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This is he pee e iewed e sion o he a icle accep ed o publica ion in Jou nal o The mal
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Biology, Volume 96, 2021, 102856, which has been published in inal o m a
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h ps://doi.o g/10.1016/j.j he bio.2021.102856 I is deposi ed unde he e ms o he C ea i e
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Commons A ibu ion-NonComme cial-NoDe i a i es License
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(h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/), which pe mi s non-comme cial e-use,
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dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed,
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and is no al e ed, ans o med, o buil upon in any way.”
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Running Ti le: CTmax a ia ion in we lands
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Va ia ion in uppe he mal ole ance among 19 species om empe a e we lands
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Ma co Ka zenbe ge 1, 2*, Helde Dua e 1, Rick Relyea 3, 4, Juan F ancisco Bel án 5, Miguel
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Tejedo 1
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1 Depa men o E olu iona y Ecology, Es ación Biológica Doñana, CSIC, c/ Amé ico
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Vespucio s/n, 41092 Se illa, Spain
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2 Labo a ó io de Bioin o má ica e Biologia E olu i a, Depa men o Gene ics, Uni e sidade
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Fede al de Pe nambuco, A . P o . Mo aes Rego, 1235 - Cidade Uni e si á ia, CEP
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50670-901 Reci e, Pe nambuco, B azil
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3 Da in F esh Wa e Ins i u e, Depa men o Biological Sciences, Rensselae Poly echnic
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Ins i u e, T oy, NY 12180 USA
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4 Depa men o Biological Sciences, Uni e si y o Pi sbu gh, Pi sbu gh, PA 15260, USA
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5 Depa amen o Zoology, Uni e sidad de Se illa, A da. Reina Me cedes s/n, 41012-Se illa,
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Spain
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* co esponding au ho . E-mail: [email p o ec ed]
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ORCID iD: 0000-0003-0023-9655
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ABSTRACT
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Communi ies usually possess a mul i ude o in e connec ed ophic in e ac ions wi hin
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ood webs. Thei egula ion gene ally depends on a balance be ween bo om-up and op-
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down e ec s. Howe e , i sensi i i y o empe a u e a ies among species, ising
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empe a u es may change ophic in e ac ions ia di ec and indi ec e ec s. We examined
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he c i ical he mal maximum (CTmax) o 19 species om empe a e we lands (insec
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p eda o s, amphibian la ae, zooplank on and amphipods) and de e mined i hey a y in
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hei sensi i i y o wa ming empe a u es. CTmax di e ed be ween he g oups, wi h p eda o y
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insec s ha ing highe CTmax han amphibians (bo h he bi o ous la al anu ans and p eda o y
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la al salamande s), amphipods and zooplank on. In a scena io o global wa ming, hese
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di e ences in he mal ole ance may a ec op-down and bo om-up p ocesses, pa icula ly
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conside ing ha insec p eda o s a e mo e likely o main ain o imp o e hei pe o mance a
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highe empe a u es, which could lead o inc eased p eda ion a es on he he bi o es in he
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ood web. Fu he s udies a e needed o unde s and how he ene gy lows h ough
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communi ies, how species’ ene gy budge s may change and whe he o he physiological and
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beha io al esponses (such as pheno ypic plas ici y and he mo egula ion) can bu e o
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inc ease hese changes in he op-down egula ion o we land ood webs.
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Keywo ds: c i ical he mal maximum; op-down egula ion; amphibians; insec s;
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zooplank on; clima e change
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1. INTRODUCTION
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P edic ing he impac s o clima e change and unde s anding species’ esponses o
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accele a ing en i onmen al changes has been a majo challenge o he scien i ic communi y.
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The e is inc easing e idence ha species’ phenologies and dis ibu ions a e changing in
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esponse o cu en clima e change (e.g., Pa mesan and Yohe 2003, Pa mesan 2006).
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Renewed in e es in he mal physiology has p oduced la ge da abases ha enable a global
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pe spec i e o species’ physiological limi s and hei ela ion o he en i onmen (e.g.,
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Deu sch e al., 2008; Dua e e al., 2012; Ka zenbe ge e al., 2014; Sunday e al., 2014;).
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These da a ha e gi en new insigh s in o how species (and some communi ies) may espond
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o cu en and u u e clima e change and a e p o iding a gene al assessmen o which axa
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may be he mos ulne able.
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In spi e o inc easing in o ma ion on he esponses o species and popula ions o
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clima e change, obus models o ecological sys ems a e s ill badly needed o o ecas he
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u u e s a e o communi ies and ecosys ems unde long- e m en i onmen al changes (Jochum
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e al., 2012; Shu in e al., 2012). Howe e , he mul i ude o ac o s ha a ec ecosys ems and
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hei complex in e ac ions ha e hinde ed he de elopmen o hese models. P edic ed
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en i onmen al changes include an inc ease in he equency o hea wa es and o he ex eme
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e en s (Di enbaugh and Ash aq, 2010; Schä e al., 2004). Shi s in UV adia ion,
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p ecipi a ion and empe a u e pa e ns a e expec ed o a y geog aphically (IPCC, 2013).
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Fu he mo e, se e al aspec s o he en i onmen a e simul aneously a ec ed by geochemical
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cycles and changes in hese cycles may in luence local en i onmen al condi ions
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(Ch is ensen e al., 2006; Vineb ooke e al., 2004). Apa om he physical en i onmen da a,
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models should also inco po a e in o ma ion abou species’ physiological and li e-his o y
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ai s. Di e en ial e olu iona y esponses o species’ physiological ai s o clima e change
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may also p omo e shi s in communi y in e ac ions, ood web dynamics and ecosys em
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p ocesses (Coulson e al., 2011; Gilman e al., 2010). Howe e , cu en expe imen al
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e idence is limi ed (Jochum e al., 2012). Mo eo e , he di ec e ec s on species’ physiology
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and demog aphics may be u he al e ed by indi ec e ec s ia ecological in e ac ions in
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ood webs (Bo hwell e al., 1994; Ockendon e al., 2014; Su le e al., 2007).
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The c i ical he mal maximum (CTmax) is he empe a u e a which an o ganism loses
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i s abili y o a oid he condi ions ha will lead o i s dea h (Cowles and Boge , 1944).
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The mal pe o mance cu es a e usually asymme ical, wi h he in e al be ween he
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op imum empe a u e and he c i ical he mal maximum commonly cha ac e ized by a s eep
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decline in pe o mance (Huey and Kingsol e , 1989). Howe e , de e mining op imum
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empe a u e is usually me hodologically mo e di icul han de e mining CTmax (e.g.,
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Ka zenbe ge e al. 2014). Since op imum empe a u e and CTmax ha e been es ablished as
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co-adap i e ai s (Angille a, 2009; Huey e al., 2009), a species wi h high CTmax is expec ed
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o also ha e a high op imum empe a u e. Hence, de e mining in e speci ic a ia ion in CTmax
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and wa ming ole ance ( he di e ence be ween CTmax and cu en en i onmen al
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empe a u es) is a simple way o assess species ulne abili y o he di ec e ec s o clima e
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change (Deu sch e al., 2008; Tewksbu y e al., 2008).
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Cu en global wa ming may p omo e changes in species in e ac ions and communi y
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s uc u e (Dell e al. 2011), pa icula ly when species ha e con as ing he mal niches. A
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educ ion in a ailable niche space o species wi h low hea ole ance can po en ially enhance
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densi y-dependen in e ac ions, whe eas species wi h high hea ole ance could bene i om
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he elease o compe i i e p essu es (Diamond e al., 2017). Wa m-adap ed consume s a e
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also expec ed o exe inc eased op-down p essu e, leading o a educ ion in he biomass o
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species om he lowe ophic le els i he la e a e less hea ole an (U ban e al., 2017).
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Species asymme ies in he mal esponses may also a ec he dynamics o consume –
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p oduce in e ac ions due o di e ences in ac i a ion ene gies ( he li e-dinne p inciple)
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(Dawkins and K ebs, 1979; Dell e al., 2014, 2011). Top p eda o s may be close o hei
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ole ance limi s (Pincebou de e al., 2008; Twomey e al., 2012), wi h ca ni o es ha ing peak
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pe o mances a empe a u es 10ºC lowe han he bi o es (Dell e al., 2014; Voig e al.,
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2003). Howe e , much mo e in o ma ion is needed o es ablish a comp ehensi e
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gene aliza ion o he mal ole ance ac oss ophic le els.
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Di e ences in he mal ole ance ac oss ophic le els may also a ec op-down and
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bo om-up e ec s in ood webs (Relyea and Rickle s, 2018). Wa ming can in luence ophic
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in e ac ions and al e he ela i e impo ance o hese op-down and bo om-up e ec s by
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inc easing he me abolic equi emen s o species (Dillon e al., 2010). Se e al s udies ha e
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demons a ed ha op-down e ec s inc ease wi h wa ming, s eng hening he ophic cascade
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om consume s o p oduce s (Hoekman, 2010; Jochum e al., 2012; K a ina e al., 2012;
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O’Conno e al., 2009; Shu in e al., 2012). This occu s when he me abolic equi emen s o
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consume s inc ease as e wi h empe a u e han ha o p oduce s (Allen e al., 2005),
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esul ing in an inc ease in consume ac i i ies (Dillon e al., 2010; Hoekman, 2010; O’Conno
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e al., 2009; Shu in e al., 2012). Howe e , me abolic demands can inc ease as e han
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eeding a es (Rall e al., 2010) and inc eased eeding a es may also lead o esou ce
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compe i ion. Mo eo e , dec eased ood in ake may also educe g ow h a es, educe op imal
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empe a u es, and educe uppe he mal limi s o g ow h (Huey and Kingsol e , 2019).
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The e o e, in he long- e m, consume s may su e om educed i ness, lowe abundance
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and educed biomass when compa ed o p oduce s, he eby weakening he op-down e ec s
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(O’Conno e al., 2011). In addi ion, wa ming ends o a o o ganisms ha compe e be e
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o nu ien s (Falkowski and Oli e , 2007) and smalle o ganisms (Dau esne e al., 2009;
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Y on-Du oche e al., 2011; Y on-Du oche and Allen, 2012). Bo h o hese ac o s should
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in luence communi y size s uc u e and al e species composi ion (Y on-Du oche e al.,
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2011).
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We aimed o unde s and how he cu en clima e-change scena io may a ec a
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empo a y eshwa e we land communi y by de e mining he c i ical he mal maxima o
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species om di e en ophic le els. The species include p ima y consume s ( adpoles,
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zooplank on and amphipods) and seconda y and e ia y consume s (salamande la ae and
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p eda o y insec s, espec i ely; Fig. 1). These axa ha e been used o s udy he dynamics o
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ood web s uc u e and he mechanisms con olling he bo om-up and op-down p ocesses in
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empe a e we lands o se e al decades (Jones e al., 2016; Leibold and Wilbu , 1992; S ole
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and Relyea, 2016; Wilbu , 1997). CTmax alues may be phylogene ically cons ained (Huey,
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1982; Huey e al., 2009; Kelle mann e al., 2012), al hough hey a e adap i ely associa ed
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wi h en i onmen al empe a u es e en when con olling o phylogeny (e.g., Dua e e al.
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2012). Hence, we expec ed o ind di e ences in he mal physiology among highe
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axonomic g oups (e.g., Dua e e al. 2012; Sunday e al. 2014) and among ophic le els.
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Based on p e ious s udies, we expec ed p eda o y insec species o ha e highe CTmax alues
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han amphibians (e.g., Sunday e al. 2014). We also expec ed body mass o be a good
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p edic o o uppe he mal esis ance ac oss species o ec o he ms (Klockmann e al., 2017),
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al hough his ela ionship may no be e iden wi hin species (Dua e e al., 2012).
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2. METHODS
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2.1. Field collec ion and animal husband y
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In sp ing 2010, we collec ed 11 species o amphibians (egg masses), ou species o
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aqua ic insec s, h ee species o amphipods and one species o zooplank on (Cladoce a) om
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na u al ponds and we lands. Each species was collec ed a a single loca ion (Tables 1-2). All
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animals we e b ough o he Pyma uning Labo a o y o Ecology (Uni e si y o Pi sbu gh), in
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no hwes Pennsyl ania, USA. Mic oen i onmen al pond empe a u es we e measu ed in
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se en loca ions by placing HOBO Pendan ® empe a u e da alogge s in mos collec ion si es
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a he deepes pa o he pond (Table 2). When he mal s a i ica ion occu s, usually du ing
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sunny days wi h li le o no wind (Boeckman and Bidwell, 2015), hese measu emen s a e
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assumed o ep esen he minimum en i onmen al empe a u es o which he animals a e
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exposed du ing he ime pe iod conside ed; o he loca ions wi hin he pond (shallowe
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loca ions o highe in he wa e column) p esumably had highe empe a u es (Banc o e al.,
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2008; Boeckman and Bidwell, 2015; Obe le e al., 2019; Song e al., 2013). Wa e
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empe a u e was eco ded e e y 5–15 min du ing he pe iod in which mos species in he
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communi y we e p esen .
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The species we used belong o di e en ophic le els o a we land ood web,
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including he bi o es, de i i o es, and p eda o s (Figu e 1). Mos o hese species o e lap in
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dis ibu ion so hey can co-occu (a leas pa ially) and in e ac . Since eeding p e e ences o
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anu an la ae depend on species and may include mul iple esou ces, such as pe iphy on,
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zooplank on, phy oplank on and de i us (Al ig e al., 2007; A ibas e al., 2015; Ca ei a e
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al., 2016; Mon aña e al., 2019), we conside ed se e al po en ial ene gy pa hways o his
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g oup. In he labo a o y, he zooplank on and amphipod species we e kep in plas ic
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con aine s (40 x 25 x 20 cm) wi h app oxima ely 10 L, o which an aliquo o il e ed (397-
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mm ne ) local pond wa e was added as sou ce o algae. Aqua ic insec s we e kep
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indi idually in 500-mL plas ic cups ( illed wi h 400 mL o wa e ) and ed adpoles e e y 2 d.
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Ou doo pools we e illed wi h aged well wa e o accommoda e he amphibian eggs. All egg
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masses om he same species we e placed oge he in he same pool. Tadpoles we e hen ed
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abbi pelle s ad libi um and allowed o g ow un il eaching he desi ed de elopmen al s age.
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Mo eo e , salamande la ae we e ed zooplank on ad libi um.
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2.2. C i ical he mal maximum assessmen
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Se s o amphibian aqua ic la ae (anu an adpoles and la al salamande s) we e
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b ough indoo s o acclima e o he expe imen . Amphibian la ae we e es ed a a
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de elopmen al s age whe e hey we e able o swim eely and begin eeding independen ly.
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In mos anu an species, his occu s a e eaching Gosne s age 25 (Gosne , 1960). O he
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o ganisms we e es ed a he same de elopmen al s age as hey we e when collec ed (Table
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3). Amphibian la ae, insec s, amphipods and zooplank on we e kep a an acclima ion
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empe a u e o 20°C (app oxima ely he a e age empe a u e expe ienced in he ou doo
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pools), wi h a 12L:12D pho ope iod, o ou days, as in p e ious s udies (Dua e e al., 2012;
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Gu ié ez-Pesque a e al., 2016; Simon e al., 2015). This allowed o he animals o acclima e
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o he lab empe a u e and s abilize hei CTmax (Allen e al., 2012; B a s om, 1968;
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Buchanan e al., 1988; Hu chison, 1961). A e he acclima ion pe iod, he species we e es ed
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o hei CTmax (B a s om, 1968; Hu chison, 1961) using Hu chison’s dynamic me hod
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(Lu e schmid and Hu chison, 1997a).
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The CTmax ials used a wa e ba h which consis ed o a 250-mL con aine illed wi h
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200 mL o dechlo ina ed wa e a 20 °C placed wi hin a la ge 2-L con aine , se upon a
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magne ic s i e ho pla e. Wa e empe a u e was measu ed in he smalle con aine , whe eas
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he magne ic s i e was placed in he la ge con aine o a oid pe u bing he o ganisms. We
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exposed he o ganisms o a cons an hea ing a e o 1.0 °C min-1, as in p e ious s udies
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(Dua e e al., 2012; Simon e al., 2015). This hea ing a e is as enough o a oid acclima ion
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du ing he CTmax ials bu also slow enough o a oid bo h hea shock and a signi ican lag
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be ween wa e and body empe a u es (Lu e schmid and Hu chison, 1997a, 1997b). While
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app oaching hei uppe he mal limi , o ganism i s lose hei igh ing esponse, hen go
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h ough a s age o comple e immobili y be o e eaching he onse o spasms, which p ecedes
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dea h (Lu e schmid and Hu chison, 1997a, 1997b). Fo adpoles, he onse o spasms was
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conside ed he expe imen al endpoin . In he case o he insec s, amphipods and zooplank on,
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since spasms could no be obse ed du ing he expe imen , we used comple e immobili y as
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he endpoin o he c i ical he mal ole ance expe imen s. Once CTmax was eached, we
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placed all o ganisms in o coole wa e (20°C) o allow o comple e eco e y. Those
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indi iduals unable o eco e we e excluded o he analyses. All expe imen s we e app o ed
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by he Ins i u ional Animal Ca e and Use Commi ee om he Uni e si y o Pi sbu gh
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(P o ocol #12050451).
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2.3. S a is ical analysis
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To de e mine how he uppe he mal limi s a ied ac oss species, we conduc ed a
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gene alized linea model (log-linked gamma dis ibu ion) using CTmax as he dependen
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a iable, species as a ca ego ical ac o and mass as a co a ia e (including he in e ac ion
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be ween species and mass). Al hough i is ecommended o inco po a e phylogene ic
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in o ma ion (Felsens ein, 1985; Ga land J . e al., 1992), we could no implemen a PGLS
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analysis since he numbe o species (n=19) is below he ecommended h eshold o >20
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(Blombe g e al., 2003). The e o e, o accoun o he non-independence o species, we also
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conduc ed a gene alized linea mixed model (log-linked gamma dis ibu ion), ha included
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he axonomic le els ( om species o phylum) as nes ed, andom e ec s (Seebache e al.,
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2015), We hen compa ed bo h models using he Akaike in o ma ion c i e ion (AIC) (Akaike,
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1974), o de e mine i he inclusion o highe axonomic le els imp o ed ou model. Nex , we
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conduc ed Tukey HSD pos -hoc es s o see which species di e ed om each o he . To
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examine he po en ial link be ween body size and CTmax, we also assessed he ela ionship
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be ween CTmax and mass, wi hin each species, using Pea son’s co ela ion coe icien .
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Ou second analysis examined he e ec s o ophic le el on CTmax. Fo each species,
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ophic le el was de e mined as he longes chain leng h om a consume o a basal species,
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plus one (Pimm, 1980). The ob ained ophic le els we e hen used as a g ouping a iable in
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unde s and he empo al and spa ial dynamics o hese eshwa e ood webs unde he
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cu en and u u e global wa ming.
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ACKNOWLEDGMENTS
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We hank Aa on S ole , Jessica Hua, Will B ogan, John Hammond and Rickey Co h an o
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hei assis ance wi h ield collec ion and in he labo a o y. This wo k was unded by a
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Fundação pa a a Ciência e Tecnologia (FCT) PhD ellowship (SFRH/BD/60271/2009) o
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MK, a U.S. Na ional Science Founda ion g an (#0716149) o RR, and a Spanish MICINN
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g an (CGL2009-12767-C02-02) and MINECO awa ds (CGL2012-40246-C02-01,
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CGL2017-86924-P) o MT and JFB.
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620
Table 5. Gene alized linea mixed model (log-link gamma dis ibu ion) o de e mine he
701
e ec s o ophic le el, body mass and hei in e ac ion on CTmax. Taxonomic le els om
702
species o phylum we e included as nes ed, andom e ec s o accoun o he non-
703
independence o ela ed species.
704
705
Fixed e ec s
d
Sum sq
Mean Sq
F
p
ophic
3
0.0820
0.0273
150.2
< 0.001
mass
1
0.0011
0.0011
5.8
0.017
ophic*mass
3
0.0003
0.0001
0.6
0.636
Random e ec s
Va iance ± SD
phylum
<0.00001 ± <0.00001
class
<0.00001 ± 0.00004
o de
<0.00001 ± 0.00005
amily
<0.00001 ± 0.00011
genus
0.00002 ± 0.00426
species
0.00010 ± 0.00977
Residual
0.00018 ± 0.01349
706

Figu e 1. Simpli ied we land ood web wi h ophic ela ions be ween he s udied species
707
(modi ied om Wilbu 1997). Solid a ows indica e he p ima y di ec ion o ene gy low.
708
Do ed a ows indica e po en ial ene gy low pa hways, depending on adpole species (Al ig e
709
al., 2007; A ibas e al., 2015; Mon aña e al., 2019). Dashed a ow indica es a seconda y
710
ene gy low ha occu s when salamande la ae g ow bigge han some adpole species and
711
a e hen able o consume hem. A) p eda o y insec s: Anax longipes, E y hemis simplicollis,
712
Le hoce us ame icanus and Noc onec a sp.. B) la al salamande s: Ambys oma la e ale. C)
713
la al anu ans: Anaxy us ame icanus, Hyla e sicolo , Pseudac is c uci e , P. e ia um, P.
714
ise ia a, Rana ca esbeiana, R. clami ans, R. palus is, R. pipiens and R. syl a ica. D)
715
zooplakn on: Daphnia magna. E) Amphipods: Hyalella sp., H. spinicauda and H. wellbo ni.
716
717
Figu e 2. Boxplo (median and qua iles) o c i ical he mal maximum (CTmax) o he s udied
718
species. Species we e g ouped acco ding o hei axonomy. Amphipods and zooplank on
719
we e g ouped oge he (Zoo/Apod g oup) since hey ep esen he main phy oplank on
720
consume s. Dashed lines indica e he a e age CTmax o each g oup and he espec i e
721
s anda d de ia ion. Species: ALO, Anax longipes; ESI, E y hemis simplicollis; LAM,
722
Le hoce us ame icanus; NOC, Noc onec a sp.; ALA, Ambys oma la e ale; AAM, Anaxy us
723
ame icanus; HVE, Hyla e sicolo ; PCR, Pseudac is c uci e ; PFE, P. e ia um; PTR, P.
724
ise ia a; LCA, Rana ca esbeiana; RCL, R. clami ans; RPA, R. palus is; RPI, R. pipiens;
725
RSY, R. syl a ica; DMA, Daphnia magna; HYA, Hyalella sp.; HSP, H. spinicauda; HWE,
726
H. wellbo ni.
727
728
729
730
731