Variation in upper thermal tolerance among 19 species from temperate wetlands

1 This is he pee e iewed e sion o he a icle accep ed o publica ion in Jou nal o The mal 1 Biology, Volume 96, 2021, 102856, which has been published in inal o m a 2 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 3 Commons A ibu ion-NonComme cial-NoDe i a i es License 4 (h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/), which pe mi s non-comme cial e-use, 5 dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed, 6 and is no al e ed, ans o med, o buil upon in any way.” 7 Running Ti le: CTmax a ia ion in we lands 8 9 Va ia ion in uppe he mal ole ance among 19 species om empe a e we lands 10 11 Ma co Ka zenbe ge 1, 2*, Helde Dua e 1, Rick Relyea 3, 4, Juan F ancisco Bel án 5, Miguel 12 Tejedo 1 13 14 1 Depa men o E olu iona y Ecology, Es ación Biológica Doñana, CSIC, c/ Amé ico 15 Vespucio s/n, 41092 Se illa, Spain 16 2 Labo a ó io de Bioin o má ica e Biologia E olu i a, Depa men o Gene ics, Uni e sidade 17 Fede al de Pe nambuco, A . P o . Mo aes Rego, 1235 - Cidade Uni e si á ia, CEP 18 50670-901 Reci e, Pe nambuco, B azil 19 3 Da in F esh Wa e Ins i u e, Depa men o Biological Sciences, Rensselae Poly echnic 20 Ins i u e, T oy, NY 12180 USA 21 4 Depa men o Biological Sciences, Uni e si y o Pi sbu gh, Pi sbu gh, PA 15260, USA 22 5 Depa amen o Zoology, Uni e sidad de Se illa, A da. Reina Me cedes s/n, 41012-Se illa, 23 Spain 24 25 * co esponding au ho . E-mail: [email p o ec ed] 26 ORCID iD: 0000-0003-0023-9655 27 2 ABSTRACT 28 Communi ies usually possess a mul i ude o in e connec ed ophic in e ac ions wi hin 29 ood webs. Thei egula ion gene ally depends on a balance be ween bo om-up and op- 30 down e ec s. Howe e , i sensi i i y o empe a u e a ies among species, ising 31 empe a u es may change ophic in e ac ions ia di ec and indi ec e ec s. We examined 32 he c i ical he mal maximum (CTmax) o 19 species om empe a e we lands (insec 33 p eda o s, amphibian la ae, zooplank on and amphipods) and de e mined i hey a y in 34 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 35 insec s ha ing highe CTmax han amphibians (bo h he bi o ous la al anu ans and p eda o y 36 la al salamande s), amphipods and zooplank on. In a scena io o global wa ming, hese 37 di e ences in he mal ole ance may a ec op-down and bo om-up p ocesses, pa icula ly 38 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 39 highe empe a u es, which could lead o inc eased p eda ion a es on he he bi o es in he 40 ood web. Fu he s udies a e needed o unde s and how he ene gy lows h ough 41 communi ies, how species’ ene gy budge s may change and whe he o he physiological and 42 beha io al esponses (such as pheno ypic plas ici y and he mo egula ion) can bu e o 43 inc ease hese changes in he op-down egula ion o we land ood webs. 44 45 Keywo ds: c i ical he mal maximum; op-down egula ion; amphibians; insec s; 46 zooplank on; clima e change 47 3 1. INTRODUCTION 48 P edic ing he impac s o clima e change and unde s anding species’ esponses o 49 accele a ing en i onmen al changes has been a majo challenge o he scien i ic communi y. 50 The e is inc easing e idence ha species’ phenologies and dis ibu ions a e changing in 51 esponse o cu en clima e change (e.g., Pa mesan and Yohe 2003, Pa mesan 2006). 52 Renewed in e es in he mal physiology has p oduced la ge da abases ha enable a global 53 pe spec i e o species’ physiological limi s and hei ela ion o he en i onmen (e.g., 54 Deu sch e al., 2008; Dua e e al., 2012; Ka zenbe ge e al., 2014; Sunday e al., 2014;). 55 These da a ha e gi en new insigh s in o how species (and some communi ies) may espond 56 o cu en and u u e clima e change and a e p o iding a gene al assessmen o which axa 57 may be he mos ulne able. 58 In spi e o inc easing in o ma ion on he esponses o species and popula ions o 59 clima e change, obus models o ecological sys ems a e s ill badly needed o o ecas he 60 u u e s a e o communi ies and ecosys ems unde long- e m en i onmen al changes (Jochum 61 e al., 2012; Shu in e al., 2012). Howe e , he mul i ude o ac o s ha a ec ecosys ems and 62 hei complex in e ac ions ha e hinde ed he de elopmen o hese models. P edic ed 63 en i onmen al changes include an inc ease in he equency o hea wa es and o he ex eme 64 e en s (Di enbaugh and Ash aq, 2010; Schä e al., 2004). Shi s in UV adia ion, 65 p ecipi a ion and empe a u e pa e ns a e expec ed o a y geog aphically (IPCC, 2013). 66 Fu he mo e, se e al aspec s o he en i onmen a e simul aneously a ec ed by geochemical 67 cycles and changes in hese cycles may in luence local en i onmen al condi ions 68 (Ch is ensen e al., 2006; Vineb ooke e al., 2004). Apa om he physical en i onmen da a, 69 models should also inco po a e in o ma ion abou species’ physiological and li e-his o y 70 ai s. Di e en ial e olu iona y esponses o species’ physiological ai s o clima e change 71 may also p omo e shi s in communi y in e ac ions, ood web dynamics and ecosys em 72 4 p ocesses (Coulson e al., 2011; Gilman e al., 2010). Howe e , cu en expe imen al 73 e idence is limi ed (Jochum e al., 2012). Mo eo e , he di ec e ec s on species’ physiology 74 and demog aphics may be u he al e ed by indi ec e ec s ia ecological in e ac ions in 75 ood webs (Bo hwell e al., 1994; Ockendon e al., 2014; Su le e al., 2007). 76 The c i ical he mal maximum (CTmax) is he empe a u e a which an o ganism loses 77 i s abili y o a oid he condi ions ha will lead o i s dea h (Cowles and Boge , 1944). 78 The mal pe o mance cu es a e usually asymme ical, wi h he in e al be ween he 79 op imum empe a u e and he c i ical he mal maximum commonly cha ac e ized by a s eep 80 decline in pe o mance (Huey and Kingsol e , 1989). Howe e , de e mining op imum 81 empe a u e is usually me hodologically mo e di icul han de e mining CTmax (e.g., 82 Ka zenbe ge e al. 2014). Since op imum empe a u e and CTmax ha e been es ablished as 83 co-adap i e ai s (Angille a, 2009; Huey e al., 2009), a species wi h high CTmax is expec ed 84 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 85 and wa ming ole ance ( he di e ence be ween CTmax and cu en en i onmen al 86 empe a u es) is a simple way o assess species ulne abili y o he di ec e ec s o clima e 87 change (Deu sch e al., 2008; Tewksbu y e al., 2008). 88 Cu en global wa ming may p omo e changes in species in e ac ions and communi y 89 s uc u e (Dell e al. 2011), pa icula ly when species ha e con as ing he mal niches. A 90 educ ion in a ailable niche space o species wi h low hea ole ance can po en ially enhance 91 densi y-dependen in e ac ions, whe eas species wi h high hea ole ance could bene i om 92 he elease o compe i i e p essu es (Diamond e al., 2017). Wa m-adap ed consume s a e 93 also expec ed o exe inc eased op-down p essu e, leading o a educ ion in he biomass o 94 species om he lowe ophic le els i he la e a e less hea ole an (U ban e al., 2017). 95 Species asymme ies in he mal esponses may also a ec he dynamics o consume – 96 p oduce in e ac ions due o di e ences in ac i a ion ene gies ( he li e-dinne p inciple) 97 5 (Dawkins and K ebs, 1979; Dell e al., 2014, 2011). Top p eda o s may be close o hei 98 ole ance limi s (Pincebou de e al., 2008; Twomey e al., 2012), wi h ca ni o es ha ing peak 99 pe o mances a empe a u es 10ºC lowe han he bi o es (Dell e al., 2014; Voig e al., 100 2003). Howe e , much mo e in o ma ion is needed o es ablish a comp ehensi e 101 gene aliza ion o he mal ole ance ac oss ophic le els. 102 Di e ences in he mal ole ance ac oss ophic le els may also a ec op-down and 103 bo om-up e ec s in ood webs (Relyea and Rickle s, 2018). Wa ming can in luence ophic 104 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 105 inc easing he me abolic equi emen s o species (Dillon e al., 2010). Se e al s udies ha e 106 demons a ed ha op-down e ec s inc ease wi h wa ming, s eng hening he ophic cascade 107 om consume s o p oduce s (Hoekman, 2010; Jochum e al., 2012; K a ina e al., 2012; 108 O’Conno e al., 2009; Shu in e al., 2012). This occu s when he me abolic equi emen s o 109 consume s inc ease as e wi h empe a u e han ha o p oduce s (Allen e al., 2005), 110 esul ing in an inc ease in consume ac i i ies (Dillon e al., 2010; Hoekman, 2010; O’Conno 111 e al., 2009; Shu in e al., 2012). Howe e , me abolic demands can inc ease as e han 112 eeding a es (Rall e al., 2010) and inc eased eeding a es may also lead o esou ce 113 compe i ion. Mo eo e , dec eased ood in ake may also educe g ow h a es, educe op imal 114 empe a u es, and educe uppe he mal limi s o g ow h (Huey and Kingsol e , 2019). 115 The e o e, in he long- e m, consume s may su e om educed i ness, lowe abundance 116 and educed biomass when compa ed o p oduce s, he eby weakening he op-down e ec s 117 (O’Conno e al., 2011). In addi ion, wa ming ends o a o o ganisms ha compe e be e 118 o nu ien s (Falkowski and Oli e , 2007) and smalle o ganisms (Dau esne e al., 2009; 119 Y on-Du oche e al., 2011; Y on-Du oche and Allen, 2012). Bo h o hese ac o s should 120 in luence communi y size s uc u e and al e species composi ion (Y on-Du oche e al., 121 2011). 122 6 We aimed o unde s and how he cu en clima e-change scena io may a ec a 123 empo a y eshwa e we land communi y by de e mining he c i ical he mal maxima o 124 species om di e en ophic le els. The species include p ima y consume s ( adpoles, 125 zooplank on and amphipods) and seconda y and e ia y consume s (salamande la ae and 126 p eda o y insec s, espec i ely; Fig. 1). These axa ha e been used o s udy he dynamics o 127 ood web s uc u e and he mechanisms con olling he bo om-up and op-down p ocesses in 128 empe a e we lands o se e al decades (Jones e al., 2016; Leibold and Wilbu , 1992; S ole 129 and Relyea, 2016; Wilbu , 1997). CTmax alues may be phylogene ically cons ained (Huey, 130 1982; Huey e al., 2009; Kelle mann e al., 2012), al hough hey a e adap i ely associa ed 131 wi h en i onmen al empe a u es e en when con olling o phylogeny (e.g., Dua e e al. 132 2012). Hence, we expec ed o ind di e ences in he mal physiology among highe 133 axonomic g oups (e.g., Dua e e al. 2012; Sunday e al. 2014) and among ophic le els. 134 Based on p e ious s udies, we expec ed p eda o y insec species o ha e highe CTmax alues 135 han amphibians (e.g., Sunday e al. 2014). We also expec ed body mass o be a good 136 p edic o o uppe he mal esis ance ac oss species o ec o he ms (Klockmann e al., 2017), 137 al hough his ela ionship may no be e iden wi hin species (Dua e e al., 2012). 138 139 2. METHODS 140 2.1. Field collec ion and animal husband y 141 In sp ing 2010, we collec ed 11 species o amphibians (egg masses), ou species o 142 aqua ic insec s, h ee species o amphipods and one species o zooplank on (Cladoce a) om 143 na u al ponds and we lands. Each species was collec ed a a single loca ion (Tables 1-2). All 144 animals we e b ough o he Pyma uning Labo a o y o Ecology (Uni e si y o Pi sbu gh), in 145 no hwes Pennsyl ania, USA. Mic oen i onmen al pond empe a u es we e measu ed in 146 se en loca ions by placing HOBO Pendan ® empe a u e da alogge s in mos collec ion si es 147 7 a he deepes pa o he pond (Table 2). When he mal s a i ica ion occu s, usually du ing 148 sunny days wi h li le o no wind (Boeckman and Bidwell, 2015), hese measu emen s a e 149 assumed o ep esen he minimum en i onmen al empe a u es o which he animals a e 150 exposed du ing he ime pe iod conside ed; o he loca ions wi hin he pond (shallowe 151 loca ions o highe in he wa e column) p esumably had highe empe a u es (Banc o e al., 152 2008; Boeckman and Bidwell, 2015; Obe le e al., 2019; Song e al., 2013). Wa e 153 empe a u e was eco ded e e y 5–15 min du ing he pe iod in which mos species in he 154 communi y we e p esen . 155 The species we used belong o di e en ophic le els o a we land ood web, 156 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 157 dis ibu ion so hey can co-occu (a leas pa ially) and in e ac . Since eeding p e e ences o 158 anu an la ae depend on species and may include mul iple esou ces, such as pe iphy on, 159 zooplank on, phy oplank on and de i us (Al ig e al., 2007; A ibas e al., 2015; Ca ei a e 160 al., 2016; Mon aña e al., 2019), we conside ed se e al po en ial ene gy pa hways o his 161 g oup. In he labo a o y, he zooplank on and amphipod species we e kep in plas ic 162 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- 163 mm ne ) local pond wa e was added as sou ce o algae. Aqua ic insec s we e kep 164 indi idually in 500-mL plas ic cups ( illed wi h 400 mL o wa e ) and ed adpoles e e y 2 d. 165 Ou doo pools we e illed wi h aged well wa e o accommoda e he amphibian eggs. All egg 166 masses om he same species we e placed oge he in he same pool. Tadpoles we e hen ed 167 abbi pelle s ad libi um and allowed o g ow un il eaching he desi ed de elopmen al s age. 168 Mo eo e , salamande la ae we e ed zooplank on ad libi um. 169 170 2.2. C i ical he mal maximum assessmen 171 8 Se s o amphibian aqua ic la ae (anu an adpoles and la al salamande s) we e 172 b ough indoo s o acclima e o he expe imen . Amphibian la ae we e es ed a a 173 de elopmen al s age whe e hey we e able o swim eely and begin eeding independen ly. 174 In mos anu an species, his occu s a e eaching Gosne s age 25 (Gosne , 1960). O he 175 o ganisms we e es ed a he same de elopmen al s age as hey we e when collec ed (Table 176 3). Amphibian la ae, insec s, amphipods and zooplank on we e kep a an acclima ion 177 empe a u e o 20°C (app oxima ely he a e age empe a u e expe ienced in he ou doo 178 pools), wi h a 12L:12D pho ope iod, o ou days, as in p e ious s udies (Dua e e al., 2012; 179 Gu ié ez-Pesque a e al., 2016; Simon e al., 2015). This allowed o he animals o acclima e 180 o he lab empe a u e and s abilize hei CTmax (Allen e al., 2012; B a s om, 1968; 181 Buchanan e al., 1988; Hu chison, 1961). A e he acclima ion pe iod, he species we e es ed 182 o hei CTmax (B a s om, 1968; Hu chison, 1961) using Hu chison’s dynamic me hod 183 (Lu e schmid and Hu chison, 1997a). 184 The CTmax ials used a wa e ba h which consis ed o a 250-mL con aine illed wi h 185 200 mL o dechlo ina ed wa e a 20 °C placed wi hin a la ge 2-L con aine , se upon a 186 magne ic s i e ho pla e. Wa e empe a u e was measu ed in he smalle con aine , whe eas 187 he magne ic s i e was placed in he la ge con aine o a oid pe u bing he o ganisms. We 188 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 189 (Dua e e al., 2012; Simon e al., 2015). This hea ing a e is as enough o a oid acclima ion 190 du ing he CTmax ials bu also slow enough o a oid bo h hea shock and a signi ican lag 191 be ween wa e and body empe a u es (Lu e schmid and Hu chison, 1997a, 1997b). While 192 app oaching hei uppe he mal limi , o ganism i s lose hei igh ing esponse, hen go 193 h ough a s age o comple e immobili y be o e eaching he onse o spasms, which p ecedes 194 dea h (Lu e schmid and Hu chison, 1997a, 1997b). Fo adpoles, he onse o spasms was 195 conside ed he expe imen al endpoin . In he case o he insec s, amphipods and zooplank on, 196 9 since spasms could no be obse ed du ing he expe imen , we used comple e immobili y as 197 he endpoin o he c i ical he mal ole ance expe imen s. Once CTmax was eached, we 198 placed all o ganisms in o coole wa e (20°C) o allow o comple e eco e y. Those 199 indi iduals unable o eco e we e excluded o he analyses. All expe imen s we e app o ed 200 by he Ins i u ional Animal Ca e and Use Commi ee om he Uni e si y o Pi sbu gh 201 (P o ocol #12050451). 202 203 2.3. S a is ical analysis 204 To de e mine how he uppe he mal limi s a ied ac oss species, we conduc ed a 205 gene alized linea model (log-linked gamma dis ibu ion) using CTmax as he dependen 206 a iable, species as a ca ego ical ac o and mass as a co a ia e (including he in e ac ion 207 be ween species and mass). Al hough i is ecommended o inco po a e phylogene ic 208 in o ma ion (Felsens ein, 1985; Ga land J . e al., 1992), we could no implemen a PGLS 209 analysis since he numbe o species (n=19) is below he ecommended h eshold o >20 210 (Blombe g e al., 2003). The e o e, o accoun o he non-independence o species, we also 211 conduc ed a gene alized linea mixed model (log-linked gamma dis ibu ion), ha included 212 he axonomic le els ( om species o phylum) as nes ed, andom e ec s (Seebache e al., 213 2015), We hen compa ed bo h models using he Akaike in o ma ion c i e ion (AIC) (Akaike, 214 1974), o de e mine i he inclusion o highe axonomic le els imp o ed ou model. Nex , we 215 conduc ed Tukey HSD pos -hoc es s o see which species di e ed om each o he . To 216 examine he po en ial link be ween body size and CTmax, we also assessed he ela ionship 217 be ween CTmax and mass, wi hin each species, using Pea son’s co ela ion coe icien . 218 Ou second analysis examined he e ec s o ophic le el on CTmax. Fo each species, 219 ophic le el was de e mined as he longes chain leng h om a consume o a basal species, 220 plus one (Pimm, 1980). The ob ained ophic le els we e hen used as a g ouping a iable in 221 16 unde s and he empo al and spa ial dynamics o hese eshwa e ood webs unde he 371 cu en and u u e global wa ming. 372 373 ACKNOWLEDGMENTS 374 We hank Aa on S ole , Jessica Hua, Will B ogan, John Hammond and Rickey Co h an o 375 hei assis ance wi h ield collec ion and in he labo a o y. 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E osion o liza d di e si y by clima e change and al e ed he mal 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