). In ou esul s, s em node
TNC in eme gen plan s was no a ec ed by salini y, hough i dec eased wi h
inc easing salini y in ee- loa ing plan s, e lec ing ha hey we e mobilizing hese
s o age ese es o escape and su i e in ha sh condi ions. Ca bohyd a e s o age
pa e ns can a y g ea ly among seasons, g ow h o ms, and li e his o y s ages in
coas al aqua ic mac ophy es (Lamme an e al. 2024), highligh ing he impo ance
o conside ing di e ences in s ess esponses among g ow h o ms.
T ai esponses o salini y di e be ween g ow h o ms
Like A. philoxe oides, o he ma - o ming, soil- oo ed, eme gen mac ophy es (e.g.,
My iophyllum aqua icum Vell. (Ve dc.); pa o ’s- ea he ; Ludwigia peploides (Kun h)
P.K. Ra en and o he wa e p im oses), o ee- loa ing species (e.g., Eichho nia c assipes
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
(Ma ius) Solms; wa e hyacin h; Pis ia s a io es L.; wa e le uce) exhibi bo h eme -
gen and ee- loa ing s a egies. To da e, expe imen s e alua ing salini y e ec s on such
mac ophy es ha e s udied single g ow h o ms wi hin a species, po en ially mis ep e-
sen ing s ess ole ance o species ha shi be ween al e na e g ow h o ms (Mo ei a e
al. 2023). O e all, ou esul s indica e ee- loa ing A. philoxe oides expe ienced g ea e
dele e ious e ec s wi h inc easing salini y han he eme gen g ow h o m. The highe
capaci y o eme gen A. philoxe oides o sus ain salini y s ess appea ed o be op imal
in mesohaline (12 pp ) condi ions. Eme gen plan s eached he lowe ing li e s age
and p oduced highe biomass han ee- loa ing plan s in polyhaline o euhaline con-
di ions. In ou eco e y expe imen , mos o he ee- loa ing A. philoxe oides plan s
we e able o su i e e en in euhaline condi ions o 21 days, and hey always e ained
some ad en i ious oo s. Howe e , hei biomass was e y low a 24–36 pp (< 1 g),
sugges ing e y limi ed capaci y, i any, o eco e in eshwa e condi ions a e high
salini y exposu e. Ne e heless, ee- loa ing plan s we e able o lowe in eshwa e
condi ions a e being exposed o 12 pp , a signal o eco e y om sal s ess in b ackish
condi ions. In ligh o hese eco e y esul s, he escape s a egy om sal s ess by ag-
men a ion o ee- loa ing ame s de ached om eme gen plan s could be success ul
i dispe sal o loa ing s ems o low salini y wa e occu s wi hin a ew weeks ollowing
exposu e o de imen ally b ackish salini y condi ions.
Implica ions o bio ic s ess (he bi o y) ole ance
Gi en he high gene ic di e si y o non-na i e A. philoxe oides ac oss he U.S. ange
(Williams e al. 2020) and an incomple e unde s anding o sal ole ance h esh-
olds and mechanisms unde lying esponses o con as ing g ow h o ms o in asi e
A. philoxe oides o inc easing salini y s ess, a comp ehensi e esea ch app oach was
needed o unde s and he isk o ange expansions and suppo clima e adap i e
managemen plans in he con ex o sea le el ise. Biological con ol o A. philox-
e oides by he Agasicles hyg ophila Selman & Vog bee le has been highly success ul
in eshwa e we lands h oughou he sou heas e n USA. Al hough A. hyg ophila
has been impo an o managemen o A. philoxe oides, we know li le abou how
salini y migh change plan ai s impo an o he su i al o he bee le (e.g., hol-
low s ems, Maddox e al. 1971; b anching a chi ec u e, Ha ms e al. 2023).
On he whole, in esponse o inc easing salini y, mo e ai s would seem o
suppo he bi o y by he biocon ol agen . Lea N concen a ion and s em b anch-
ing inc eased wi h inc easing sal s ess in eme gen plan s, po en ially inc easing
pala abili y o he bi o es (Reich 2014; Ha ms and C onin 2019) and ma habi a
o A. hyg ophila, espec i ely. Inc eased s em b anching may p o ide g ea e op-
po uni ies o hyd ocho ous dispe sal o ame hos s wi h insec he bi o es om
highe o lowe salini y zones (o ice e sa) ollowing dis u bance (Ha ms e al.
2023), wi h po en ially con as ing ou comes o he bi o y. Al hough phenolic
compounds p o ec plan s om mul iple abio ic and bio ic s esso s, including
salini y (Kuma e al. 2020; Chauhan e al. 2023; Ahlawa e al. 2024), eme gen
plan s in mesohaline condi ions and ee- loa ing plan s in mesohaline o euhaline
salini y accumula ed ewe o al phenolic compounds han unde eshwa e con-
di ions, sugges ing plan de ense agains he bi o y will decline wi h inc easing sa-
lini y. Howe e , low alloca ion o phenolics in eshwa e condi ions sugges s he
plan s may be be e de ended agains he bi o y in eshwa e (Singh e al. 2021).
Also, as salini y inc eased, less hollow, mo e igid s ems we e p oduced, po en ially
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
educing sui abili y o lea bee le pupa ion and dispe sal by hyd ocho y. Gi en he
con as ing implica ions o ai esponses by A. philoxe oides, he po en ial e icacy
o insec biological con ol agen s ac oss salini y g adien s me i s u he s udy.
Implica ions o in asi eness o Al e nan he a philoxe oides wi h sea
le el ise
Coas al looding by ex eme ide le els impac ing low-lying we lands a ound he
San F ancisco Bay–Del a Es ua y is p ojec ed o inc ease in magni ude and e-
quency concu en wi h con inued empe a u e wa ming and sea le el ise (Wang
e al. 2025). In his sys em, salini y in luences ege a ion pa e ns as i dec eases
wi h dis ance om he Paci ic Ocean and as i inc eases wi h in e idal ele a ion
wi hin b ackish we lands. The Medi e anean clima e wi h ho , d y summe s e-
sul s in ele a ed in e s i ial soil salini y in b ackish and sal ma shes (Callaway e al.
2007; Schile e al. 2011). The ecen in asion o A. philoxe oides in ou s udy a ea
has now sp ead along a longi udinal salini y g adien anging p ima ily om esh-
wa e inland Del a o oligohaline–high mesohaline (12–18 pp ) Suisun Ma sh
eaches and down-es ua y in o seasonal polyhaline condi ions (Au ho s, unpub-
lished da a). This occupied a ea includes he ele a ional salini y s ess g adien
om wa e ways upslope o he maximum idal ele a ion along na u al banks and
a i icial le ees and in o high ma sh plains and e es ial eco ones.
Na i e plan species locally dominan o subdominan in he lowe in e idal
zones in eshwa e and oligohaline–mesohaline eaches a he onse o he in a-
sion o A. philoxe oides (Au ho s, unpublished da a) a e now expe iencing sea le el
ise and impac s o he in asion. These include all clonal s ands o lood- ole an
sedges, ca ails, and eeds (e.g., Schoenoplec us, Typha, and Ph agmi es species). Sal -
g ass (Dis ichlis spica a (L.) G eene), pickleweed (Sa coco nia paci ica (S andley)
A.J. Sco ; pe Ball 2003), and o he succulen halophy es p e ail a highe in e -
idal ele a ions. Impo an ly, he idal we land ege a ion in aded by A. philoxe oi-
des ha is ulne able o changing salini y s ess also suppo s endemic plan species
and he highes p oduc i i y and biological di e si y in he es ua y (Pa ke e al.
2011). In gene al, mesocosm and ield obse a ions sugges dominan axa di e in
hei sensi i i y o inc easing salini y, wi h some mo e sensi i e han wha we ob-
se ed in ou s udy wi h A. philoxe oides. Fo example, in a mesocosm expe imen ,
inc easing salini y educed he g ow h o he na i e succulen S. paci ica om San
F ancisco Es ua y, al hough i ole a ed 30 pp le els (Woo and Takekawa 2012).
Na i e Typha domingensis Pe soon and T. la i olia L. a e epo ed o be mode a ely
ole an o b ackish salini y bu a lowe h esholds (5–8 pp ) han obse ed o
A. philoxe oides in ou expe imen (Macek and Rejmánko á 2007; Hadad e al.
2018). Howe e , ield obse a ions sugges T. domingensis main ains g ow h in o
somewha highe b ackish condi ions in ou s udy es ua y, and sympa ic, non-na-
i e T. angus i olia L. ole a es highe mesohaline salini y han i s congene s (Ban-
sal e al. 2019; Mo ei a e al. 2023). Likewise, sal ole ance is epo ed as “low” o
na i e Ph agmi es aus alis subsp. ame icanus Sal ons all, P.M. Pe e son & So eng
compa ed o in asi e non-na i e Eu opean and A ican Ph agmi es aus alis gen-
o ypes (Vasquez e al. 2005), which can ole a e salini y mo e concen a ed han
seawa e (Achenbach e al. 2013; Achenbach and B ix 2014).
The ela i e success o an in asi e plan species is dependen on he le el o en-
i onmen al s ess in he habi a (Alpe e al. 2000) and on na i e species’ abili ies
28
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
o espond o he concomi an compe i i e and en i onmen al p essu es. In Cali-
o nia’s es ua ine we lands, Callaway e al. (2007) p edic ed ha inc eases in ide-
wa e salini y will impa mo e immedia e s esses on idal we land ege a ion han
g ea e lood-induced s ess. Inc eased physiological s esses imposed by sea le el
ise can weaken he compe i i e abili ies o ulne able na i e species al eady nea
hei s ess ole ance h esholds, opening he dis u bed habi a o es ablishmen by
oppo unis ic in ade s (Gonzalez e al. 2024). In his con ex , g ea e sal ole ance
o in asi e plan species may suppo hei supe io compe i i e abili y o e na i e
species and hei in asi eness in saline en i onmen s (Liu e al. 2017; Liu e al.
2019; Guo e al. 2023). Pa adoxically, plan communi ies in ha sh habi a s a e
o en less in aded by non-na i e species han hose in mo e benign habi a s (Uye-
da e al. 2013; Ze e man e al. 2015; Zhao e al. 2025). Inc eased salini y s ess
can signi ican ly educe biomass p oduc ion o bo h na i e and in asi e species,
hough nega i e s ess e ec s ha e no esul ed in he elimina ion o many in asi e
aqua ic plan species. The in asion ou comes o na i e s. non-na i e in e speci ic
in e ac ions appea o depend on he numbe and in ensi y o en i onmen al s ess
ac o s in e ec and on unc ional plan ai s ela ed o pe o mance, s ess ole -
ance/a oidance s a egies, and p opagule p essu e ( an Kleunen e al. 2010; Ze e -
man e al. 2015; Zhao e al. 2025). Ou comes om in e ac ing e ec s o mul iple
s esses imposed by salini y, o he en i onmen al change ac o s, and in asion o
idal we lands by A. philoxe oides a e he e o e complex and unce ain.
Al hough s ess ole ance s a egies a e likely a play h oughou he in asion
con inuum, he compe i i e abili y o alien in ade s compa ed o na i e plan s
is key o hei in asi eness (Guo e al. 2022). In aqua ic sys ems, s ong compe -
i i e e ec s o A. philoxe oides ha e been a ibu ed o i s ma - o ming g ow h
o m, comp ised o in e wo en shoo s ha sp ead and blanke o e na i e we -
land plan s (see e iew, Tan ee e al. 2018). In complemen a y ield esea ch
in p og ess, we ha e been e alua ing he apid sp ead o A. philoxe oides in ou
s udy es ua y, whe e i s eme gen ma s a e displacing all clonal mac ophy es,
including na i e Schoenoplec us acu us (Muhl. ex Bigelow) Á. Lö e & D. Lö e
a . occiden alis (Wa son) S.G. Sm., S. cali o nicus (C.A. Meye ) Soják, Typha
domingensis, T. la i olia, Ph agmi es aus alis subsp. ame icanus, and o he species
in inging we lands along idal sloughs and island sho es in he b ackish Suisun
Ma sh (Suppl. ma e ial 1: ig. S5).
Conclusion
O e all, ou esul s indica e ha A. philoxe oides is a acul a i e halophy e well
adap ed o oligohaline o mesohaline salini y le els. Rema kably, plan s su i ed
ac oss he ull ange o eshwa e o euhaline expe imen al condi ions, wi h ai s
e ealing he in asi e weed’s s ess ole ance, a oidance, and escape s a egies o
endu ing salini y-induced physiological s ess. These di e se s a egies may enable
A. philoxe oides o wi hs and empo al and spa ial inc eases in salini y in idal we -
lands un il mo e a o able en i onmen al condi ions a e eached. Ha ing mul iple
s a egies sugges s he in ade will be esilien o a ange o condi ions ha migh
accompany sea-le el ise (e.g., al e ed he bi o y o disease, empe a u e ex emes).
Collec i ely, he g ow h, physiological, and biochemical ai s unde lying hese
s a egies can con ibu e o main aining he compe i i e abili y o A. philoxe oides,
suppo ing i s con inued in asi eness as es ua ine salini y in usion inc eases wi h
29
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B enda J. G ewell e al.: Al e nan he a philoxe oides salini y esponses
sea-le el ise. Imp o ed unde s anding o he mechanis ic ai s unde lying he
capaci y o A. philoxe oides o su i e salini y s ess can also be used o imp o e
p edic i e models o in asi e plan g ow h (Ja ed e al. 2022) ela i e o clima e
change e ec s on biological in asions, he eby imp o ing in asi e species isk as-
sessmen s and managemen p io i iza ion.
Acknowledgemen s
The au ho s hank Ca oline Jua ez, B yce King, and Angelica Reddy (USDA-ARS)
o assis ance wi h expe imen al main enance, ha es , and sample p ocessing, and
Robin Ca e -E ans (Cali o nia Depa men o Wa e Resou ces) o access o he
plan collec ion si e. We hank Filipe Ribei o and wo anonymous e iewe s o
sugges ions ha imp o ed ou manusc ip .
Addi ional in o ma ion
Con lic o in e es
The au ho s ha e decla ed ha no compe ing in e es s exis .
E hical s a emen
No e hical s a emen was epo ed.
Use o AI
No use o AI was epo ed.
Funding
This esea ch was pa ially suppo ed by coope a i e ag eemen 58-2030-0-038-F be ween he
U.S. Depa men o Ag icul u e, Ag icul u al Resea ch Se ice (USDA ARS), and he Uni e si-
y o Se ille. Blanca Gallego-Té a was unded by Jun a de Andalucía (Talen o Doc o es POST-
DOC_21_00090). Men ion o ade names o comme cial p oduc s is solely o p o ide speci ic
in o ma ion and does no imply ecommenda ion o endo semen by USDA.
Au ho con ibu ions
Concep ualiza ion: BJG, PDP, NEH, RED, JMC; Me hodology: BJG, PDP, NEH, RED, JMC;
In es iga ion: BJG, PDP, CJF, JMC; Da a cu a ion: CJF; Fo mal analysis: BG-T, JMC, BJG; W i ing
– o iginal d a : BJG, BG-T, JMC, CJF, RED, NEH, PDP; W i ing – e iew and edi ing: all au ho s.
Au ho ORCIDs
B enda J. G ewell h ps://o cid.o g/0000-0001-6768-3836
Blanca Gallego-Té a h ps://o cid.o g/0000-0002-1718-2977
Jesús M. Cas illo h ps://o cid.o g/0000-0003-1949-4349
Ca yn J. Fu ell h ps://o cid.o g/0000-0003-1440-7242
Rebecca E. D eno sky h ps://o cid.o g/0000-0003-1154-5869
Na han E. Ha ms h ps://o cid.o g/0000-0002-1614-3255
Paul D. P a h ps://o cid.o g/0000-0003-4423-7926
Da a a ailabili y
Da a suppo ing his s udy a e a ailable om John Ca oll Uni e si y, G aselli Lib a y’s "Ca oll
Collec ed" eposi o y: h ps://collec ed.jcu.edu/alliga o _weed_salini y_s udy/1/.
30
NeoBio a 102: 9–36 (2025), DOI: 10.3897/neobio a.102.150325
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