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Long-term thermal acclimation drives adaptive physiological adjustments of a marine gastropod to reduce sensitivity to climate change

January 2021
The Science of The Total Environment 771:145208

January 2021
771:145208

DOI:10.1016/j.scitotenv.2021.145208

Authors:

Jonathan Y.S. Leung

Shantou University

Bayden Dwight Russell

The University of Hong Kong

Melinda A Coleman

New South Wales Department of Primary Industries

Brendan P Kelaher

Southern Cross University

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Ocean warming is predicted to challenge the persistence of a variety of marine organisms, especially when combined with ocean acidification. Whilst temperature affects virtually all physiological processes, the extent to which thermal history mediates the adaptive capacity of marine organisms to climate change has been largely overlooked. Using populations of a marine gastropod (Turbo undulatus) with different thermal histories (cool vs. warm), we compared their physiological adjustments following exposure (8-week) to ocean acidification and warming. Compared to cool-acclimated counterparts, we found that warm-acclimated individuals had higher thermal threshold (i.e. increased CTmax by 2°C), which was unaffected by the exposure to ocean acidification and warming. Thermal history also strongly mediated physiological effects, where warm-acclimated individuals adjusted to warming by conserving energy, suggested by lower respiration and ingestion rates, energy budget (i.e. scope for growth) and O:N ratio. After exposure to warming, warm-acclimated individuals had higher metabolic rates and greater energy budget due to boosted ingestion rates, but such compensatory feeding disappeared when combined with ocean acidification. Overall, we suggest that thermal history can be a critical mediator of physiological performance under future climatic conditions. Given the relatively gradual rate of global warming, marine organisms may be better able to adaptively adjust their physiology to future climate than what short-term experiments currently convey.

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UNCORRECTED PROOF

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Contents lists available at ScienceDirect

-7=9B79C:H<9.CH5@BJ=FCBA9BH

journal homepage: http://ees.elsevier.com

&CB;H9FA H<9FA5@ 577@=A5H=CB 8F=J9G 585DH=J9 D<MG=C@C;=75@ 58>IGHA9BHG C: 5 A5F=B9

;5GHFCDC8 HC F98I79 G9BG=H=J=HM HC 7@=A5H9 7<5B;9

$CB5H<5B 3- &9IB; 56 5M89B  ,IGG9@@ 7 '9@=B85  C@9A5B 8 F9B85B * %9@5<9F 9 -95B  CBB9@@ 6⁎

5Faculty of Materials and Energy, Southwest University, Chongqing 400715, China

6Southern Seas Ecology Laboratories, The Environment Institute, School of Biological Sciences, The University of Adelaide, South Australia, Australia

7The Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Hong Kong, SAR, China

8New South Wales Department of Primary Industries, Fisheries, National Marine Science Centre, 2 Bay Drive, Co@s Harbour, NSW 2450, Australia

9National Marine Science Centre and Marine Ecology Research Centre, Southern Cross University, PO Box 4321, Co@s Harbour, NSW 2450, Australia

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Article history:

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779DH98  $5BI5FM 

J5=@56@9 CB@=B9 LLL

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Keywords

85DH5H=CB

!5GHFCDC8

)795B 57=8=Y75H=CB

)795B K5FA=B;

*<MG=C@C;M

.<9FA5@ <=GHCFM

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)795B K5FA=B; =G DF98=7H98 HC 7<5@@9B;9 H<9 D9FG=GH9B79 C: 5 J5F=9HM C: A5F=B9 CF;5B=GAG 9GD97=5@@M K<9B

7CA6=B98 K=H< C795B 57=8=Y75H=CB 1<=@9 H9AD9F5HIF9 5::97HG J=FHI5@@M 5@@ D<MG=C@C;=75@ DFC79GG9G H<9 9LH9BH HC

K<=7< H<9FA5@ <=GHCFM A98=5H9G H<9 585DH=J9 75D57=HM C: A5F=B9 CF;5B=GAG HC 7@=A5H9 7<5B;9 <5G 699B @5F;9@M

CJ9F@CC?98 /G=B; DCDI@5H=CBG C: 5 A5F=B9 ;5GHFCDC8 Turbo undulatus K=H< 8=::9F9BH H<9FA5@ <=GHCF=9G 7CC@ JG

K5FA K9 7CAD5F98 H<9=F D<MG=C@C;=75@ 58>IGHA9BHG :C@@CK=B; 9LDCGIF9 K99? HC C795B 57=8=Y75H=CB 5B8

K5FA=B; CAD5F98 HC 7CC@577@=A5H98 7CIBH9FD5FHG K9 :CIB8 H<5H K5FA577@=A5H98 =B8=J=8I5@G <58 <=;<9F

H<9FA5@ H<F9G<C@8 =9 =B7F95G98 .A5L 6M  U K<=7< K5G IB5::97H98 6M H<9 9LDCGIF9 HC C795B 57=8=Y75H=CB

5B8 K5FA=B; .<9FA5@ <=GHCFM 5@GC GHFCB;@M A98=5H98 D<MG=C@C;=75@ 9::97HG K<9F9 K5FA577@=A5H98 =B8=J=8I5@G

58>IGH98 HC K5FA=B; 6M 7CBG9FJ=B; 9B9F;M GI;;9GH98 6M @CK9F F9GD=F5H=CB 5B8 =B;9GH=CB F5H9G 9B9F;M 6I8;9H

=9 G7CD9 :CF ;FCKH< 5B8 )( F5H=C :H9F 9LDCGIF9 HC K5FA=B; K5FA577@=A5H98 =B8=J=8I5@G <58 <=;<9F A9H5

6C@=7 F5H9G 5B8 ;F95H9F 9B9F;M 6I8;9H 8I9 HC 6CCGH98 =B;9GH=CB F5H9G 6IH GI7< 7CAD9BG5HCFM :998=B; 8=G5DD95F98

K<9B 7CA6=B98 K=H< C795B 57=8=Y75H=CB )J9F5@@ K9 GI;;9GH H<5H H<9FA5@ <=GHCFM 75B 69 5 7F=H=75@ A98=5HCF C:

D<MG=C@C;=75@ D9F:CFA5B79 IB89F :IHIF9 7@=A5H=7 7CB8=H=CBG !=J9B H<9 F9@5H=J9@M ;F58I5@ F5H9 C: ;@C65@ K5FA=B;

A5F=B9 CF;5B=GAG A5M 69 69HH9F 56@9 HC 585DH=J9@M 58>IGH H<9=F D<MG=C@C;M HC :IHIF9 7@=A5H9 H<5B K<5H G<CFHH9FA

9LD9F=A9BHG 7IFF9BH@M 7CBJ9M

V 

1. Introduction

BH<FCDC;9B=7 )9A=GG=CBG CJ9F H<9 @5GH 79BHIFM <5J9 75IG98 C6

G9FJ56@9 7<5B;9G =B C795B=7 7@=A5H9 D5FH=7I@5F@M H<9 =B7F95G9 =B 5J9F

5;9 G95 GIF:579 H9AD9F5HIF9 ?BCKB 5G C795B K5FA=B; #* 

.<=G ;@C65@ D<9BCA9BCB =G :CF975GH HC =BH9BG=:M CJ9F H=A9 5B8 <5G H<IG

8F5KB GI6GH5BH=5@ 5HH9BH=CB CJ9F 7CB79FBG H<5H H<9 YHB9GG 5B8 GIFJ=J5@

C: A5BM A5F=B9 CF;5B=GAG K=@@ 8=A=B=G< =B H<9 B95F :IHIF9 *C@C7N5B

G?5 9H 5@  9GD97=5@@M H<CG9 5@F958M @=J=B; 7@CG9 HC H<9=F H<9F

A5@ H<F9G<C@8 88=H=CB5@@M =B7F95G98 )9A=GG=CBG K=@@ 75IG9 C795B

57=8=Y75H=CB #*  K<=7< A5M 9L579F65H9 H<9 58J9FG9 9::97HG

C: C795B K5FA=B; CB A5F=B9 CF;5B=GAG 9; *F585 9H 5@ &9

IB; 9H 5@ 15B; 9H 5@  *F98=7H=CBG C: :IHIF9 A5F=B9

97CGMGH9AG H<9F9:CF9 GI;;9GH GI6GH5BH=5@ IB79FH5=BHM =B H<9=F :IB7H=CB

5B8 D9FG=GH9B79 (5;9@?9F?9B 5B8 CBB9@@ 

⁎CFF9GDCB8=B; 5IH<CF

E-mail address: G95B7CBB9@@589@5=8998I5I - CBB9@@

!FCK=B; 9J=89B79 G<CKG H<5H 9@9J5H98 H9AD9F5HIF9G 75B 6CCGH H<9

YHB9GG C: A5F=B9 CF;5B=GAG K=H<=B D<MG=C@C;=75@ H<F9G<C@8G DCH9BH=5@@M

=ADFCJ=B; 585DH=J9 75D57=HM HC 7CD9 K=H< 7@=A5H9 7<5B;9 !@5B8CB 5B8

'=@@9F &9IB; 9H 5@ 5 5 "9B79 A5BM A5F=B9 CF

;5B=GAG A5M 69 ACF9 577CAAC85H=B; HC ;F58I5@ K5FA=B; H<5B K<5H

G<CFHH9FA 9LD9F=A9BH5@ GHI8=9G 75B 7CBJ9M -<CFHH9FA F5AD=B; C: 9L

D9F=A9BH5@ H9AD9F5HIF9 GI7< 5G F5D=8 CF 57IH9 K5FA=B; 75B 9L5;;9F5H9

H<9 A95GIF98 9::97HG C: H9AD9F5HIF9 CB D<MG=C@C;M 5B8 B9;5H9 585DH=J9

F9GDCBG9G -99657<9F 9H 5@  #B8998 C795B K5FA=B; =G 5 F9@5

H=J9@M ;F58I5@ DFC79GG H<5H C77IFG CJ9F AI@H=D@9 ;9B9F5H=CBG C: A5BM A5

F=B9 CF;5B=GAG #*  8IF=B; K<=7< F9G=GH5B79 HC H<9 ;F58I5@ =B

7F95G9 =B H9AD9F5HIF9 A5M 9JC@J9 G H<9 8IF5H=CB C: H<9FA5@ 9J9BHG 75B

89H9FA=B9 CF;5B=GA5@ F9GDCBG9G ,C<F 9H 5@  =H =G 8=:Y7I@H HC 5G

79FH5=B H<9 =AD57HG C: C795B K5FA=B; CB A5F=B9 CF;5B=GAG =: @CB;H9FA

H<9FA5@ 577@=A5H=CB =G BCH H5?9B =BHC 7CBG=89F5H=CB

.<9 =BZI9B79 C: C795B K5FA=B; CB H<9 D9F:CFA5B79 C: A5F=B9 CF

;5B=GAG =G DF=A5F=@M 89H9FA=B98 6M H<9=F H<9FA5@ H<F9G<C@8 G=B79 A5BM

D<MG=C@C;=75@ DFC79GG9G 5F9 H9AD9F5HIF989D9B89BH "C7<57<?5 5B8

-CA9FC &9IB; 9H 5@ 5 1<9B H9AD9F5HIF9G 9L7998 H<9

H<9FA5@ H<F9G<C@8 C: CF;5B=GAG H<9=F D<MG=C@C;=75@ D9F:CFA5B79 9B

9F;M 65@5B79 5B8 I@H=A5H9@M YHB9GG 5F9 IB89FA=B98 -C?C@CJ5 9H 5@

<HHDG8C=CF;>G7=HCH9BJ

V 

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208

 #B 7CBHF5GH 69B9Y7=5@ 9::97HG C: C795B K5FA=B; 75B 69 C6G9FJ98

K<9B H<9 9@9J5H98 H9AD9F5HIF9 :5@@G =BHC H<9 CDH=A5@ H9AD9F5HIF9 F5B;9

C: CF;5B=GAG *TFHB9F 9H 5@ &9IB; 9H 5@ 5 G GI7<

H<9FA5@ H<F9G<C@8 <5G 699B :F9EI9BH@M H9GH98 HC DF98=7H H<9 JI@B9F56=@

=HM C: A5F=B9 CF;5B=GAG HC C795B K5FA=B; 9; (;IM9B 9H 5@ 

'589=F5 9H 5@  #H =G BCH9KCFH<M <CK9J9F H<5H H<9FA5@ H<F9G<

C@8 =G 5 D@5GH=7 HF5=H H<5H CF;5B=GAG 75B =B7F95G9 H<FCI;< @CB;H9FA H<9F

A5@ 577@=A5H=CB C:H9B G99B =B 8=::9F9BH DCDI@5H=CBG H<FCI;<CIH H<9 8=G

HF=6IH=CB C: 5 GD97=9G -H=@@A5B '5;CNN= 5B8 5@CG= 

!=CA= 9H 5@  .<IG 9LD@CF=B; <CK H<9FA5@ <=GHCFM =BZI9B79G

H<9FA5@ H<F9G<C@8 D<MG=C@C;=75@ D9F:CFA5B79 5B8 9B9F;M 65@5B79 75B

DFCJ=89 5 ACF9 F9@=56@9 DF98=7H=CB C: H<9 YHB9GG C: A5F=B9 CF;5B=GAG =B

:IHIF9 C795BG

*CDI@5H=CBG C: 5 GD97=9G :FCA 8=::9F9BH @C75@=H=9G K=H<=B H<9 ;9C

;F5D<=7 8=GHF=6IH=CB 9; K5FA98;9 JG 7CC@ A=8F5B;9 =B K<=7< AI@

H=D@9 ;9B9F5H=CBG <5J9 @=J98 IB89F 8=::9F9BH H<9FA5@ 7CB8=H=CBG DFCJ=89

5B CDDCFHIB=HM HC H5?9 H<9FA5@ <=GHCFM =BHC 577CIBH K<9B HFM=B; HC

IB89FGH5B8 D<MG=C@C;=75@ F9GDCBG9G HC K5FA=B; .<9 F9GDCBG9G C: H<9

K5FA577@=A5H98 =B8=J=8I5@G 75B 69 IG98 HC =B:9F H<9 585DH=J9 75D57

=HM C: H<9 7CC@577@=A5H98 7CIBH9FD5FHG HC :IHIF9 C795B K5FA=B; #B H<=G

GHI8M H<9F9:CF9 K9 7C@@97H98 ;5GHFCDC8G Turbo undulatus :FCA @C75@

=H=9G K=H< 8=::9F9BH H<9FA5@ 7CB8=H=CBG 7CC@ JG K5FA 5B8 7CAD5F98

H<9=F H<9FA5@ H<F9G<C@8 D<MG=C@C;=75@ D9F:CFA5B79 9; F9GD=F5H=CB F5H9

=B;9GH=CB F5H9 5B8 9B9F;M 5GG=A=@5H=CB 9B9F;M 6I8;9H 5B8 6C8M 7CB

8=H=CB 5:H9F 9LDCGIF9 HC C795B 57=8=Y75H=CB 5B8 K5FA=B; CAD5F98 HC

H<9 7CC@577@=A5H98 ;5GHFCDC8G K9 <MDCH<9G=G98 H<5H H<9 K5FA577@=

A5H98 ;5GHFCDC8G KCI@8 <5J9 <=;<9F H<9FA5@ H<F9G<C@8 =B8=75H98 6M

<=;<9F 7F=H=75@ H<9FA5@ A5L=AIA .A5L :CF K<=7< H<9=F D<MG=C@C;=75@

D9F:CFA5B79 5B8 9B9F;M 6I8;9H KCI@8 69 @9GG =AD57H98 6M H<9 K5FA=B;

F9;=A9 C: H<9 7CC@577@=A5H98 DCDI@5H=CB #B 588=H=CB K9 9LD97H98 H<5H

H<9 H<9FA5@ H<F9G<C@8 D<MG=C@C;=75@ D9F:CFA5B79 5B8 9B9F;M 6I8;9H C:

;5GHFCDC8G KCI@8 69 F98I798 6M C795B 57=8=Y75H=CB =FF9GD97H=J9 C: H<9F

A5@ <=GHCFM M 7CBG=89F=B; @CB;H9FA H<9FA5@ 577@=A5H=CB K=H<=B 5B

97C@C;=75@@MF9@9J5BH H<9FA5@ <=GHCFM H<=G GHI8M DFCJ=89G 5 ACF9 7CA

DF9<9BG=J9 9J5@I5H=CB C: H<9 F9GDCBG9G C: A5F=B9 CF;5B=GAG HC C795B

K5FA=B; 5B8 G<98G @=;<H CB <CK H<9FA5@ 585DH5H=CB A5M 5@@CK H<9A HC

DF9J5=@ =B :IHIF9 C795BG

2. Materials and methods

2.1. Collection of specimens

Turbo undulatus =G 5B 56IB85BH <9F6=JCFCIG ;5GHFCDC8 K=89@M 8=G

HF=6IH98 =B H<9 H9AD9F5H9 A5F=B9 K5H9FG C: IGHF5@=5 5B8 DF98CA=B5BH@M

=B<56=HG G<5@@CK GI6H=85@ NCB9G K<9F9 =H D@5MG 5B =ADCFH5BH FC@9 =B GHFI7

HIF=B; 97C@C;=75@ 5B8 9B9F;M 8MB5A=7G #B8=J=8I5@G C: 58I@H Tundula-

tus G<9@@ @9B;H< – AA K9F9 7C@@97H98 =B 5IHIAB :FCA H<9 G<5@@CK

GI6H=85@ NCB9G 5H )-I@@=J5B 957<  U U- U -CIH<

IGHF5@=5 5B8 5H 'I@@5K5M "958@5B8  U U- U (9K

-CIH< 15@9G .<9G9 HKC FC7?M F99:G <5J9 G=A=@5F <56=H5H 7<5F57H9F

=GH=7G 5B8 G95K5H9F DFCD9FH=9G 9; D" G5@=B=HM 5B8 HCH5@ 5@?5@=B=HM

.56@9 - 6IH 8=::9F9BH H<9FA5@ 7CB8=H=CBG 5BBI5@ G95 GIF:579 H9AD9F

5HIF9 F5B;9 – U :CF )-I@@=J5B 957< JG – U :CF 'I@@5K5M

"958@5B8 =; - A95B=B; H<5H H<9 DCDI@5H=CBG C: ;5GHFCDC8G :FCA

H<9G9 HKC G=H9G <5J9 8=::9F9BH H<9FA5@ <=GHCF=9G =9 7CC@ JG K5FA G

GI7< “7CC@577@=A5H98 ;5GHFCDC8G”5B8 “K5FA577@=A5H98 ;5GHFCDC8G”

K9F9 IG98 =B H<=G D5D9F HC 89G7F=69 H<CG9 7C@@97H98 :FCA )-I@@=J5B

957< 5B8 'I@@5K5M "958@5B8 F9GD97H=J9@M #B H<9 @56CF5HCFM H<9 ;5G

HFCDC8G K9F9 A5=BH5=B98 =B D@5GH=7 H5B?G  A \  7A \  7A 7CB

H5=B=B; B5HIF5@ G95K5H9F D"  W  H9AD9F5HIF9  W  U

5B8 G5@=B=HM  W  DDH K=H< 7CBH=BICIG 59F5H=CB :CF H<F99 K99?G

.C 5JC=8 H<9 G<C7? 9::97H 75IG98 6M 5 GI889B 7<5B;9 =B H9AD9F5

HIF9 H<9 G95K5H9F H9AD9F5HIF9 =B H<9 D@5GH=7 H5B?G K5G ;F58I5@@M 58

>IGH98 :FCA H<5H 5H H<9 7C@@97H=CB G=H9 =9  U CF  U HC  U

5H 5 7<5B;9 F5H9 C:  U D9F 85M -95 @9HHI79 Ulva lactuca K5G 7C@

@97H98 :FCA H<9 Y9@8 5B8 K5G DFCJ=898 5G

:CC8 :CF H<9 ;5GHFCDC8G -95K5H9F =B H<9 H5B?G K5G F9B9K98 9J9FM H<F99

85MG

2.2. Experimental setup

#B H<=G GHI8M HKC p)@9J9@G  DDA 5B8  DDA 5B8 HKC

H9AD9F5HIF9 @9J9@G  U 5B8  U K9F9 7<CG9B HC C6H5=B :CIF HF95H

A9BH 7CB8=H=CBG 65G98 CB H<9=F 7FCGG98 7CA6=B5H=CBG .<9 9@9J5H98 p)

5B8 H9AD9F5HIF9 G=AI@5H9 H<9 DF98=7H98 ,* G79B5F=C :CF H<9 M95F

 #*  K<9F95G H<9 5A6=9BH H9AD9F5HIF9 =G 65G98 CB H<9

=BG=HI A95GIF9A9BH C: G95K5H9F H9AD9F5HIF9 5H H<9 7CC@9F G=H9 =B GIA

A9F =9 )-I@@=J5B 957< GC H<5H H<9 K5FA577@=A5H98 ;5GHFCDC8G =9

:FCA 'I@@5K5M "958@5B8 7CI@8 69 IG98 HC 9J5@I5H9 585DH=J9 75D57=HM

HC C795B K5FA=B; K=H<=B D<MG=C@C;=75@ H<F9G<C@8G C@@CK=B; H<9 K99?

577@=A5H=CB D9F=C8 H<F99 ;5GHFCDC8G K9F9 DIH =BHC 5 D@5GH=7 5EI5F=IA

 7A \  7A \  7A Y@@98 K=H< O & B5HIF5@ G95K5H9F 58>IGH98

HC CB9 C: H<9 HF95HA9BH 7CB8=H=CBG :CF  K99?G n  F9D@=75H9 5EI5F=5

D9F HF95HA9BH D9F DCDI@5H=CB .<9 H5F;9H H9AD9F5HIF9G K9F9 A5=BH5=B98

6M DIHH=B; H<9 5EI5F=5 =B K5H9F 65H<G K=H< K5H9F H9AD9F5HIF9 F9;I

@5H98 6M <95H9F7<=@@9F IB=HG . .) #H5@M .<9 9@9J5H98 p)

K5G 57<=9J98 5B8 A5=BH5=B98 6M 7CBH=BICIG@M 59F5H=B; H<9 G95K5H9F

K=H< )9BF=7<98 5HACGD<9F=7 5=F IG=B; 5 ;5G A=L9F *9;5G  ' 

C@IA6IG #BGHFIA9BHG /- K<9F95G H<9 5A6=9BH p)6M 7CBH=BI

CIG@M 59F5H=B; H<9 G95K5H9F K=H< 5HACGD<9F=7 5=F !5GHFCDC8G K9F9 :98

Ulva lactuca 58 @=6=HIA K<=7< K5G F9D@9B=G<98 K<9B B979GG5FM -95K5

H9F K5G F9B9K98 CB79 9J9FM H<F99 85MG O 7<5B;9 HC DF9J9BH 57

7IAI@5H=CB C: :5979G 5B8 A9H56C@=7 K5GH9 .9AD9F5HIF9 5B8 D" C: G95

K5H9F K9F9 85=@M A95GIF98 IG=B; 5 D"H9AD9F5HIF9 A9H9F "# 

"(( #BGHFIA9BHG !9FA5BM 75@=6F5H98 IG=B; (- 6I[9FG -5@=B=HM

5B8 HCH5@ 5@?5@=B=HM K9F9 A95GIF98 K99?@M IG=B; 5 <5B8<9@8 F9:F57

HCA9H9F 5B8 5 DCH9BH=CA9HF=7 H=HF5HCF  .=HF5B8C '9HFC<A -K=HN9F

@5B8 F9GD97H=J9@M .<9 p) 8=GGC@J98 =BCF;5B=7 75F6CB # 5B8 G5H

IF5H=CB GH5H9G C: 75@7=H9 Ω75@ 5B8 5F5;CB=H9 Ω5F5 K9F9 75@7I@5H98 IG

=B; H<9 )-3- DFC;F5A *=9FFCH 9H 5@  K=H< 8=GGC7=5H=CB 7CB

GH5BHG :FCA '9<F657< 9H 5@  F9YHH98 6M =7?GCB 5B8 '=@@9FC

 .<9 G95K5H9F 75F6CB5H9 7<9A=GHFM 8IF=B; H<9 K99? 9LDCGIF9

D9F=C8 =G G<CKB =B .56@9 

2.3. Physiological performance and body condition

:H9F H<9 K99? 9LDCGIF9 HC H<9 HF95HA9BH 7CB8=H=CBG H<9 D<MG

=C@C;=75@ D9F:CFA5B79 C: ;5GHFCDC8G K5G 5GG9GG98 IG=B; H<9 G7CD9 :CF

;FCKH< 5DDFC57< K<9F9 F9GD=F5H=CB 56GCFDH=CB 5B8 9L7F9H=CB F5H9G

K9F9 A95GIF98 HC 9GH=A5H9 9B9F;M 6I8;9H .<9 9LD9F=A9BH5@ DFC798IF9G

89G7F=698 =B &9IB; 9H 5@ 5 K9F9 58CDH98 K=H< A=BCF AC8=Y75

H=CBG .C 89H9FA=B9 F9GD=F5H=CB F5H9 HKC ;5GHFCDC8G :FCA 957< 5EI5F=IA

K9F9 =B8=J=8I5@@M DIH =BHC 5  A& 5=FH=;<H 7<5A69F Y@@98 K=H< G95

K5H9F 58>IGH98 HC H<9 F9GD97H=J9 HF95HA9BH 7CB8=H=CBG =9 9LD9F=A9B

H5@ G95K5H9F 5B8 5@@CK98 HC F9GH :CF  < n  F9D@=75H9 7<5A69FG D9F

HF95HA9BH D9F DCDI@5H=CB :H9F H<=G F9GH=B; D9F=C8 H<9 7<5A69F G95

K5H9F K5G :I@@M F9D@5798 K=H< CLM;9BG5HIF5H98 9LD9F=A9BH5@ G95K5H9F

K=H< =B=H=5@ 8=GGC@J98 CLM;9B 7CB79BHF5H=CB A95GIF98 IG=B; 5B CDH=75@

8=GGC@J98 CLM;9B DFC69  =6CL  *F9-9BG !9FA5BM .<9 7<5A69F K5G

H<9B 7@CG98 5B8 DIH =BHC 5 K5H9F 65H< 5H H<9 H5F;9H H9AD9F5HIF9 HC A5=B

H5=B H<9 H9AD9F5HIF9 C: 7<5A69F G95K5H9F :H9F  < H<9 YB5@ 8=GGC@J98

CLM;9B 7CB79BHF5H=CB C: H<9 7<5A69F G95K5H9F K5G A95GIF98 8IF=B;

K<=7< ;9BH@9 GH=FF=B; C: 7<5A69F G95K5H9F K5G DFCJ=898 IBH=@ 5 GH56@9

F958=B; K5G F97CF898 @5B? G5AD@9G =9 BC ;5GHFCDC8 K9F9 IG98 HC

7CFF97H H<9 657?;FCIB8 7<5B;9 =B 8=GGC@J98 CLM;9B 7CB79BHF5H=CB ,9G

D=F5H=CB F5H9 K5G 9LDF9GG98 5G CLM;9B 7CBGIA98 D9F Z9G< K9=;<H C: ;5G

HFCDC8 D9F <CIF K<9F9 H<9 Z9G< K9=;<H A95GIF98 CB 5 :F9G< K9=;<H 65

G=G K5G C6H5=B98 H<FCI;< 8=GG97H=CBG H<5H K9F9 7CB8I7H98 5:H9F YB=G<=B;

H<9 :C@@CK=B; 9LD9F=A9BHG

.C EI5BH=:M 56GCFDH=CB F5H9 HKC ;5GHFCDC8G :FCA 957< 5EI5F=IA

K<=7< <58 699B IG98 :CF F9GD=F5H=CB F5H9 A95GIF9A9BH K9F9 GH5FJ98

:CF CB9 85M DF=CF HC H<9 :998=B; HF=5@ .<9M K9F9 H<9B =B8=J=8I5@@M DIH

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208 

Table 1

-95K5H9F 7CB8=H=CBG 8IF=B; H<9 K99? 9LDCGIF9 A95B W - CBHFC@  DDA  U )  DDA  U .9AD  DDA  U )\ .9AD  DDA  U

'95GIF98D5F5A9H9FG 5@7I@5H98D5F5A9H9FG

.F95HA9BH -5@=B=HMDDH .9AD9F5HIF9U D"(-G75@9 .CH5@5@?5@=B=HMμAC@ ?; −p)DDA #μAC@ ?; −Ω75@ Ω5F5

CC@577@=A5H98;5GHFCDC8G

CBHFC@  W   W   W   W   W   W   W   W 

) W   W   W   W   W   W   W   W 

.9AD  W   W   W   W   W   W   W   W 

)\ .9AD  W   W   W   W   W   W   W   W 

15FA577@=A5H98;5GHFCDC8G

CBHFC@  W   W   W   W   W   W   W   W 

) W   W   W   W   W   W   W   W 

.9AD  W   W   W   W   W   W   W   W 

)\ .9AD  W   W   W   W   W   W   W   W 

=BHC 5 7@95B D@5GH=7 7CBH5=B9F Y@@98 K=H<  & C: B5HIF5@ G95K5H9F A5=B

H5=B98 IB89F H<9=F F9GD97H=J9 HF95HA9BH 7CB8=H=CBG n  F9D@=75H9 7CB

H5=B9FG D9F HF95HA9BH D9F DCDI@5H=CB @CHH98 Ulva O ; :F9G< K9=;<H

K5G 58898 =BHC 957< 7CBH5=B9F 5B8 H<9 ;5GHFCDC8G K9F9 5@@CK98 HC :998

H<9 Ulva :CF  < .<9B H<9 Ulva K5G F9ACJ98 6@CHH98 5B8 K9=;<98

.<9 K5H9F 7CBH9BH C: Ulva K5G C6H5=B98 6M CJ9B8M=B; GC H<5H =B;9GH=CB

F5H9 K5G 75@7I@5H98 5G 8FM K9=;<H C: Ulva 7CBGIA98 D9F Z9G< K9=;<H C:

;5GHFCDC8 D9F <CIF .<9 :5979G =B H<9 7CBH5=B9F K9F9 7C@@97H98 F=BG98

K=H< 89=CB=N98 K5H9F 5B8 8F=98 CB 5 DF9K9=;<98 5@IA=B=IA :C=@ HC C6

H5=B H<9 8FM K9=;<H .<9 5G<:F99 8FM K9=;<H C: Ulva 5B8 :5979G K5G 89

H9FA=B98 6M K9=;<H @CGG IDCB =;B=H=CB 5H  U =B 5 AI:Z9 :IFB579 :CF

 < GC H<5H 5GG=A=@5H=CB 9:Y7=9B7M K5G 75@7I@5H98 577CF8=B; HC H<9 :C@

@CK=B; 9EI5H=CB CBCJ9F 

K<9F9 AE =G H<9 5GG=A=@5H=CB 9:Y7=9B7M F′ =G H<9 5G<:F99 8FM K9=;<H HC

8FM K9=;<H F5H=C C: :CC8 E' =G H<9 5G<:F99 8FM K9=;<H HC 8FM K9=;<H F5H=C

C: :5979G

6GCFDH=CB F5H9 K5G ;=J9B 6M H<9 DFC8I7H C: =B;9GH=CB F5H9 5B8 5G

G=A=@5H=CB 9:Y7=9B7M K<9F9 H<9 =B;9GH=CB F5H9 K5G 7CBJ9FH98 =BHC 9B9F;M

9EI=J5@9BH 6M H<9 9B9F;M 7CBH9BH C: Ulva  ?$ ;−:FCA )-I@@=J5B

957<  ?$ ;−:FCA 'I@@5K5M "958@5B8 89H9FA=B98 6M 5 6CA6

75@CF=A9H9F  5G=7 #% !9FA5BM .C EI5BH=:M 9L7F9H=CB F5H9

H<9 G95K5H9F =B H<9 D@5GH=7 7CBH5=B9F K5G 7C@@97H98 5:H9F H<9 :998=B; HF=5@

n  F9D@=75H9 7CBH5=B9FG D9F HF95HA9BH D9F DCDI@5H=CB :C@@CK98 6M

A95GIF=B; H<9 5AACB=IA 7CB79BHF5H=CB C: G95K5H9F IG=B; 5 ZCK =B>97

H=CB 5B5@MG9F +I=?<9A  &57<5H #BGHFIA9BHG /- .<9 5AAC

B=IA 7CB79BHF5H=CBG C: G95K5H9F =B H<9 6@5B? =9 B5HIF5@ G95K5H9F 5B8

7CBHFC@ =9 B5HIF5@ G95K5H9F  Ulva K9F9 A95GIF98 HC 7CFF97H H<9 9L

7F9H=CB F5H9 C: ;5GHFCDC8G L7F9H=CB F5H9 K5G 9LDF9GG98 5G 5AACB=5 9L

7F9H98 D9F Z9G< K9=;<H C: ;5GHFCDC8 D9F <CIF .<9 F5H=C C: CLM;9B 7CB

GIA98 HC 5AACB=5 9L7F9H98 )( F5H=C K5G 75@7I@5H98 5G 5B =B8=75HCF

:CF H<9 IH=@=N5H=CB C: DFCH9=BG 75F6C<M8F5H9G 5B8 @=D=8G :CF 9B9F;M A9

H56C@=GA =B H<9 ;5GHFCDC8G -7CD9 :CF ;FCKH< 5G 5 DFCLM :CF 9B9F;M 6I8

;9H K5G 75@7I@5H98 577CF8=B; HC H<9 :C@@CK=B; 9EI5H=CB

K<9F9 -:! =G G7CD9 :CF ;FCKH< $ ;−<− , =G 56GCFDH=CB F5H9 ,, =G

F9GD=F5H=CB F5H9 , =G 9L7F9H=CB F5H9 ,9GD=F5H=CB F5H9 5B8 9L7F9H=CB F5H9

K9F9 7CBJ9FH98 =BHC 9B9F;M 9EI=J5@9BH IG=B; H<9 7CBJ9FG=CB :57HCFG C:

 $ A; )−5B8  $ μ; ("−@@=CHH 5B8 5J=GCB 

F9GD97H=J9@M

:H9F A95GIF=B; H<9 56CJ9 J5F=56@9G H<9 HCH5@ K9=;<H C: H<9 ;5G

HFCDC8G K5G A95GIF98 IG=B; 5B 9@97HFCB=7 65@5B79 HC H<9 B95F9GH

 ; .<9B H<9M K9F9 8=GG97H98 75F9:I@@M HC C6H5=B H<9 Z9G< K9=;<H

K<=7< K5G :IFH<9F G9D5F5H98 =BHC :CCH K9=;<H 5B8 CF;5B K9=;<H .<9

G<9@@ K9=;<H K5G ;=J9B 6M H<9 8=::9F9B79 69HK99B HCH5@ K9=;<H 5B8 Z9G<

K9=;<H .<9 F5H=C C: Z9G< K9=;<H HC G<9@@ K9=;<H K5G 75@7I@5H98 HC

=B8=75H9 H<9 D9F:CFA5B79 69HK99B GCA5H=7 ;FCKH< 5B8 G<9@@ ;FCKH<

K<9F95G H<9 F5H=C C: CF;5B K9=;<H HC Z9G< K9=;<H K5G 75@7I@5H98 HC =B8=

75H9 9B9F;M F9G9FJ9G &9IB; 9H 5@ 5 .<9 =B=H=5@ J5@I9G C: H<9G9

F5H=CG K9F9 C6H5=B98 IG=B; 588=H=CB5@ ;5GHFCDC8G n  K<=7< K9F9

BCH IG98 :CF H<9 K99? 9LDCGIF9 GC H<5H H<9 9::97HG C: p)5B8 H9A

D9F5HIF9 CB H<9G9 F5H=CG 75B 69 9GH=A5H98

2.4. Thermal threshold

C@@CK=B; H<9 K99? 9LDCGIF9 H<9 F9GD=F5H=CB F5H9 C: ;5GHFCDC8G

K5G A95GIF98 :FCA  U HC  U K=H< 5B =B7F95G=B; H9AD9F5HIF9 F5AD

C:  U <−!=CA= 9H 5@ &9IB; 9H 5@ 6 HC 5GG9GG H<9

H<9FA5@ @=A=H C: 59FC6=7 A9H56C@=GA .<9 @C7CACHCFM 69<5J=CIF C: ;5G

HFCDC8G K5G G=AI@H5B9CIG@M C6G9FJ98 HC 9GH=A5H9 7F=H=75@ H<9FA5@ A5L

=AIA .A5L 5G H<9 H<9FA5@ H<F9G<C@8 =B8=75H98 6M H<9 @CGG C: ACHCF

7CCF8=B5H=CB &IHH9FG7<A=8H 5B8 "IH7<=GCB  .<9 9LD9F=A9B

H5@ DFC798IF9G 89G7F=698 =B &9IB; 9H 5@ 6 K9F9 IG98 K=H< A=

BCF AC8=Y75H=CBG 9:CF9 9LD9F=A9BH5H=CB H<9 G95K5H9F H9AD9F5HIF9 =B

H<9 5EI5F=5 K5G ;F58I5@@M F98I798 :FCA  U CF  U :CF H<9 9@9J5H98

H9AD9F5HIF9 HF95HA9BHG HC  U 5H 5 897F95G=B; F5H9 C:  U 85M−IG=B;

<95H9F7<=@@9F IB=HG . .) #H5@M .<9 ;5GHFCDC8G K9F9 5@@CK98

HC 577@=A5H9 HC H<9 F98I7=B; H9AD9F5HIF9 :CF 5 K99? .<9B CB9 ;5GHFC

DC8 K5G HF5BG:9FF98 =BHC 5  A& 5=FH=;<H 7<5A69F Y@@98 K=H< 9LD9F

=A9BH5@ G95K5H9F 5H  U 5B8 5@@CK98 HC F9GH :CF  < n  F9D@=75H9

7<5A69FG D9F HF95HA9BH D9F DCDI@5H=CB .<9 F9GD=F5H=CB F5H9 K5G A95

GIF98 IG=B; H<9 G5A9 A9H<C8 89G7F=698 56CJ9 G99 -97H=CB  .<9

@C7CACHCFM 69<5J=CIF C: H<9 ;5GHFCDC8G =B H<9 7<5A69FG K5G C6G9FJ98

.A5L =G =B8=75H98 K<9B H<9M :5=@ HC 5HH57< CB H<9 K5@@ C: H<9 7<5A69F

C@@CK=B; 957< A95GIF9A9BH H<9 7<5A69F G95K5H9F K5G :I@@M F9D@5798

K=H< CLM;9BG5HIF5H98 9LD9F=A9BH5@ G95K5H9F 5H H<9 B9LH H9AD9F5HIF9

@9J9@ =9  U =AA98=5H9@M .<=G DFC798IF9 :CF A95GIF=B; F9GD=F5H=CB

F5H9 5B8 C6G9FJ=B; @C7CACHCFM 69<5J=CIF K5G F9D95H98 IG=B; H<9 G5A9

;5GHFCDC8G IBH=@ A95GIF9A9BH :CF H<9 @5GH H9AD9F5HIF9 @9J9@ =9  U

K5G 7CAD@9H98 @5B? G5AD@9G =9 BC ;5GHFCDC8 K9F9 IG98 HC 7CFF97H

H<9 657?;FCIB8 7<5B;9 =B 8=GGC@J98 CLM;9B 7CB79BHF5H=CB

2.5. Statistical analysis

.<9 85H5 C: D<MG=C@C;=75@ D9F:CFA5B79 9B9F;M 6I8;9H 5B8 6C8M 7CB

8=H=CB :FCA H<9 HKC ;5GHFCDC8G D9F 5EI5F=IA K9F9 5J9F5;98 HC F9DF9

G9BH 5 F9D@=75H9 n  F9D@=75H9 5EI5F=5 D9F HF95HA9BH D9F DCDI@5H=CB

.<F99K5M 5B5@MG=G C: J5F=5B79 ()0 K5G 5DD@=98 HC H9GH H<9 9::97HG

C: p) H9AD9F5HIF9 H<9FA5@ <=GHCFM 5B8 H<9=F 7CA6=B5H=CBG CB H<9G9

J5F=56@9G IG=B; GC:HK5F9 *,#',  K=H< *,'(0) 588CB

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208

3. Results

3.1. Thermal threshold

.<9 7CC@577@=A5H98 ;5GHFCDC8G K9F9 69<5J=CIF5@@M =B57H=J9 K=H<

@CK F9GD=F5H=CB F5H9G 5H  U 6IH H<9=F 57H=J=HM @9J9@ ;F58I5@@M =B

7F95G98 5@CB; H<9 H9AD9F5HIF9 F5AD =B 5@@ HF95HA9BHG IBH=@ F957<=B; H<9

D95?  =; 5–8 .<9 F9GD=F5H=CB F5H9G D95?98 5H  U =B 5@@ HF95H

A9BHG 9L79DH :CF H<CG9 9LDCG98 HC H<9 9@9J5H98 H9AD9F5HIF9 =B =GC@5

H=CB D95?   U :C@@CK98 6M 5B C6J=CIG 8FCD BCH<9F D95? =B F9G

D=F5H=CB F5H9G 5DD95F98 5H  U =B 5@@ HF95HA9BHG 69MCB8 K<=7< 5 GI6

GH5BH=5@ 897F95G9 K5G C6G9FJ98 .<9 7CC@577@=A5H98 ;5GHFCDC8G 7CBG=G

H9BH@M @CGH H<9=F 5HH57<A9BH CB H<9 7<5A69F K5@@ 5B8 GI::9F98 :FCA AIG

7@9 GD5GAG 5H  U .56@9 - K<=7< F9DF9G9BH98 H<9=F .A5L

-@=;<H@M 8=::9F9BH D5HH9FBG K9F9 C6G9FJ98 =B H<9 K5FA577@=A5H98

;5GHFCDC8G K<=7< <58 @CK9F F9GD=F5H=CB F5H9G H<5B H<9 7CC@577@=A5H98

;5GHFCDC8G =B 5@@ HF95HA9BHG 6M 5DDFCL=A5H9@M HKC HC H<F99 H=A9G 5H ACGH

C: H<9 H9GH98 H9AD9F5HIF9G 57FCGG H<9 H9AD9F5HIF9 F5AD  =; 5–8

,9GD=F5H=CB F5H9G D95?98 5H  U :CF H<9 7CBHFC@  U :CF 9@9J5H98 p)

5B8 H9AD9F5HIF9 =B =GC@5H=CB 5B8  U :CF H<9=F 7CA6=B5H=CB .<9B H<9

F9GD=F5H=CB F5H9G ;F58I5@@M 897F95G98 K=H< =B7F95G=B; H9AD9F5HIF9 K=H<

CIH H<9 5DD95F5B79 C: 5BCH<9F D95? 9L79DH H<9 7CA6=B98 9@9J5H98 p)

5B8 H9AD9F5HIF9 HF95HA9BH 5H  U 'CGH C: H<9 K5FA577@=A5H98 ;5G

HFCDC8G  F957<98 .A5L 5H  U =FF9GD97H=J9 C: H<9 HF95HA9BH

7CB8=H=CBG .56@9 - A95B=B; H<5H H<9M <58 <=;<9F H<9FA5@ H<F9G<C@8

H<5B H<9 7CC@577@=A5H98 7CIBH9FD5FHG

3.2. Physiological performance and body condition

.<9 F9GD=F5H=CB F5H9G C: H<9 K5FA577@=A5H98 ;5GHFCDC8G K9F9 @CK9F

H<5B H<CG9 C: H<9 7CC@577@=A5H98 ;5GHFCDC8G IB89F 5@@ HF95HA9BH 7CB8=

H=CBG  =; 5 .56@9 - @9J5H98 H9AD9F5HIF9 =B7F95G98 F9GD=F5H=CB

F5H9G F9;5F8@9GG C: p)@9J9@ #B;9GH=CB F5H9G K9F9 5@GC =BZI9B798 6M

H<9FA5@ <=GHCFM K<9F9 H<9 7CC@577@=A5H98 ;5GHFCDC8G <58 <=;<9F :998

=B; F5H9G H<5B H<9 K5FA577@=A5H98 ;5GHFCDC8G 5H 5A6=9BH H9AD9F5

HIF9  =; 6 .56@9 - #B 7CBHF5GH 9@9J5H98 H9AD9F5HIF9 =B =GC@5H=CB

6CCGH98 H<9 :998=B; F5H9G C: ;5GHFCDC8G =FF9GD97H=J9 C: H<9 H<9FA5@ <=G

HCFM 6IH H<=G 9::97H 8=G5DD95F98 K<9B 7CA6=B98 K=H< 9@9J5H98 p)

GG=A=@5H=CB 9:Y7=9B7M K5G =BG=;B=:=75BH@M 5::97H98 6M p) H9AD9F5

HIF9 5B8 H<9FA5@ <=GHCFM  =; 7 .56@9 - 5B8 H<9F9:CF9 H<9 D5HH9FB

C: 56GCFDH=CB F5H9 K5G G=A=@5F HC H<5H C: =B;9GH=CB F5H9  =; 8 .56@9

- L7F9H=CB F5H9G K9F9 F5=G98 6M H<9 9@9J5H98 H9AD9F5HIF9 9GD97=5@@M

:CF H<9 K5FA577@=A5H98 ;5GHFCDC8G  =; 9 .56@9 - B9F;M 6I8

;9H K5G 6CCGH98 6M H<9 9@9J5H98 p)5B8 H9AD9F5HIF9 =B =GC@5H=CB 6IH

H<=G 9::97H K5G B9;5H98 6M H<9=F 7CA6=B5H=CB  =; : .56@9 - .<9

7CC@577@=A5H98 ;5GHFCDC8G <58 <=;<9F 9B9F;M 6I8;9H H<5B H<9 K5FA57

7@=A5H98 ;5GHFCDC8G 5H H<9 5A6=9BH H9AD9F5HIF9

.<9 )( F5H=C C: H<9 K5FA577@=A5H98 ;5GHFCDC8G K5G @CK9F H<5B

H<5H C: H<9 7CC@577@=A5H98 ;5GHFCDC8G K<9F95G p)5B8 H9AD9F5HIF9

<58 =BG=;B=:=75BH 9::97HG  =; 5 .56@9 - CH< Z9G< K9=;<H HC G<9@@

K9=;<H F5H=C 5B8 CF;5B K9=;<H HC Z9G< K9=;<H F5H=C K9F9 IB5::97H98

6M p) H9AD9F5HIF9 5B8 H<9FA5@ <=GHCFM  =; 6 5B8 7 .56@9 -

CAD5F98 HC H<9 =B=H=5@ J5@I9G H<9 Z9G< K9=;<H HC G<9@@ K9=;<H F5H=C

F9A5=B98 F9@5H=J9@M IB7<5B;98 9L79DH :CF H<9 K5FA577@=A5H98 ;5G

HFCDC8G 9LDCG98 HC H<9 9@9J5H98 H9AD9F5HIF9 .<9 CF;5B K9=;<H HC Z9G<

K9=;<H F5H=C =B7F95G98 =B8=75H=B; H<9 577IAI@5H=CB C: 9B9F;M F9G9FJ9G

4. Discussion

)795B K5FA=B; <5G 699B G<CKB HC =AD5=F H<9 YHB9GG C: A5BM A5

F=B9 CF;5B=GAG DCGG=6@M @958=B; HC GI6GH5BH=5@ 7<5B;9G =B H<9=F DCDI@5

H=CBG 5B8 7CAAIB=H=9G "CK9J9F H<9 585DH=J9 75D57=HM C: A5F=B9 CF

;5B=GAG HC 7CD9 K=H< C795B K5FA=B; H<FCI;< @CB;H9FA H<9FA5@ 577@=

Fig. 1. .<9 F9GD=F5H=CB F5H9 C: Turbo undulatus 5@CB; 5B =B7F95G=B; H9AD9F5HIF9 F5AD  U <− :FCA  U HC  U A95B W - n  .<9 ;5GHFCDC8G K=H< 8=::9F9BH H<9FA5@ <=GHC

F=9G K9F9 9LDCG98 HC 8=::9F9BH 7CA6=B5H=CBG C: p)5B8 H9AD9F5HIF9 :CF  K99?G .A5L =B8=75H9G H<9 H9AD9F5HIF9 5H K<=7< H<9 ACHCF 7CCF8=B5H=CB =G @CGH CBHFC@  DDA  U )

 DDA  U .9AD  DDA  U )\ .9AD  DDA  U

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208 

Fig. 2. .<9 9::97HG C: K99? 9LDCGIF9 HC C795B 57=8=Y75H=CB 5B8 K5FA=B; CB H<9 D<MG=C@C;=75@ D9F:CFA5B79 =B7@I8=B; 5 F9GD=F5H=CB F5H9 6 =B;9GH=CB F5H9 7 5GG=A=@5H=CB 9:Y7=9B7M

8 56GCFDH=CB F5H9 9 9L7F9H=CB F5H9 5B8 : 9B9F;M 6I8;9H C: ;5GHFCDC8 Turbo undulatus K<=7< <58 8=::9F9BH H<9FA5@ <=GHCF=9G A95B  - n  CBHFC@  DDA  U )

 DDA  U .9AD  DDA  U )\ .9AD  DDA  U

A5H=CB =G C:H9B IB89F9GH=A5H98 ,C<F 9H 5@  M 7CAD5F=B; H<9

D<MG=C@C;=75@ D9F:CFA5B79 5B8 H<9FA5@ H<F9G<C@8 C: DCDI@5H=CBG K=H<

8=::9F9BH H<9FA5@ <=GHCF=9G 7CC@ JG K5FA K9 F9J95@ H<5H @CB;H9FA

H<9FA5@ 577@=A5H=CB =G 5 7F=H=75@ DFC79GG 5@@CK=B; A5F=B9 CF;5B=GAG HC

F98I79 H<9=F G9BG=H=J=HM HC 7@=A5H9 7<5B;9 K<=7< A5M 5@@CK H<9A HC

D9FG=GH K=H<=B H<9=F 7IFF9BH 8=GHF=6IH=CB @CB;9F H<5B DF98=7H98 =B :IHIF9

C795BG

4.1. Thermal threshold

.<9FA5@ H<F9G<C@8 =G 5 ?9M :57HCF 89H9FA=B=B; H<9 GIG79DH=6=@=HM C:

A5F=B9 CF;5B=GAG HC C795B K5FA=B; G=B79 A5BM J=H5@ D<MG=C@C;=75@

DFC79GG9G 5F9 F9;I@5H98 6M H9AD9F5HIF9 *TFHB9F 9H 5@ &9IB;

9H 5@ 59BB9HH 9H 5@  .<IG A5F=B9 CF;5B=GAG H<5H 5F9

5@F958M @=J=B; 7@CG9 HC H<9=F H<9FA5@ H<F9G<C@8 KCI@8 69 D5FH=7I@5F@M JI@

B9F56@9 HC C795B K5FA=B; (;IM9B 9H 5@  (9J9FH<9@9GG H<9F

A5@ H<F9G<C@8 =G 5 D@5GH=7 HF5=H A95B=B; H<5H A5F=B9 CF;5B=GAG A5M

69 56@9 HC 9LH9B8 H<9=F IDD9F H<9FA5@ @=A=HG =B F9GDCBG9 HC F=G=B; H9A

D9F5HIF9 I7?@9M 5B8 "I9M ,C<F 9H 5@  CF 9L5A

D@9 H<9 HFCD=75@ CMGH9F Isognomon nucleus <5G =B7F95G98 H<9FA5@ H<F9G<

C@8 K<9B DF99LDCG98 HC G<CFHH9FA H<9FA5@ GHF9GG  U =B 5=F :CF  <

=B8=75H=B; D@5GH=7=HM C: D<MG=C@C;=75@ DFC79GG9G HC H<9FA5@ GHF9GG !=CA=

9H 5@  39H K<9H<9F H<=G F9GDCBG9 =G 585DH=J9 5B8 D9FG=GH9BH =B

H<9 @CB; H9FA F9A5=BG IB79FH5=B 6975IG9 =H =B8I79G HF589C[G 9; F9

8I798 :998=B; F5H9G 5B8 H<IG A5M CB@M C::9F H9ADCF5FM F9@=9: :FCA H<9F

A5@ GHF9GG *5F?9F 9H 5@  G GI7< K9 HCC? 5 GH9D :IFH<9F 6M

7CAD5F=B; H<9 IDD9F H<9FA5@ @=A=HG C: ;5GHFCDC8G K=H< 8=::9F9BH H<9FA5@

<=GHCF=9G =9 :C@@CK=B; @CB;H9FA H<9FA5@ 577@=A5H=CB 5B8 :CIB8 H<5H

H<9 K5FA577@=A5H98 ;5GHFCDC8G <58 <=;<9F H<9FA5@ H<F9G<C@8 H<5B H<9

7CC@577@=A5H98 ;5GHFCDC8G K<9F95G H<9 F9@5H=J9@M G<CFHH9FA 9LDCGIF9

=9  K99?G HC C795B 57=8=Y75H=CB 5B8 K5FA=B; CB@M G@=;<H@M G<=:H98

H<9 H<9FA5@ @=A=H C: 59FC6=7 A9H56C@=GA .<9G9 F9GI@HG =AD@M H<5H H<9

@9B;H< C: H<9FA5@ 577@=A5H=CB CF H<9FA5@ <=GHCFM D@5MG 5 7F=H=75@ FC@9 =B

89H9FA=B=B; IDD9F H<9FA5@ @=A=HG 5B8 GI6GH5BH=5H9 H<9 DFCDCG=H=CB H<5H

H<9FA5@ H<F9G<C@8 =G @5F;9@M GI6>97H HC 89J9@CDA9BH5@ 577@=A5H=CB F5H<9F

H<5B 58I@H 577@=A5H=CB %9@@9FA5BB 9H 5@ 

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208

Fig. 3. .<9 9::97HG C: K99? 9LDCGIF9 HC C795B 57=8=Y75H=CB 5B8 K5FA=B; CB H<9 6C8M

7CB8=H=CB =B7@I8=B; 5 )( F5H=C 6 Z9G< K9=;<H HC G<9@@ K9=;<H F5H=C 5B8 7 CF;5B

K9=;<H HC Z9G< K9=;<H F5H=C C: ;5GHFCDC8 Turbo undulatus K<=7< <58 8=::9F9BH H<9FA5@ <=G

HCF=9G A95B W - n 

F5<=A 9H 5@  #B :57H ACGH DF9J=CIG GHI8=9G =;BCF9 89J9@CD

A9BH5@ 577@=A5H=CB =B H<9 9LD9F=A9BH5@ 89G=;B 9; CB@M DFCJ=89 :9K

85MG :CF H<9 58I@HG HC 577@=A5H9 HC H<9 9@9J5H98 H9AD9F5HIF9 5B8 H<9F9

:CF9 H<9 F9GI@HG H9B8 HC F9DF9G9BH HF5BG=9BH F9J9FG=6@9 F9GDCBG9G 9;

<95H<5F89B=B; IBD<M 9H 5@  #B 7CBHF5GH @CB;@5GH=B; =F

F9J9FG=6@9 F9GDCBG9G HC C795B K5FA=B; A=;<H C77IF K<9B A5F=B9 CF

;5B=GAG <5J9 9LD9F=9B798 H<9FA5@ 9J9BHG 8IF=B; 95F@M 89J9@CDA9BH

%9@@9FA5BB 9H 5@ F5<=A 9H 5@  .<9 A97<5B=GA IB

89F@M=B; H<9 =B7F95G9 =B H<9FA5@ H<F9G<C@8 H<FCI;< 89J9@CDA9BH5@ 57

7@=A5H=CB F9A5=BG IB7@95F 6IH =H A5M 69 A98=5H98 6M H<9 F9AC89@

@=B; C: 79@@ A9A6F5B9G CF HF5BG7F=DHCA9 7<5B;9G 8IF=B; CBHC;9BM 5H

H<9 95F@M @=:9 GH5;9G B;=@@9HH5 <9B 9H 5@  #B8998

@=:9 GH5;9G 5F9 =BHF=BG=75@@M @=B?98 5B8 H<9F9:CF9 H<9 9J9BHG 9LD9F=9B798

=B H<9 95F@M @=:9 GH5;9G 75B =BZI9B79 H<9 CF;5B=GA5@ D9F:CFA5B79 =B

H<9 GI6G9EI9BH @=:9 GH5;9G '5FG<5@@ 5B8 'CF;5B &9IB; 5B8

'7:99 &=9GB9F 9H 5@  !9B9H=7 585DH5H=CB A5M 69 5B

CH<9F :57HCF 7CBHF=6IH=B; HC H<9 =B7F95G9 =B H<9FA5@ H<F9G<C@8 6975IG9

D<9BCHMD=7 D@5GH=7=HM 75B 69 A98=5H98 6M ;9B9H=7 7CBHFC@ !<5@5A6CF

9H 5@ -CA9FC  CF 9L5AD@9 H<9 ;9B9 9LDF9GG=CB C:

<95H G<C7? DFCH9=BG K5G A5F?98@M 9@9J5H98 =B H<9 K5FA585DH98 DCDI

@5H=CB C: 7CD9DC8G Tigriopus californicus 7CAD5F98 HC H<9 7CC@585DH98

7CIBH9FD5FH -7<CJ=@@9 9H 5@  =B8=75H=B; H<5H H<9FA5@ HC@9F5B79

75B 69 6CCGH98 H<FCI;< ;9B9H=7 AC8=Y75H=CB 57FCGG 7CBGD97=Y7 DCDI

@5H=CBG *9F9=F5 9H 5@  .C 85H9 <CK ;9B9H=7 8=J9F;9B79 =BZI

9B79G H<9FA5@ 585DH5H=CB <5G F979=J98 F9@5H=J9@M @=HH@9 5HH9BH=CB 5B8 89

G9FJ9G :IFH<9F =BJ9GH=;5H=CB

CAD5F=B; H<9 DFCY@9G C: 59FC6=7 A9H56C@=GA 5@CB; H<9 =B7F95G=B;

H9AD9F5HIF9 F5AD H<9 7CC@577@=A5H98 ;5GHFCDC8G <58 <=;<9F F9GD=F5

H=CB F5H9G =9 69=B; ACF9 A9H56C@=75@@M 57H=J9 H<5B H<CG9 :FCA H<9

K5FA577@=A5H98 DCDI@5H=CB 39H H<9 7CC@577@=A5H98 ;5GHFCDC8G <58

5 G<5FD9F 897@=B9 =B F9GD=F5H=CB F5H9G 5:H9F F957<=B; H<9 D95? GI;;9GH

=B; <=;<9F G9BG=H=J=HM HC H<9FA5@ GHF9GG H<5H DCGG=6@M F9GI@HG :FCA ;F95H9F

CLM;9B 89A5B8 :CF A5=BH9B5B79 -9AG5F?5N9FCIB= 5B8 09F69F?

 1<9B CLM;9B GIDD@M 697CA9G =BGI:Y7=9BH HC A99H =B7F95G=B;

CLM;9B 89A5B8 :CF 9B9F;M A9H56C@=GA 8I9 HC H9AD9F5HIF9 F=G9 GCA9 J=

H5@ D<MG=C@C;=75@ DFC79GG9G B998 HC 69 G<IH 8CKB H<9F96M IB89FA=B=B;

CF;5B=GA5@ D9F:CFA5B79 *TFHB9F -C?C@CJ5 9H 5@  #B

H<=G F9;5F8 H<9 K5FA577@=A5H98 ;5GHFCDC8G DCH9BH=5@@M <5J9 5 ;F95H9F

75D57=HM HC F9GDCB8 HC C795B K5FA=B; 6975IG9 C: H<9=F @CK9F CLM;9B 89

A5B8 5B8 69HH9F F9;I@5HCFM 75D57=HM :CF CLM;9B 7CBGIADH=CB K<=7< F9

8I79 H<9=F @=?9@=<CC8 HC GI::9F :FCA <MDCL=5 =B8I798 6M H<9FA5@ GHF9GG

09F69F? 5B8 =@HCB -99657<9F 9H 5@  -=A=@5F F9

GI@HG <5J9 699B C6G9FJ98 =B 5AD<=DC8G K<9F9 K5FA577@=A5H98 DCD

I@5H=CBG <58 @CK9F CLM;9B 89A5B8 5B8 <=;<9F H<9FA5@ H<F9G<C@8 H<5B

7C@8577@=A5H98 7CIBH9FD5FHG '55NCIN= 9H 5@ -9AG5F?5N9F

CIB= 5B8 09F69F?  GI;;9GH=B; H<5H H<9FA5@ H<F9G<C@8 =G 5GGC

7=5H98 K=H< H<9 65@5B79 69HK99B CLM;9B GIDD@M 5B8 89A5B8 *TFHB9F

 #B8998 F98I7=B; 59FC6=7 A9H56C@=GA =G 7CBG=89F98 5B 585DH=J9

GHF5H9;M :CF GIFJ=J=B; =B H<9FA5@@M GHF9GG:I@ 9BJ=FCBA9BHG H<FCI;< H<9

F98I7H=CB =B 9B9F;M 9LD9B8=HIF9 '5FG<5@@ 9H 5@ '5FG<5@@ 5B8

'7+I5=8 09F69F? 9H 5@ &9IB; 9H 5@ 5

1<=@9 H<9 G<CFHH9FA 9LDCGIF9 HC C795B 57=8=Y75H=CB 5B8 K5FA=B;

<58 BC C6G9FJ56@9 9::97H CB H<9 H<9FA5@ H<F9G<C@8 .A5L C: Tundula-

tus H<9M AC8I@5H98 H<9 H9AD9F5HIF9 C: A5L=AIA 59FC6=7 A9H56C@=GA

CF 9L5AD@9 D95? A9H56C@=GA 5DD95F98 5H  U K<9B H<9 7CC@577@=

A5H98 ;5GHFCDC8G K9F9 9LDCG98 HC K5FA=B; =B =GC@5H=CB 6IH F98I798

HC  U K<9B H<9M K9F9 9LDCG98 HC 7CA6=B98 9@9J5H98 p)5B8 H9A

D9F5HIF9 #ADCFH5BH@M 5 G=A=@5F D5HH9FB K5G :CIB8 =B H<9 K5FA577@=

A5H98 DCDI@5H=CB GI;;9GH=B; H<5H C795B 57=8=Y75H=CB B5FFCKG H<9 H<9F

A5@ K=B8CKG C: 59FC6=7 A9H56C@=GA 5B8 =B7F95G9G H<9 G9BG=H=J=HM HC H<9F

A5@ GHF9GG *TFHB9F 5B8 5FF9@@ 15B; 9H 5@  #B :57H

A5BM A5F=B9 CF;5B=GAG GI::9F :FCA <MD9F75DB=5 IB89F C795B 57=8=Y

75H=CB 8I9 HC H<9 IB7CAD9BG5H98 897F95G9 =B 9LHF579@@I@5F D" 9J9B

HI5@@M 75IG=B; A9H56C@=7 89DF9GG=CB '=7<59@=8=G 9H 5@ =G

G5B5M5?9 9H 5@ *TFHB9F  #BH9F9GH=B;@M 5 G97CB8 D95?

=B H<9 DFCY@9 C: 59FC6=7 A9H56C@=GA K5G 7CBG=GH9BH@M C6G9FJ98 =B H<9

7CC@577@=A5H98 ;5GHFCDC8G 5H  U -=B79 H<=G H9AD9F5HIF9 =G DCGG=6@M

<=;< 9BCI;< HC 75IG9 @9H<5@ AC@97I@5F 85A5;9 9; DFCH9=B 89B5HIF5

H=CB *TFHB9F 9H 5@  GI7< 5 8F5GH=7 =B7F95G9 =B 59FC6=7 A9H56

C@=GA A5M 69 8F=J9B 6M H<9 CBG9H C: 9B9F;M89A5B8=B; AC@97I@5F 89

:9B79 F9GDCBG9G 9; DFC8I7H=CB C: <95H G<C7? DFCH9=BG 5B8 5BH=CL=85BH

9BNMA9G CB; 9H 5@ *TFHB9F &9IB; 9H 5@ 5

5G H<9 @5GH F9GCFH HC 7CIBH9F :5H5@ H<9FA5@ GHF9GG .<9 6=AC85@=HM C: 59F

C6=7 A9H56C@=GA 5@CB; H<9 =B7F95G=B; H9AD9F5HIF9 F5AD =G BCH ;9B9F

5@@M C6G9FJ98 =B GI6H=85@ CF;5B=GAG &9IB; 9H 5@ 6 "9A

F5> 9H 5@  6IH =G F9DCFH98 =B GCA9 =BH9FH=85@ CF;5B=GAG 9;

AC@@IG7G K=H< 5 G97CB8 D95? H<5H 5DD95FG 56CJ9 H<9FA5@@M =BG9BG=

H=J9 6F95?DC=BH H9AD9F5HIF9G '5FG<5@@ 9H 5@ 09F69F? 9H 5@

"I= 9H 5@  #B CIF GHI8M <CK9J9F BC G97CB8 D95? K5G

C6G9FJ98 =B H<9 K5FA577@=A5H98 DCDI@5H=CB ?9DH IB89F 9=H<9F 5A6=9BH

CF 9@9J5H98 H9AD9F5HIF9G =AD@M=B; @9GG 89D9B89B79 CB H<9 9B9F;M7CGH@M

<95H G<C7? F9GDCBG9G H<5H 5F9 BCH 585DH=J9 =B H<9 @CB; H9FA 8I9 HC 9B

9F;M HF589C[G 1=@GCB 5B8 F5B?@=B F5<=A 9H 5@ 

.<=G YB8=B; :IFH<9F 7CFFC6CF5H9G H<9 DFCDCG=H=CB H<5H 9B9F;M7CBG9FJ

=B; A9H56C@=7 89DF9GG=CB =G 5 69B9Y7=5@ GHF5H9;M 5@@CK=B; D9FG=GH9B79 IB

89F 57IH9@M GHF9GG:I@ H<9FA5@ 9BJ=FCBA9BHG '5FG<5@@ 5B8 '7+I5=8

09F69F? 9H 5@ '5AC 9H 5@  CF =BGH5B79 H<9

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208 

59FC6=7 A9H56C@=GA C: ;5GHFCDC8 Echinolittorina malaccana K5G 89

DF9GG98 K=H<=B =HG H<9FA5@@M =BG9BG=H=J9 NCB9 69HK99B  U 5B8  U

5B8 CB@M =B7F95G98 56CJ9  U HC 57H=J5H9 <95H G<C7? F9GDCBG9 IBH=@

F957<=B; FF<9B=IG 6F95?DC=BH H9AD9F5HIF9  U K<9F96M H<9 @=A=H98

9B9F;M ;5=B IB89F H<9FA5@@M GHF9GG:I@ 7CB8=H=CBG 75B 69 CJ9F7CA9 '5F

G<5@@ 9H 5@  1<5H =G IB7@95F <CK9J9F =G H<9 9LH9BH HC K<=7<

H<=G GHF5H9;M C: 9B9F;M 7CBG9FJ5H=CB A5M 69 A5@585DH=J9 =B H<9 @CB;9F

H9FA

4.2. Physiological performance and body condition

.<9FA5@ <=GHCFM A5M G<=:H H<9 CDH=A5@ H9AD9F5HIF9 F5B;9 C: CF;5B

=GAG 5B8 <9B79 5::97H H<9=F D<MG=C@C;=75@ D9F:CFA5B79 5B8 9B9F;M 6I8

;9H 19 :CIB8 H<5H 59FC6=7 A9H56C@=GA K5G @5F;9@M 5::97H98 6M H<9FA5@

<=GHCFM K<9F9 H<9 K5FA577@=A5H98 DCDI@5H=CB <58 7CBG=GH9BH@M @CK9F

F9GD=F5H=CB F5H9G H<5B H<9 7CC@577@=A5H98 DCDI@5H=CB D5FH :FCA H<9

@CB;H9FA H<9FA5@ 577@=A5H=CB HC H<9 K5FA9F 9BJ=FCBA9BH G99 -97H=CB

 H<=G C6G9FJ5H=CB A5M 69 6975IG9 H<9 5A6=9BH H9AD9F5HIF9  U

=G H<9 GIAA9F H9AD9F5HIF9 B5HIF5@@M 9LD9F=9B798 6M H<9 7CC@577@=A5H98

DCDI@5H=CB 6IH =G H<9 K=BH9F H9AD9F5HIF9 6M H<9 K5FA577@=A5H98 DCD

I@5H=CB K<=7< =G 7@CG9F HC H<9 9EI5HCF=5@ 8=GHF=6IH=CB @=A=H C: H<=G GD97=9G

-I7< 8=::9F9B79 =B H<9 D9F79DH=CB C: G95GCB5@=HM 6M H<9 ;5GHFCDC8G A5M

5::97H H<9=F 57H=J=HM @9J9@ '=F5B85 9H 5@  ,9;5F8@9GG C: H<9F

A5@ <=GHCFM H<9 F9GD=F5H=CB F5H9G C: ;5GHFCDC8G K9F9 6CCGH98 6M K5FA

=B; 6975IG9 ACF9 A9H56C@=7 9B9F;M B998G HC 69 ;9B9F5H98 =B CF89F HC

A99H H<9 ;F95H9F 9B9F;M 89A5B8 :CF A5=BH9B5B79 5H H<9 <=;<9F H9AD9F

5HIF9 *TFHB9F 9H 5@  "CK9J9F CH<9F GI6H=85@ <9F6=JCFCIG ;5G

HFCDC8G Thalotia conica 5B8 Phasianella australis K=H< 5 G=A=@5F 8=GHF=6

IH=CB HC Tundulatus 8=8 BCH <5J9 =B7F95G98 59FC6=7 A9H56C@=GA :C@@CK

=B; DFC@CB;98 577@=A5H=CB HC H<9 9@9J5H98 H9AD9F5HIF9 5H  U &9IB;

9H 5@ 6  .<=G C6G9FJ5H=CB A5M F9GI@H :FCA H<9 GI6@9H<5@

H<9FA5@ GHF9GG =ADCG98 CB Tconica 5B8 Paustralis K<=7< <5J9 @CK9F

H<9FA5@ H<F9G<C@8 .A5L  U H<5B Tundulatus .A5L – U

.<9 K5FA577@=A5H98 ;5GHFCDC8G ;9B9F5@@M <58 @CK9F =B;9GH=CB F5H9G

H<5B H<9=F 7CC@577@=A5H98 7CIBH9FD5FHG 6975IG9 H<9 :CFA9F F9EI=F9 @9GG

9B9F;M =BH5?9 HC A5=BH5=B 9B9F;M <CA9CGH5G=G =B J=9K C: @CK9F F9GD=F5

H=CB F5H9G &9IB; 9H 5@ 5 .<=G C6G9FJ5H=CB 5DD95FG HC 7CAD@M

K=H< H<9 A9H56C@=7 H<9CFM C: 97C@C;M H<5H H<9 A9H56C@=7 F5H9 C: CF;5B

=GAG ;CJ9FBG ACGH C: H<9 6=C@C;=75@ F5H9G =B7@I8=B; :998=B; F5H9 K<9B

589EI5H9 F9GCIF79G 5F9 5J5=@56@9 FCKB 9H 5@ %=XF6C9 5B8

"=FGH IF89B 9H 5@  (9J9FH<9@9GG H<9 :998=B; D9F

:CFA5B79 C: ;5GHFCDC8G K5G :IFH<9F AC8I@5H98 6M C795B 57=8=Y75H=CB

5B8 K5FA=B; CF =BGH5B79 H<9 ;5GHFCDC8G <58 <=;<9F :998=B; F5H9G IB

89F C795B K5FA=B; K<=7< 75B <9@D C[G9H H<9 <=;<9F 9B9F;M 89A5B8

:CF A5=BH9B5B79 &9IB; 9H 5@  "CK9J9F H<=G 6CCGH=B; 9::97H

K5G F9J9FG98 6M C795B 57=8=Y75H=CB A95B=B; H<5H H<9 :998=B; D9F:CF

A5B79 C: ;5GHFCDC8G 6975A9 ACF9 GIG79DH=6@9 HC H<9 58J9FG9 9::97HG C:

=B7F95G98 57=8=HM ,IGG9@@ 9H 5@ %9DD9@ 9H 5@ &9IB;

9H 5@ (5J5FFC 9H 5@  -I7< F98I798 :998=B; D9F:CF

A5B79 BCH CB@M 8=A=B=G<9G H<9 9B9F;M 6I8;9H C: =B8=J=8I5@ <9F6=JCF9G

6IH A5M 5::97H DF=A5FM DFC8I7H=J=HM 5B8 9B9F;M ZCK K=H<=B :CC8 K96G

 9FF9=F5 9H 5@  1<9F9 7@=A5H9 8F=J9G =B7F95G98 :998=B; D9F:CF

A5B79 9; *FCJCGH 9H 5@  GMGH9AK=89 DFC8I7H=J=HM A5M 5@GC

=B7F95G9 K<9B GIDDCFH98 6M 9B<5B798 DF=A5FM DFC8I7H=J=HM CI6@9

85M 9H 5@ 

.<9 IH=@=N5H=CB C: A57FCBIHF=9BHG :CF 9B9F;M A9H56C@=GA 75B 69 =B

8=75H98 6M )( F5H=C K<9F9 DFCH9=BG 5F9 DF98CA=B5BH@M IG98 K<9B )(

F5H=C =G @CK9F H<5B  -BCK 5B8 1=@@=5AG &5B;9B6I7< 5B8

*TFHB9F  #B H<=G GHI8M H<9 )( F5H=C C: H<9 K5FA577@=A5H98

;5GHFCDC8G K5G @CK9F H<5B H<5H C: H<9=F 7CC@577@=A5H98 7CIBH9FD5FHG

8I9 HC H<9 @CK9F F9GD=F5H=CB F5H9G 39H DFCH9=BG K9F9 GH=@@ BCH GI6GH5B

H=5@@M IG98 6M H<9 K5FA577@=A5H98 ;5GHFCDC8G :CF 9B9F;M A9H56C@=GA 5G

H<9 )( F5H=C K5G <=;<9F H<5B  .<9 <=;<9F )( F5H=C C: H<9 7CC@57

7@=A5H98 ;5GHFCDC8G GI;;9GHG H<5H 75F6C<M8F5H9G 5B8 @=D=8G K9F9 A5=B@M

IG98 5G H<9 9B9F;M GCIF79 HC :I9@ H<9 <=;<9F F9GD=F5H=CB 5B8 :998=B;

F5H9G -C?C@CJ5 9H 5@  *FC@CB;98 9LDCGIF9 HC C795B 57=8=Y75

H=CB 5B8 K5FA=B; 9;   ACBH< <5G 699B G<CKB HC IB89FA=B9 H<9

6C8M 7CB8=H=CB C: A5F=B9 CF;5B=GAG &9IB; 9H 5@ 6  #B

7CBHF5GH K9 :CIB8 H<5H H<9 ;5GHFCDC8G :FCA 6CH< DCDI@5H=CBG <58 =B

7F95G98 9B9F;M F9G9FJ9G =9 <=;<9F CF;5B K9=;<H HC Z9G< K9=;<H F5H=C

K<=7< =G IB89FD=BB98 6M H<9 DCG=H=J9 9B9F;M 6I8;9H =9 9B9F;M GIFD@IG

5B8 <95@H<M 7CB8=H=CBG H<FCI;<CIH H<9 9LDCGIF9 39H C795B 57=8=Y75H=CB

5DD95F98 HC 5@H9F H<9 D9F:CFA5B79 69HK99B GCA5H=7 ;FCKH< 5B8 G<9@@

;FCKH< C: H<9 K5FA577@=A5H98 ;5GHFCDC8G 5H H<9 9@9J5H98 H9AD9F5HIF9

.<9 F98I798 Z9G< K9=;<H HC G<9@@ K9=;<H F5H=C 7: =B=H=5@ J5@I9 =B8=

75H9G H<5H G<9@@ ;FCKH< =G F9@5H=J9@M :5GH9F H<5B GCA5H=7 ;FCKH< H<IG CIF

YB8=B;G F9J95@ H<5H G<9@@ 6I=@8=B; K5G :57=@=H5H98 6M C795B K5FA=B; 6IH

H<=G DCG=H=J9 9::97H K5G F9J9FG98 6M C795B 57=8=Y75H=CB #B8998 C795B

57=8=Y75H=CB 75B 7CADFCA=G9 G<9@@ ;FCKH< 6M F98I7=B; 9B9F;M 6I8;9H

:CF G<9@@ 6I=@8=B; &9IB; 9H 5@ 6 5 =B7F95G=B; 9B9F;M

7CGHG C: 75@7=Y75H=CB 5B8 <CA9CGH5G=G *TFHB9F -D5@8=B; 9H 5@

 5B8 75IG=B; G<9@@ 8=GGC@IH=CB MFB9 5B8 =HN9F &9IB;

9H 5@ 6

4.3. Implications for the e@ects of ocean warming on marine organisms

/DD9F H<9FA5@ H<F9G<C@8 5B8 D<MG=C@C;=75@ D9F:CFA5B79 5F9 :F9

EI9BH@M 5GG9GG98 HC 897=D<9F H<9 =AD57HG C: C795B K5FA=B; CB H<9 YH

B9GG 5B8 GIFJ=J5@ C: A5F=B9 CF;5B=GAG 1<=@9 G<CFHH9FA 58I@H 577@=

A5H=CB =G C:H9B D9F:CFA98 HC 9F58=75H9 H<9 9::97HG C: Y9@8 7CB8=H=CBG

CB 9LD9F=A9BH5@ CF;5B=GAG DF9J=CIG GHI8=9G H9B8 HC CJ9F@CC? @CB;H9FA

H<9FA5@ 577@=A5H=CB CF H<9FA5@ <=GHCFM H<5H DCH9BH=5@@M 7CB:CIB8G H<9

9::97HG C: C795B K5FA=B; #B :57H H<9 H=A=B; 5B8 @9B;H< C: 577@=A5

H=CB D9F=C8 75B ;F95H@M 5::97H H<9 H<9FA5@ F9GDCBG9 C: A5F=B9 CF;5B

=GAG ,9N9B89 9H 5@ -99657<9F 9H 5@ F5<=A 9H 5@

 CF 9L5AD@9 H<9 H<9FA5@ HC@9F5B79 C: H<9 5AD<=DC8 Gammarus

fossarum =B7F95G98 K=H< H<9 @9B;H< C: 577@=A5H=CB D9F=C8 -9AG5F?5N9

FCIB= 5B8 09F69F?  GI;;9GH=B; H<5H @CB;H9FA H<9FA5@ 577@=

A5H=CB 5@@CKG A5F=B9 CF;5B=GAG HC 6I[9F H<9 9::97HG C: C795B K5FA=B;

"9F9 K9 F9J95@ H<5H IDD9F H<9FA5@ H<F9G<C@8 5B8 D<MG=C@C;=75@ D9F:CF

A5B79 K9F9 DF98CA=B5BH@M 5::97H98 6M H<9FA5@ <=GHCFM F5H<9F H<5B F9@

5H=J9@M G<CFHH9FA 9LDCGIF9 HC H<9 5@H9F98 G95K5H9F 7CB8=H=CBG =AD@M=B;

H<5H H<9 9::97HG C: C795B K5FA=B; A5M 69 A=G=BH9FDF9H98 =B GCA9 =B

GH5B79G G=B79 H<9FA5@ <=GHCFM =G G9@8CA 7CBG=89F98 =B H<9 9LD9F=A9BH5@

5GG9GGA9BHG .<9 9LH9B898 H<9FA5@ HC@9F5B79 .A5L =B H<9 K5FA57

7@=A5H98 DCDI@5H=CB =G DCGG=6@M 5 7CBG9EI9B79 C: 585DH=J9 D<MG=C@C;=75@

58>IGHA9BHG  =;  =B7@I8=B; A9H56C@=7 F5H9 5B8 AC@97I@5F 89:9B79

=9 79@@I@5F GHF9GG F9GDCBG9 K<=7< 75B 9BGIF9 A5=BH9B5B79 C: D<MG=

C@C;=75@ :IB7H=CB 5B8 GIFJ=J5@ =B K5FA9F 9BJ=FCBA9BHG #B8998 A5BM

A5F=B9 CF;5B=GAG 5F9 G<CFH@=J98 5B8 GA5@@G=N98 H<9F9:CF9 H<9M 5F9 9L

D97H98 HC <5J9 5 <=;< 75D57=HM HC 577@=A5H9 CF 585DH HC H<9 G@CK =B

7F95G=B; F5H9 C: H9AD9F5HIF9 57FCGG AI@H=D@9 ;9B9F5H=CBG 'CF@9M 9H 5@

,C<F 9H 5@  .C C6H5=B 5 ACF9 97C@C;=75@@MF9@9J5BH 9J5@

I5H=CB C: H<9 =AD57HG C: K5FA=B; 5B8 57=8=:M=B; C795BG H<9 H=A9G75@9 C:

9LD9F=A9BHG G<CI@8 69 9LH9B898 9; @5FJ59 HC >IJ9B=@9G ,IGG9@@ 9H 5@

*5F?9F 9H 5@ &9IB; 5B8 '7:99 &=9GB9F 9H 5@

 6975IG9 89J9@CDA9BH5@ 577@=A5H=CB 5DD95FG HC 5::97H H<9 H<9FA5@

H<F9G<C@8 5B8 <9B79 GIFJ=J5@ C: A5F=B9 CF;5B=GAG =B :IHIF9 C795BG

5. Conclusion

M 7CAD5F=B; H<9 D<MG=C@C;=75@ D9F:CFA5B79 C: ;5GHFCDC8G :FCA HKC

DCDI@5H=CBG K=H< 8=::9F9BH H<9FA5@ <=GHCF=9G 7CC@ JG K5FA H<=G GHI8M

<=;<@=;<HG H<9 GI6GH5BH=5@ FC@9 C: @CB;H9FA H<9FA5@ 577@=A5H=CB H<5H

A5M 5@@CK DCDI@5H=CBG HC 58>IGH HC 7<5B;=B; 7@=A5H9 CJ9F H<9 @CB;

H9FA 19 G<CK F98I798 G9BG=H=J=HM C: 5 ;5GHFCDC8 HC 7@=A5H9 7<5B;9

K<9F9 =B8=J=8I5@G 89F=J98 :FCA AI@H=D@9 ;9B9F5H=CBG C: 5 K5FA9F 7@=

A5H9 <5J9 5 ;F95H9F 75D57=HM HC 58>IGH H<9=F A9H56C@=7 F5H9 5B8 7CB

G9FJ9 9B9F;M HC D9FG=GH =B K5FA9F 5B8 ACF9 57=8=7 9BJ=FCBA9BHG  =;

 .<9G9 C6G9FJ5H=CBG DC=BH HC 5B =B<9F9BH 58>IGH56=@=HM C: A5F=B9 CF

;5B=GAG 5B8 5 DCH9BH=5@ 75D57=HM :CF H<9=F D9FG=GH9B79 IB89F :IHIF9 7@=

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208

Fig. 4.  7CB79DHI5@ 8=5;F5A =@@IGHF5H=B; H<9 585DH=J9 D<MG=C@C;=75@ 58>IGHA9BHG C: ;5G

HFCDC8G :C@@CK=B; @CB;H9FA H<9FA5@ 577@=A5H=CB =B8=75H98 6M H<9 7<5B;9 =B 59FC6=7 A9

H56C@=GA 5@CB; 5B =B7F95G=B; H9AD9F5HIF9 F5AD 9FC6=7 A9H56C@=GA K5G @5F;9@M GI6>97H

HC H<9 H<9FA5@ <=GHCFM C: ;5GHFCDC8G ;=J9B H<9 @5F;9 7<5B;9 =B F9GD=F5H=CB F5H9G 75IG98 6M

H<9FA5@ 577@=A5H=CB F9@5H=J9 HC H<9 GA5@@ J5F=5H=CB 75IG98 6M G<CFHH9FA 9LDCGIF9 HC C795B

57=8=Y75H=CB 5B8 K5FA=B; G<CKB 6M H<9 G<5898 5F95 =9  7CBY89B79 =BH9FJ5@ :H9F

@CB;H9FA H<9FA5@ 577@=A5H=CB H<9 ;5GHFCDC8G K9F9 56@9 HC  =ADFCJ9 F9;I@5H=CB C: CLM

;9B 7CBGIADH=CB =9 F98I798 F5H9 C: 7<5B;9 5@CB; H<9 H9AD9F5HIF9 F5AD  A=B=A=G9

9B9F;M 9LD9B8=HIF9 6M F98I7=B; F9GD=F5H=CB F5H9G  =B7F95G9 H<9 IDD9F H<9FA5@ H<F9G<C@8

=9 9LH9B898 .A5L  F9@M @9GG CB H<9 9B9F;M89A5B8=B; <95H G<C7? F9GDCBG9G =B8=

75H98 6M H<9 56G9B79 C: G97CB8 D95? 5H H<9 9LHF9A9 H9AD9F5HIF9 .<9 7IFJ9G K9F9 YHH98

6M !5IGG=5B 8=GHF=6IH=CB K<9F9 H<9 6=AC85@=HM :CF H<9 7CC@577@=A5H98 ;5GHFCDC8G =G YHH98

6M H<9 GIA C: HKC !5IGG=5B 8=GHF=6IH=CBG

A5H=7 7CB8=H=CBG

Declaration of competing interest

.<9 5IH<CFG 897@5F9 H<5H H<9M <5J9 BC ?BCKB 7CAD9H=B; YB5B7=5@ =B

H9F9GHG CF D9FGCB5@ F9@5H=CBG<=DG H<5H 7CI@8 <5J9 5DD95F98 HC =BZI9B79

H<9 KCF? F9DCFH98 =B H<=G D5D9F

Acknowledgements

-IDDCFH K5G DFCJ=898 6M H<9 IB85A9BH5@ ,9G95F7< IB8G :CF H<9

9BHF5@ /B=J9FG=H=9G -1/ <=B5 *CGH8C7HCF5@ -7=9B79 CIB85

H=CB !F5BH HC $3-& ' IGHF5@=5B ,9G95F7< CIB7=@ =G

7CJ9FM *FC;F5A ;F5BH HC , - 5B8 *% * 5 Uni-

versitas 21 9@@CKG<=D HC , 5B8 , IHIF9 9@@CKG<=D HC -

 .

Appendix A. Supplementary data

-IDD@9A9BH5FM 85H5 HC H<=G 5FH=7@9 75B 69 :CIB8 CB@=B9 5H <HHDG8C=

CF;>G7=HCH9BJ

References

B;=@@9HH5 '$  .<9FA5@ 85DH5H=CB  .<9CF9H=75@ 5B8 AD=F=75@ -MBH<9G=G )/*

)L:CF8

9BB9HH - I5FH9 ' '5F6P ( 19FB69F; .  #BH9;F5H=B; K=H<=B GD97=9G

J5F=5H=CB =B H<9FA5@ D<MG=C@C;M =BHC 7@=A5H9 7<5B;9 97C@C;M *<=@ .F5BG , -C7 

 

F5<=A  'IGH5D<5 ( '5FG<5@@ $  (CBF9J9FG=6@9 5B8 F9J9FG=6@9 <95H

HC@9F5B79 D@5GH=7=HM =B HFCD=75@ =BH9FH=85@ 5B=A5@G F9GDCB8=B; HC <56=H5H H9AD9F5HIF9

<9H9FC;9B9=HM FCBH *<MG=C@  

FCKB $" !=@@CC@M $  @@9B * -5J5;9 0' 19GH !  .CK5F8 5 A9H56C@=7

H<9CFM C: 97C@C;M 7C@C;M  –

I7?@9M & "I9M ,  "CK 9LHF9A9 H9AD9F5HIF9G =AD57H CF;5B=GAG 5B8 H<9

9JC@IH=CB C: H<9=F H<9FA5@ HC@9F5B79 #BH9;F CAD =C@  –

MFB9 ' =HN9F -  .<9 =AD57H C: 9BJ=FCBA9BH5@ 57=8=Y75H=CB CB H<9

A=7FCGHFI7HIF9 5B8 A97<5B=75@ =BH9;F=HM C: A5F=B9 =BJ9FH96F5H9 G?9@9HCBG CBG9FJ

*<MG=C@  7CN

<9B $ (C@H9 0 -7<@CHH9F9F   .9AD9F5HIF9 F9@5H98 F957H=CB BCFAG C: ;9B9

9LDF9GG=CB F9;I@5HCFM 5F7<=H97HIF9 5B8 :IB7H=CB5@ =AD@=75H=CBG 'C@ =C@ JC@ 

–

CBCJ9F ,$  GG=A=@5H=CB C: CF;5B=7 A5HH9F 6M NCCD@5B?HCB &=ABC@ )795BC;F

 –

=7?GCB ! '=@@9FC $   7CAD5F=GCB C: H<9 9EI=@=6F=IA 7CBGH5BHG :CF H<9

8=GGC7=5H=CB C: 75F6CB=7 57=8 =B G95K5H9F A98=5 99D -95 ,9G   –

=GG5B5M5?9  @CI;< , -D=79F $# $CB9G '  [97HG C: <MD9F75DB=5 CB

57=8–65G9 65@5B79 5B8 CGAC=CBCF9;I@5H=CB =B DF5KBG 975DC85 *5@59ACB=859

EI5H =C@  –

CB; 3 3I - 15B; + CB; -  *<MG=C@C;=75@ F9GDCBG9G =B 5 J5F=56@9

9BJ=FCBA9BH F9@5H=CBG<=DG 69HK99B A9H56C@=GA "GD 5B8 H<9FACHC@9F5B79 =B 5B

=BH9FH=85@GI6H=85@ GD97=9G *&C- )B9  9

CI6@985M 4 (5;9@?9F?9B # CIHHG ' !C@89B69F; -/ CBB9@@ -  

HF=D@9 HFCD<=7 6CCGH <CK 75F6CB 9A=GG=CBG =B8=F97H@M 7<5B;9 5 A5F=B9 :CC8 7<5=B

!@C6 <5B;9 =C@  –

IBD<M $ ,I;;=9FC % 45ACF5 &( ,5;; (&  '9H56C@CA=7 5B5@MG=G C:

<95H<5F89B=B; =B 58I@H ;F99B@=DD98 AIGG9@ Perna canaliculus 5 ?9M FC@9 :CF GI77=B=7

57=8 5B8 H<9 !ergic GMB5DG9 D5H<K5M $ .<9FA =C@  –

IF89B $' 9HH $ "I[5F8 & ,I<@ " -A=H< %&  6MGG5@

89DCG=H:998=B; F5H9G 7CBG=GH9BH K=H< H<9 A9H56C@=7 H<9CFM C: 97C@C;M 7C@C;M 

9

@@=CHH $' 5J=GCB 1  B9F;M 9EI=J5@9BHG C: CLM;9B 7CBGIADH=CB =B 5B=A5@

9B9F;9H=7G )97C@C;=5  –

9FF9=F5 ' (5;9@?9F?9B # !C@89B69F; -/ 15@89B ! &9IB; $3- CBB9@@ -

 IB7H=CB5@ @CGG =B <9F6=JCF9G 8F=J9G FIB5K5M 9LD5BG=CB C: K998M 5@;59 =B 5

B95F:IHIF9 C795B -7= .CH5@ BJ=FCB  

!<5@5A6CF % '7%5M $% 5FFC@@ -* ,9NB=7? (  85DH=J9 J9FGIG

BCB585DH=J9 D<9BCHMD=7 D@5GH=7=HM 5B8 H<9 DCH9BH=5@ :CF 7CBH9ADCF5FM 585DH5H=CB =B

B9K 9BJ=FCBA9BHG IB7H 7C@  –

!=CA=  '5B85;@=C  !5BA5B99 ' "5B ! CB; 31 1=@@=5AG ! -5FP !

 .<9 =ADCFH5B79 C: H<9FA5@ <=GHCFM 7CGHG 5B8 69B9YHG C: <95H 9LDCGIF9 =B 5

HFCD=75@ FC7?M G<CF9 CMGH9F $ LD =C@  –

!@5B8CB "& '=@@9F .$  (C 9[97H C: <=;< p)CB >IJ9B=@9 6@I9 7F56 Callinectes

sapidus ;FCKH< 5B8 7CBGIADH=CB 89GD=H9 DCG=H=J9 F9GDCBG9G HC 7CB7IFF9BH K5FA=B;

#- $ '5F -7=  –

"9AF5>  *CGB9HH ( '=BIH= $$ =FH< & ,IGG9@@   -IFJ=J98 6IH BCH

G5:9 A5F=B9 <95HK5J9 <=B89FG A9H56C@=GA =B HKC ;5GHFCDC8 GIFJ=JCFG '5F BJ=FCB

,9G  

"C7<57<?5 *1 -CA9FC !(  =C7<9A=75@ 85DH5H=CB '97<5B=GA 5B8 *FC79GG

=B *<MG=C@C;=75@ JC@IH=CB )L:CF8 /B=J9FG=HM *F9GG (9K 3CF?

"I= .3 CB; 31 "5B ! &5I -&3 <9B; '  '99DC?5  !5BA5B99

' 1=@@=5AG !  .=A=B; A9H56C@=7 89DF9GG=CB DF98=7H=B; H<9FA5@ GHF9GG =B

9LHF9A9 =BH9FH=85@ 9BJ=FCBA9BHG A (5H  –

#*  -IAA5FM :CF DC@=7MA5?9FG #B *TFHB9F ") ,C69FHG  '5GGCB9@ACHH9

0 4<5= * .=;BCF ' *C@C7N5BG?5  '=BH9B697? % (=7C@5= ' )?9A 

*9HNC@8 $ ,5A5  19M9F ( 8G #* -D97=5@ ,9DCFH CB H<9 )795B 5B8

FMCGD<9F9 =B 5 <5B;=B; @=A5H9

%9@@9FA5BB 0 J5B "99FK55F89B  -;FS '  "CK =ADCFH5BH =G H<9FA5@ <=GHCFM

J=89B79 :CF @5GH=B; 9[97HG C: 89J9@CDA9BH5@ H9AD9F5HIF9 CB IDD9F H<9FA5@ @=A=HG =B

Drosophila melanogaster *FC7 , -C7   

%9DD9@  -7FCG5H= , CIFH9B5M -  #BH9F57H=J9 9[97HG C: C795B 57=8=Y75H=CB

5B8 K5FA=B; CB GI6H=85@ AIGG9@G 5B8 G95 GH5FG :FCA H@5BH=7 5B585 '5F =C@ ,9G

 –

%=XF6C9 . "=FGH !  -<=:HG =B A5GG G75@=B; C: F9GD=F5H=CB :998=B; 5B8 ;FCKH<

F5H9G 57FCGG @=:9:CFA HF5BG=H=CBG =B A5F=B9 D9@5;=7 CF;5B=GAG A (5H 

–

&5B;9B6I7< ' *TFHB9F ")  <5B;9G =B A9H56C@=7 F5H9 5B8 ( 9L7F9H=CB =B H<9

A5F=B9 =BJ9FH96F5H9 Sipunculus nudus IB89F 7CB8=H=CBG C: 9BJ=FCBA9BH5@ <MD9F75DB=5

$ LD =C@  –

&9IB; $3- '7:99   -HF9GG 57FCGG @=:9 GH5;9G =AD57HG F9GDCBG9G 5B8

7CBG9EI9B79G :CF A5F=B9 CF;5B=GAG -7= .CH5@ BJ=FCB  

&9IB; $3- ,IGG9@@  CBB9@@ - (; $3 &C ''3  7=8 8I@@G H<9

G9BG9G =AD5=F98 @C7CACH=CB 5B8 :CF5;=B; D9F:CFA5B79 =B 5 A5F=B9 AC@@IG? B=A

9<5J  –

&9IB; $3- ,IGG9@@  CBB9@@ - 5 '=B9F5@C;=75@ D@5GH=7=HM 57HG 5G 5

7CAD9BG5HCFM A97<5B=GA HC H<9 =AD57HG C: C795B 57=8=Y75H=CB BJ=FCB -7= .97<BC@

 –

&9IB; $3- CBB9@@ - ,IGG9@@  6 "95HK5J9G 8=A=B=G< H<9 GIFJ=J5@ C:

5 GI6H=85@ ;5GHFCDC8 H<FCI;< F98I7H=CB =B 9B9F;M 6I8;9H 5B8 89D@9H=CB C: 9B9F;M

F9G9FJ9G -7= ,9D  

&9IB; $3- (5;9@?9F?9B # ,IGG9@@  9FF9=F5 ' CBB9@@ -  CCGH98

BIHF=H=CB5@ EI5@=HM C: :CC8 6M )9BF=7<A9BH :5=@G HC C[G9H 9B9F;M 89A5B8 C:

<9F6=JCF9G IB89F C795B K5FA=B; 75IG=B; 9B9F;M 89D@9H=CB 5B8 ACFH5@=HM -7= .CH5@

BJ=FCB  –

&9IB; $3- ,IGG9@@  CBB9@@ - 5 85DH=J9 F9GDCBG9G C: A5F=B9 ;5GHFCDC8G

HC <95HK5J9G )B9 5FH<  –

&9IB; $3- CI6@985M 4 (5;9@?9F?9B # <9B 3 2=9 4 CBB9@@ - 6

"CK 75@CF=9F=7< :CC8 7CI@8 <9@D A5F=B9 75@7=Y9FG =B 5 )F=7< :IHIF9 *FC7 , -C7

  

&9IB; $3- ,IGG9@@  CBB9@@ - 5 &=B?=B; 9B9F;M 6I8;9H HC D<MG=C@C;=75@

585DH5H=CB <CK 5 75@7=:M=B; ;5GHFCDC8 58>IGHG CF GI77IA6G HC C795B 57=8=Y75H=CB 5B8

K5FA=B; -7= .CH5@ BJ=FCB  

&9IB; $3- <9B 3 (5;9@?9F?9B # 4<5B; - 2=9 4 CBB9@@ - 6 5@7=Y9FG

75B 58>IGH G<9@@ 6I=@8=B; 5H H<9 B5BCG75@9 HC F9G=GH C795B 57=8=Y75H=CB -A5@@ 



&=9GB9F  -<5A5 &(- =9<@ ( 05@9BH=B % 5FHG7< #  .<9FA5@ D@5GH=7=HM

C: H<9 ?9@D laminaria digitata *<59CD<M7959 57FCGG @=:9 7M7@9 GH5;9G F9J95@G H<9

=ADCFH5B79 C: 7C@8 G95GCBG :CF A5F=B9 :CF9GHG FCBH '5F -7=  

&IHH9FG7<A=8H 1# "IH7<=GCB 0"  .<9 7F=H=75@ H<9FA5@ A5L=AIA <=GHCFM 5B8

7F=H=EI9 5B $ 4CC@  –

'55NCIN=  *=G75FH  &9;=9F  "9FJ5BH   7CD<MG=C@C;=75@ F9GDCBG9G HC

H9AD9F5HIF9 C: H<9 “?=@@9F G<F=AD”Dikerogammarus villosus =G H<9 =BJ589F F95@@M

GHFCB;9F H<5B H<9 B5H=J9 Gammarus pulex CAD =C7<9A *<MG=C@  'C@ #BH9;F

*<MG=C@  –

UNCORRECTED PROOF

J.Y.S. Leung et al. / Science of the Total Environment xxx (xxxx) 145208 

'589=F5  (5F7=GC & 56F5@ "( 0=B5;F9   .<9FA5@ HC@9F5B79 5B8 DCH9BH=5@

=AD57HG C: 7@=A5H9 7<5B;9 CB 7C5GH5@ 5B8 9GHI5F=B9 CF;5B=GAG $ -95 ,9G  –

'5;CNN= - 5@CG= *  #BH9;F5H=B; A9H56C@=7 D9F:CFA5B79 H<9FA5@ HC@9F5B79 5B8

D@5GH=7=HM 9B56@9G :CF ACF9 577IF5H9 DF98=7H=CBG CB GD97=9G JI@B9F56=@=HM HC 57IH9 5B8

7<FCB=7 9[97HG C: ;@C65@ K5FA=B; !@C6 <5B; =C@  –

'5AC &. 9B?9B8CF[ % IH7<9F=B9 * C@9A5B ' K9F9  '=F5B85 ,$

19FB69F; . %5@5<9F *  ,9G=@=9B79 C: 5 <5FJ9GH98 ;5GHFCDC8 Turbo militaris

HC A5F=B9 <95HK5J9G '5F BJ=FCB ,9G  

'5FG<5@@ $ '7+I5=8   15FA=B; F98I79G A9H56C@=7 F5H9 =B A5F=B9 GB5=@G

585DH5H=CB HC ZI7HI5H=B; <=;< H9AD9F5HIF9G 7<5@@9B;9G H<9 A9H56C@=7 H<9CFM C:

97C@C;M *FC7 , -C7   –

'5FG<5@@ $ 'CF;5B -!  7C@C;=75@ 5B8 9JC@IH=CB5FM 7CBG9EI9B79G C: @=B?98

@=:9 <=GHCFM GH5;9G =B H<9 G95 IFF =C@  ,–,

'5FG<5@@ $ CB; 31 1=@@=5AG ! '7+I5=8   .<9FA5@ 585DH5H=CB =B

H<9 =BH9FH=85@ GB5=@ Echinolittorina malaccana 7CBHF58=7HG 7IFF9BH H<9CFM 6M F9J95@=B;

H<9 7FI7=5@ FC@9G C: F9GH=B; A9H56C@=GA $ LD =C@  –

'9<F657<  I@69FGC " "5K@9M $ *MH?CK=7 ,'  '95GIF9A9BH C:

5DD5F9BH 8=GGC7=5H=CB7CBGH5BHG C: 75F6CB=757=8 =B G95K5H9F 5H 5HACGD<9F=7DF9GGIF9

&=ABC@ )795BC;F  –

'=7<59@=8=G  )INCBI=G  *5@9F5G  *TFHB9F ")  [97HG C: @CB;H9FA

AC89F5H9 <MD9F75DB=5 CB 57=8–65G9 65@5B79 5B8 ;FCKH< F5H9 =B A5F=B9 AIGG9@G

Mytilus galloprovincialis '5F 7C@ *FC; -9F  –

'=F5B85 ,$ C@9A5B ' .5;@=5Y7C  ,5B;9@ '- '5AC &. 5FFCG  %9@5<9F

*  #BJ5G=CBA98=5H98 9[97HG CB A5F=B9 HFCD<=7 =BH9F57H=CBG =B 5 7<5B;=B;

7@=A5H9 DCG=H=J9 :998657?G :5JCIF ?9@D D9FG=GH9B79 *FC7 , -C7   

'CF@9M - (;IM9B % *97? &- &5= " .5B %  5B 577@=A5H=CB C: H<9FA5@

HC@9F5B79 =B 58I@HG 5B8 57FCGG ;9B9F5H=CBG 57H 5G 5 6I[9F 5;5=BGH 7@=A5H9 7<5B;9 =B

HFCD=75@ A5F=B9 97HCH<9FAG $ .<9FA =C@  –

(5;9@?9F?9B # CBB9@@ -  !@C65@ 5@H9F5H=CB C: C795B 97CGMGH9A :IB7H=CB=B; 8I9

HC =B7F95G=B; <IA5B )9A=GG=CBG *FC7 (5H@ 758 -7=  –

(5J5FFC $' I5FH9  '5BFQEI9N *" &5F8=9G ' .CFF9G , 7IR5 % 05F;5G

 &5;CG (  )795B K5FA=B; 5B8 9@9J5H98 75F6CB 8=CL=89 AI@H=D@9

GHF9GGCF =AD57HG CB >IJ9B=@9 AIGG9@G :FCA GCIH<9FB <=@9 #- $ '5F -7= 

–

(;IM9B %. 'CF@9M - &5= " @5F? '- .5B %- 5H9G  *97? &- 

/DD9F H9AD9F5HIF9 @=A=HG C: HFCD=75@ A5F=B9 97HCH<9FAG ;@C65@ K5FA=B; =AD@=75H=CBG

*&C- )B9  9

*5F?9F &' )’CBBCF 1 MFB9 ' C@9A5B , 0=FHI9 * CJ9 ' !=66G

' -DC<F & -75B9G  ,CGG *'  8I@H 9LDCGIF9 HC C795B 57=8=Y75H=CB =G

A5@585DH=J9 :CF @5FJ59 C: H<9 -M8B9M FC7? CMGH9F Saccostrea glomerata =B H<9 DF9G9B79

C: AI@H=D@9 GHF9GGCFG =C@ &9HH  

*9F9=F5 ,$ -5G5?= ' IFHCB ,-  85DH5H=CB HC 5 @5H=HI8=B5@ H<9FA5@ ;F58=9BH

K=H<=B 5 K=89GDF958 7CD9DC8 GD97=9G H<9 7CBHF=6IH=CBG C: ;9B9H=7 8=J9F;9B79 5B8

D<9BCHMD=7 D@5GH=7=HM *FC7 , -C7   

*=9FFCH  &9K=G  15@@579 1,  '- 9L79@ DFC;F5A 89J9@CD98 :CF )GMGH9A

75@7I@5H=CBG #B ),(&#5 .9BB9GG99 5F6CB =CL=89 #B:CFA5H=CB B5@MG=G

9BH9F )5? ,=8;9 (5H=CB5@ &56CF5HCFM /- 9D5FHA9BH C: B9F;M )5? ,=8;9

*C@C7N5BG?5 - IFFCKG '. FCKB $ 'C@=BCG $! "5@D9FB -

"C9;<!I@869F; ) %5DD9@ 0 'CCF9 *$ ,=7<5F8GCB $ -7<C9A5B -

-M89A5B 1$  ,9GDCBG9G C: A5F=B9 CF;5B=GAG HC 7@=A5H9 7<5B;9 57FCGG C795BG

FCBH '5F -7=  

*TFHB9F ")  #BH9;F5H=B; 7@=A5H9F9@5H98 GHF9GGCF 9[97HG CB A5F=B9 CF;5B=GAG

IB=:M=B; DF=B7=D@9G @=B?=B; AC@97I@9 HC 97CGMGH9A@9J9@ 7<5B;9G '5F 7C@ *FC; -9F

 –

*TFHB9F ") 5FF9@@ *  *<MG=C@C;M 5B8 7@=A5H9 7<5B;9 -7=9B79  –

*TFHB9F ") C7?  '5F?   )LM;9B 5B8 75D57=HM@=A=H98 H<9FA5@ HC@9F5B79

6F=8;=B; 97C@C;M 5B8 D<MG=C@C;M $ LD =C@  –

*F585  5FCG9@@=  '9B;C@= - F=N= & 5BH5NN=B= * 5D577=CB=  *5GEI=B=

& 56F=7=IG % I6=BG?M 4 5@=B= ! !C[F98C -  )795B K5FA=B; 5B8

57=8=Y75H=CB GMB9F;=GH=75@@M =B7F95G9 7CF5@ ACFH5@=HM -7= ,9D  

*FCJCGH $ %9@5<9F * KCF>5BMB - ,IGG9@@  CBB9@@ - !<98=B= !

!=@@5B89FG ' =;I9=F5 1 C@9A5B '  @=A5H98F=J9B 8=GD5F=H=9G 5ACB;

97C@C;=75@ =BH9F57H=CBG H<F95H9B ?9@D :CF9GH D9FG=GH9B79 !@C6 <5B;9 =C@ 

–

,9N9B89 & 5GH5R985 & -5BHCG '  .C@9F5B79 @5B8G75D9G =B H<9FA5@ 97C@C;M

IB7H 7C@  –

,C<F $, =J=H9@@C $ C<9B $' ,CNB=?  -=B9FJC  9@@ #  .<9

7CAD@9L 8F=J9FG C: H<9FA5@ 577@=A5H=CB 5B8 6F958H< =B 97HCH<9FAG 7C@ &9HH 

–

,IGG9@@  "5F@9M ! 19FB69F; . '=9GN?CKG?5 ( 1=88=7CA69 -

"5@@-D9B79F $' CBB9@@ -  *F98=7H=B; 97CGMGH9A G<=:HG F9EI=F9G B9K

5DDFC57<9G H<5H =BH9;F5H9 H<9 9[97HG C: 7@=A5H9 7<5B;9 57FCGG 9BH=F9 GMGH9AG =C@

&9HH  –

,IGG9@@  CBB9@@ - =B8@5M "- .5=H % 1=88=7CA69 - '=9GN?CKG?5 (

 )795B 57=8=Y75H=CB 5B8 F=G=B; H9AD9F5HIF9G A5M =B7F95G9 6=CY@A DF=A5FM

DFC8I7H=J=HM 6IH 897F95G9 ;F5N9F 7CBGIADH=CB 9J=89B79 :FCA 5 A9GC7CGA 9LD9F=A9BH

*<=@CG .F5BG , -C7   

-7<CJ=@@9 - 5FF9HC - 'CM !1 1C@[  IFHCB ,-  #BJ9GH=;5H=B; H<9

AC@97I@5F 65G=G C: @C75@ 585DH5H=CB HC H<9FA5@ GHF9GG DCDI@5H=CB 8=[9F9B79G =B ;9B9

9LDF9GG=CB 57FCGG H<9 HF5BG7F=DHCA9 C: H<9 7CD9DC8 Tigriopus californicus ' JC@

=C@  

-99657<9F  1<=H9 , F5B?@=B   *<MG=C@C;=75@ D@5GH=7=HM =B7F95G9G

F9G=@=9B79 C: 97HCH<9FA=7 5B=A5@G HC 7@=A5H9 7<5B;9 (5H @=A <5B;  –

-9AG5F?5N9FCIB= ' 09F69F? 1*  #H’G 56CIH H=A9 @=B?5;9G 69HK99B <95H

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Warmer and more acidic conditions enhance performance of an endemic low shore gastropod

Article

May 2023
J EXP BIOL

Changing ocean temperatures are predicted to challenge marine organisms, especially when combined with other factors, such as ocean acidification. Acclimation, as a form of phenotypic plasticity, can however, moderate the consequences of changing environments for biota. Our understanding of how altered temperature and acidification together influence species acclimation responses is, however, limited compared to responses to single stressors. This study investigated how temperature and acidification affected the thermal tolerance and righting speed of the Girdled Dogwhelk, Trochia cingulata (Linnaeus, 1771). Whelks were acclimated for two weeks to combinations of three temperatures (11°C: cold, 13°C: moderate and 15°C: warm) and two pH regimes (8.0: moderate and 7.5: acidic). We measured the temperature sensitivity of righting response by generating thermal performance curves from individual data collected at seven test temperatures and determined critical thermal minima (CTmin) and maxima (CTmax). We found that T. cingulata has a broad basal thermal tolerance range (∼38°C) and after acclimation to the warm temperature regime, both the optimal temperature for maximum righting speed and CTmax increased. Contrary to predictions, acidification did not narrow this population's thermal tolerance but increased CTmax. These plastic responses are likely driven by the predictable exposure to temperature extremes measured in the field which originate from the local tidal cycle and the periodic acidification associated with ocean upwelling in the region. This acclimation ability suggests that T. cingulata has at least some capacity to buffer the thermal changes and increased acidification predicted to occur with climate change.

Evidence of corallivorous gastropod Drupella cornus breeding on the higher latitude reefs of Rottnest Island (32°S), Western Australia

Article

Full-text available

Dec 2023
MAR BIOL

With increasing sea water temperatures, higher latitude temperate and sub-tropical coral reefs are becoming increasingly tropicalised. Although these cooler areas might offer refuge to tropical species escaping the heat, the reshaping of ecosystems can have devastating effects on the biodiversity in these areas, especially when habitat structure is affected. Recently, feeding aggregations of corallivorous gastropod Drupella cornus, a tropical species capable of large-scale reef degradation, were found at Rottnest Island in Western Australia (32°S). We provide evidence that D. cornus spawned at Rottnest Island for 2 consecutive years in 2021 and 2022, and Drupella veligers from an egg case collected at the island hatched and grew at temperatures in the laboratory that were predominantly lower than those at Rottnest Island at the same time. The spawning was possibly triggered by higher than usual La Niña-associated SSTs during the survey period, or the long period of high sea water temperature anomalies recorded around Rottnest Island. A spawning population of D. cornus can greatly affect these higher latitude reef areas, especially when accompanied by increased heat stress. Monitoring and management should be implemented to further understand what effects a breeding population of D. cornus has on Rottnest Island.

The added costs of winter ocean warming for metabolism, arm regeneration and survival in the brittle star, Ophionereis schayeri (Müller & Troschel, 1844)

Article

Jan 2023
J EXP BIOL

As the climate continues to change, it is not only the magnitude of these changes that is important, but equally critical is the timing of these events. Conditions that may be well tolerated at one time, may be detrimental if experienced at another due to seasonal acclimation. Temperature is the most critical variable as it affects most aspects of an organism's physiology. To address this, we quantified arm regeneration and respiration in the Australian brittle star, Ophionereis schayeri, for 10 weeks in response to a +3˚C warming (18.5˚C, simulating a winter heatwave) compared to ambient winter temperature (15.5˚C). The metabolic scaling rate (b=0.635 at 15.5 ˚C and 0.746 at 18.5 ˚C) with respect to size is similar to other echinoderms and was not affected by temperature. Elevated temperature resulted in up to a 3-fold increase in respiration and doubling of regeneration growth, however mortality was greater (up to 44.2% at 18.5°C), especially in the regenerating brittle stars. Metabolic rates of the brittle stars held at 18.5˚C were much higher than expected (Q10 ∼23) and similar to O. schayeri tested in summer that were near their estimated thermotolerance limits. The additional costs associated with the elevated metabolism and regeneration rates incurred by the unseasonably warm winter temperatures may lead to increased mortality and predation risk.

Mussels show capacity for persistence under, and recovery from, marine heatwaves

Article

Full-text available

Aug 2023
MAR BIOL

The ability of marine organisms to persist under, and recover from, periods of stressful conditions will shape their occurrence in future oceans characterized by exacerbated marine heatwaves (MHWs). Organism persistence and recovery may, in turn, be shaped by traits of the organisms themselves including, for example, body size. In the present study, we tested the responses (survival, heart rate, Arrhenius breakpoint temperature – ABT, clearance rate, respiration rate, and condition index) of large (5 cm) and small (3 cm) Perna viridis mussels after exposure to a three-week marine heatwave (MHW; + 4 °C) and a one-week recovery period. Exposure to elevated temperatures did not affect the survival of large or small mussels, however, at the end of the MHW both size classes exhibited increased heart rate under elevated temperatures, small mussels exhibited increased ABT, and large mussels exhibited significantly increased clearance rate. Following one week of recovery at control temperature, the altered responses had returned to be similar to those of mussels held under control conditions. The results obtained here indicate that both sizes of mussels can readily recover from exposure to short-term elevated temperatures imposed by MHWs, enabling the continued persistence of P. viridis mussels in future oceans.

Short-term exposure to independent and combined acidification and warming elicits differential responses from two tropical seagrass-associated invertebrate grazers

Article

Full-text available

Aug 2023
MAR BIOL

Ocean acidification and warming could affect animal physiology, key trophic interactions and ecosystem functioning in the long term. This study investigates the effects of four pH−temperature combination treatments simulating ocean acidification (OA), ocean warming (OW) and combined OA and OW conditions (FUTURE) relative to ambient present-day conditions (PRESENT) on the grazing of the juveniles of two seagrass-associated invertebrates namely the sea cucumber Stichopus cf. horrens and topshell Trochus maculatus over a 5-day exposure period. Diel and feeding activity of both species increased under OW and FUTURE to some extent, while the nighttime activity of Trochus but not Stichopus decreased under OA relative to PRESENT during the first 2 days. Fecal production of Stichopus did not differ among treatments, while the lowest fecal production of Trochus was observed under OA during the first 24 h of grazing. These responses suggest that Trochus may be initially more sensitive to OA compared with Stichopus. Interestingly, fecal production of Trochus in FUTURE was significantly higher than OA, suggesting that warming may ameliorate the negative effect of acidification. Diel activity, feeding and fecal production after 5 days did not differ among treatments for both species, suggesting acclimation to the acute changes in temperature and pH after a few days, although Stichopus acclimated rapidly than Trochus. The ability of the two juvenile invertebrate grazers to rapidly acclimate to increased temperature and lowered pH conditions after short-term exposure may favor their survival under projected changes in ocean conditions.

Northern shrimp from multiple origins show similar sensitivity to global change drivers, but different cellular energetic capacity

Article

Jul 2023
J EXP BIOL

Species with a wide distribution can experience regionally a wide range of environmental conditions, to which they can acclimatize or adapt. Consequently, the geographic origin of an organism can influence its responses to environmental changes, and therefore its sensitivity to combined global change drivers. This study aimed at determining the physiological responses of the northern shrimp Pandalus borealis, at different levels of biological organization and from four different geographic origins, exposed to elevated temperature and low pH to define its sensitivity to future ocean warming (OW) and acidification (OA). Shrimp sampled within the northwest Atlantic, were exposed for 30 days to combinations of three temperature (2, 6 or 10 °C) and two pH levels (7.75 or 7.40). Survival, metabolic rates, whole-organism aerobic performance and cellular energetic capacity were assessed at the end of the exposure. Our results show that shrimp survival was negatively affected by temperature above 6 °C and low pH, regardless of their origin. Additionally, shrimp from different origins show overall similar whole-organism performances: aerobic scope increasing with increasing temperature and decreasing with decreasing pH. Finally, the stability of aerobic metabolism appears to be related to cellular adjustments specific to shrimp origin. Our results show that the level of intraspecific variation differs among levels of biological organization: different cellular capacities lead to similar individual performances. Thus, the northern shrimp sensitivity to OW and OA is overall comparable among origins. Nonetheless, shrimp vulnerability to predicted global change scenarios for 2100 could differ among origins due to different regional environmental conditions.

Contrasting behavioural responses to ocean acidification and warming have the potential to disrupt herbivory

Article

Full-text available

Feb 2023

Global change has the potential to affect organisms and re-structure ecosystems where key species interactions, such as herbivory, are disrupted. The fastest ways individual herbivores – and therefore ecosystems – can respond to climate change is through shifts in behaviour. In marine habitats, environmental changes of particular concern in the future are ocean acidification and warming. Consequently, we reviewed the existing literature in this area of research, to identify if there were any over-arching trends or emerging patterns in behavioural responses of marine herbivores to ocean acidification and warming. We identified that while the body of research is growing, focus remains primarily on few locations (temperate areas), phyla (Mollusca, especially gastropods; Crustacea; Echinodermata), and behaviours (grazing rate, movement). Although representing a relatively narrow view of future herbivory, this review indicates that in many cases, the key behaviours of feeding and movement could be maintained under ocean acidification and warming. However, where change is observed, it is more likely grazing will be enhanced and movement impaired. If such patterns were to manifest under future climates, it would mean that the herbivores present would consume more yet there may be less of them as impaired movement and escape behaviours would have made them more vulnerable to predation. The exact responses will, however, likely be context-dependant. Therefore, we recommend future studies address the research gaps our review identified (i.e., a lack of understanding in tropical and polar regions, economically and ecologically important Crustacean and Echinoderm species, early life history stages, and more behavioural responses in addition to feeding and movement). Understanding the diversity of responses expected under varied contexts will be important to uncover trends in how marine invertebrates will behave under global change.

Blue appendages and temperature acclimation increase survival during acute heat stress in the upside-down jellyfish, Cassiopea xamachana

Preprint

Mar 2024

Upside-down jellyfish ( Cassiopea sp. ) are highly tolerant to multiple abiotic stressors, including fluctuating temperatures associated with shallow marine habitats. This resilience may underlie the ability of Cassiopea sp. to inhabit a wide variety of tropical habitats across the globe. Additionally, Cassiopea sp. are marked by a conspicuous array of appendage coloration; individual medusae vary in the hue and number of oral appendages, which are often strikingly blue. The function of this coloration is not understood. We aimed to understand how extrinsic and intrinsic factors may shape thermal tolerance. Adult Cassiopea xamachana were collected from two sites that vary in daily temperature range within the Florida Keys and were subjected to acute lethal heat stress experiments. To quantify a whole-organism response to heat, we measured changes in bell pulsation, which likely plays a role in feeding, oxygen exchange, and symbiont uptake. Results show that C. xamachana from the two collection sites do not exhibit different responses to heat, suggesting that temperature fluctuations do not prime individuals for higher thermal tolerance. Additionally, C. xamachana with blue appendages survived significantly higher temperatures and exhibited less change in bell pulsation rates compared to non-blue individuals. Finally, color morphs were acclimated at either ambient (26 °C) or elevated (33 °C) temperatures. We found that acclimation at 33 °C, as well as appendage color in each treatment, led to higher survival under acute heat stress. Together, these findings highlight the importance of phenotypic plasticity and coloration in Cassiopea resilience during heat stress.

Embryonic encapsulated development of the gastropod Acanthina monodon is impacted by future environmental changes of temperature and pCO2

Article

Mar 2023
MAR ENVIRON RES

Egg capsules of the gastropod Acanthina monodon were maintained during the entire period of encapsulated development at three temperatures (10, 15, 20 °C) and two pCO2 levels (400, 1200 μatm). Embryos per capsule, size at hatching, time to hatching, embryonic metabolic rates, and the resistance of juveniles to shell breakage were quantified. No embryos maintained at 20 °C developed to hatching. The combination of temperature and pCO2 levels had synergistic effects on hatching time and developmental success, antagonistic effects on number of hatchlings per capsule, resistance to juvenile shell cracking and metabolism, and additive effect on hatching size. Juveniles hatched significantly sooner at 15 °C, independent of the pCO2 level that they had been exposed to, while individuals hatched at significantly smaller sizes if they had been held under 15 °C/1200 μatm rather than at 10 °C/low pCO2. Embryos held at the higher pCO2 had a significantly greater percentage of abnormalities. For capsules maintained at low pCO2 and 15 °C, emerging juveniles had less resistance to shell breakage. Embryonic metabolism was significantly higher at 15 °C than at 10 °C, independent of pCO2 level. The lower metabolism occurred in embryos maintained at the higher pCO2 level. Thus, in this study, temperature was the factor that had the greatest effect on the encapsulated development of A. monodon, increasing the metabolism of the embryos and consequently accelerating development, which was expressed in a shorter intracapsular development time, but with smaller individuals at hatching and a lower resistance of their shells to breakage. On the other hand, the high pCO2 level suppressed metabolism, prolonged intracapsular development, and promoted more incomplete development of the embryos. However, the combination of the two factors can mitigate--to some extent--the adverse effects of both incomplete development and lower resistance to shell breakage.

Warming Affects Bioconcentration and Bioaccumulation of Per- and Polyfluoroalkyl Substances by Pelagic and Benthic Organisms in a Water–Sediment System

Article

Feb 2023

Warming and exposure to emerging global pollutants, such as per- and polyfluoroalkyl substances (PFAS), are significant stressors in the aquatic ecosystem. However, little is known about the warming effect on the bioaccumulation of PFAS in aquatic organisms. In this study, the pelagic organisms Daphnia magna and zebrafish, and the benthic organism Chironomus plumosus were exposed to 13 PFAS in a sediment-water system with a known amount of each PFAS at different temperatures (16, 20, and 24 °C). The results showed that the steady-state body burden (Cb-ss) of PFAS in pelagic organisms increased with increasing temperatures, mainly attributed to increased water concentrations. The uptake rate constant (ku) and elimination rate constant (ke) in pelagic organisms increased with increasing temperature. In contrast, warming did not significantly change or even mitigate Cb-ss of PFAS in the benthic organism Chironomus plumosus, except for PFPeA and PFHpA, which was consistent with declined sediment concentrations. The mitigation could be explained by the decreased bioaccumulation factor due to a more significant percent increase in ke than ku, especially for long-chain PFAS. This study suggests that the warming effect on the PFAS concentration varies among different media, which should be considered for their ecological risk assessment under climate change.

Calcifiers can Adjust Shell Building at the Nanoscale to Resist Ocean Acidification

Article

Full-text available

Aug 2020
SMALL

Ocean acidification is considered detrimental to marine calcifiers based on laboratory studies showing that increased seawater acidity weakens their ability to build calcareous shells needed for growth and protection. In the natural environment, however, the effects of ocean acidification are subject to ecological and evolutionary processes that may allow calcifiers to buffer or reverse these short‐term negative effects through adaptive mechanisms. Using marine snails inhabiting a naturally CO2‐enriched environment over multiple generations, it is discovered herein that they build more durable shells (i.e., mechanically more resilient) by adjusting the building blocks of their shells (i.e., calcium carbonate crystals), such as atomic rearrangement to reduce nanotwin thickness and increased incorporation of organic matter. However, these adaptive adjustments to future levels of ocean acidification (year 2100) are eroded at extreme CO2 concentrations, leading to construction of more fragile shells. The discovery of adaptive mechanisms of shell building at the nanoscale provides a new perspective on why some calcifiers may thrive and others collapse in acidifying oceans, and highlights the inherent adaptability that some species possess in adjusting to human‐caused environmental change.

Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests

Article

Full-text available

Jun 2020

Phenotypic plasticity (genotype × environment interaction) is an especially important means for sessile organisms to cope with environmental variation. While kelps, the globally most productive group of seaweeds, generally possess a wide thermal performance range, kelp populations at their warm distribution limits are threatened by ocean warming. Here, we investigated effects of temperature during ontogeny of the kelp Laminaria digitata across haploid gametophyte and diploid sporophyte life cycle stages in five distinct genetic lines. We hypothesized that thermal plasticity increases trait performance of juvenile sporophytes in experimental temperatures that match the temperature experienced during gametogenesis and recruitment, and that plasticity differs among genetic lines (genetic variation for plasticity). We applied a full-factorial experimental design to generate different temperature histories by applying 5 and 15°C during meiospore germination, gametogenesis of parental gametophytes and recruitment of offspring sporophytes (19–26 days), and juvenile sporophyte rearing (91–122 days). We then tested for thermal plasticity among temperature history treatments at 5 and 15°C in a final 12-day experiment assessing growth, the storage compound mannitol, carbon and nitrogen contents, and fluorometric responses in 3–4 month old sporophytes for five genetic lines. Our study provides evidence for the importance of cold temperatures at early development on later sporophyte performance of L. digitata. Gametogenesis and recruitment at 5°C promoted higher growth of offspring sporophytes across experimental temperatures. While photosynthetic capacity was higher at 15°C, carbon and nitrogen storage were higher at 5°C, both showing fast acclimation responses. We identified an important role of genetic variation for plasticity in shaping L. digitata’s thermal plasticity. Trait performance at 5 or 15°C (reaction norm slopes) differed among genetic lines, even showing opposite response patterns. Interestingly, genetic variation for plasticity was only significant when sporophytes were reared at 5°C. Thus, we provide evidence that the cold-temperate to Arctic kelp species, L. digitata, which possesses a wide temperature tolerance between 0 and 23°C, is impaired by warm temperature during gametogenesis and recruitment, reducing growth of juvenile sporophytes and expression of variable thermal plasticity in the wild.

The impact of environmental acidification on the microstructure and mechanical integrity of marine invertebrate skeletons

Article

Full-text available

Nov 2019

Ocean acidification (OA), from seawater uptake of anthropogenic CO2, has a suite of negative effects on the ability of marine invertebrates to produce and maintain their skeletons. Increased organism pCO2 causes hypercapnia, an energetically costly physiological stress. OA alters seawater carbonate chemistry, limiting the carbonate available to form the calcium carbonate (CaCO3) minerals used to build skeletons. The reduced saturation state of CaCO3 also causes corrosion of CaCO3 structures. Global change is also accelerating coastal acidification driven by land-run off (e.g. acid soil leachates, tannic acid). Building and maintaining marine biomaterials in the face of changing climate will depend on the balance between calcification and dissolution. Overall, in response to environmental acidification, many calcifiers produce less biomineral and so have smaller body size. Studies of skeleton development in echinoderms and molluscs across life stages show the stunting effect of OA. For corals, linear extension may be maintained, but at the expense of less dense biomineral. Conventional metrics used to quantify growth and calcification need to be augmented by characterisation of the changes to biomineral structure and mechanical integrity caused by environmental acidification. Scanning electron microscopy and microcomputed tomography of corals, tube worms and sea urchins exposed to experimental (laboratory) and natural (vents, coastal run off) acidification show a less dense biomineral with greater porosity and a larger void space. For bivalves, CaCO3 crystal deposition is more chaotic in response to both ocean and coastal acidification. Biomechanics tests reveal that these changes result in weaker, more fragile skeletons, compromising their vital protective roles. Vulnerabilities differ among taxa and depend on acidification level. Climate warming has the potential to ameliorate some of the negative effects of acidification but may also make matters worse. The integrative morphology-ecomechanics approach is key to understanding how marine biominerals will perform in the face of changing climate.

Survived but not safe: Marine heatwave hinders metabolism in two gastropod survivors

Article

Aug 2020
MAR ENVIRON RES

Marine heatwaves (MHWs) are an emerging threat to marine organisms that have increased in frequency and magnitude in the past decade. These extreme heating events can have differential impacts on organisms with some experiencing mortality while others survive. Here, we experimentally exposed two species of subtidal gastropod (Trochus sacellum and Astralium haematragum) to two realistic intensities of MHW to test the ability of different species to physiologically cope with extreme heating events. Extreme MHW conditions caused 100% mortality in both species within five days. While both species survived under moderate MHW conditions they showed evidence of nonadaptive metabolic depression. Both species demonstrated an inability to upregulate their metabolic rates at the higher temperatures following exposure to a MHW (i.e. reduced temperature of maximum metabolic rate; TMMR), suggesting a lack of molecular protective responses and ongoing physiological damage. Therefore, the physiological damage endured by heatwave survivors may lessen their ability to cope with subsequent stress until fully recovered. Repairing this damage may have serious repercussions for the rate of recovery of these normally resilient species and their ability to maintain their ecological functions post MHW, especially under the predicted increasing frequency, duration and magnitude of MHWs.

Timing Metabolic Depression: Predicting Thermal Stress in Extreme Intertidal Environments

Article

Jun 2020

Anticipatory changes in organismal responses, triggered by reliable environmental cues for future conditions, are key to species' persistence in temporally variable environments. Such responses were tested by measuring the physiological performance of a tropical high-shore oyster in tandem with the temporal predictability of environmental temperature. Heart rate of the oyster increased with environmental temperatures until body temperature reached ∼37°C, when a substantial depression occurred (∼60%) before recovery between ∼42° and 47°C, after which cardiac function collapsed. The sequential increase, depression, and recovery in cardiac performance aligned with temporal patterns in rock surface temperatures, where the risk of reaching temperatures close to the oysters' lethal limit accelerates if the rock heats up beyond ∼37°C, coinciding closely with the body temperature at which the oysters initiate metabolic depression. The increase in body temperature over a critical threshold serves as an early-warning cue to initiate anticipatory shifts in physiology and energy conservation before severe thermal stress occurs on the shore. Cross-correlating the onset of physiological mechanisms and temporal structures in environmental temperatures, therefore, reveals the potential role of reliable real-time environmental cues for future conditions in driving the evolution of anticipatory responses.

Linking energy budget to physiological adaptation: How a calcifying gastropod adjusts or succumbs to ocean acidification and warming

Article

May 2020
SCI TOTAL ENVIRON

Accelerating CO2 emissions have driven physico-chemical changes in the world's oceans, such as ocean acidification and warming. How marine organisms adjust or succumb to such environmental changes may be determined by their ability to balance energy intake against expenditure (i.e. energy budget) as energy supports physiological functions, including those with adaptive value. Here, we examined whether energy budget is a driver of physiological adaptability of marine calcifiers to the near-future ocean acidification and warming; i.e. how physiological energetics (respiration rate, feeding rate, energy assimilation and energy budget) relates to adjustments in shell growth and shell properties of a calcifying gastropod (Austrocochlea concamerata). We found that ocean warming boosted the energy budget of gastropods due to increased feeding rate, resulting in faster shell growth and greater shell strength (i.e. more mechanically resilient). When combined with ocean acidification, however, the gastropods had a substantial decrease in energy budget due to reduced feeding rate and energy assimilation, leading to the reduction in shell growth and shell strength. By linking energy budget to the adjustability of shell building, we revealed that energy availability can be critical to determine the physiological adaptability of marine calcifiers to the changing oceanic climate.

Adaptive Responses of Marine Gastropods to Heatwaves

Article

Nov 2019

Under climate change, many species are increasingly exposed to heatwaves, including marine species. Although marine species are expected to succumb to heatwaves, there is increasing interest in understanding why some can persist. As heatwaves can greatly elevate intertidal seawater temperature, we explore reasons for variation in biological performance to acute thermal stress among three species of intertidal gastropods. When thermal refuges were unavailable for adaptive behavior, we show that their biological performance (feeding rate) was either maintained (resistant), recovered from a decline (resilient), or collapsed (sensitive), depending on the strength of molecular defense (where resistant species > resilient species > sensitive species). The integration of molecular, physiological, and behavioral responses within a species illustrates the kind of adaptive capacity that allows organisms to survive heatwaves and maintain their ecological functions. In this era of unprecedented environmental change, understanding how organisms persist seems as important as understanding how organisms perish.

Stress across life stages: Impacts, responses and consequences for marine organisms

Article

Oct 2019
SCI TOTAL ENVIRON

Population dynamics of marine organisms are strongly driven by their survival in early life stages. As life stages are tightly linked, environmental stress experienced by organisms in the early life stage can worsen their performance in the subsequent life stage (i.e. carry-over effect). However, stressful events can be ephemeral and hence organisms may be able to counter the harmful effects of transient stress. Here, we analysed the published data to examine the relative strength of carry-over effects on the juvenile growth of marine organisms, caused by different stressors (hypoxia, salinity, starvation, ocean acidification and stress-induced delayed metamorphosis) confronted in their larval stage. Based on 31 relevant published studies, we revealed that food limitation had the greatest negative carry-over effect on juvenile growth. In the laboratory, we tested the effects of short-term early starvation and hypoxia on the larval growth and development of a model organism, polychaete Hydroides elegans, and assessed whether the larvae can accommodate the early stress to maintain their performance as juveniles (settlement and juvenile growth). Results showed that early starvation for 3 days (∼50% of normal larval period) retarded larval growth and development, leading to subsequent reduced settlement rate and juvenile growth. When the starvation period decreased to 1 day, however, the larvae could recover from early starvation through compensatory growth and performed normal as juveniles (c.f. control). Early exposure to hypoxia for 3 days did not affect larval growth (body length) and juvenile growth (tube length), but caused malformation of larvae and reduced settlement rate. We conclude that the adverse effects of transient stress can be carried across life stages (e.g. larval to juvenile stage), but depend on the duration of stressful events relative to larval period. As carry-over effects are primarily driven by energy acquisition, how food availability varies over time and space is fundamental to the population dynamics of marine organisms.

Functional loss in herbivores drives runaway expansion of weedy algae in a near-future ocean

Article

Aug 2019
SCI TOTAL ENVIRON

The ability of a community to absorb environmental change without undergoing structural modification is a hallmark of ecological resistance. The recognition that species interactions can stabilize community processes has led to the idea that the effects of climate change may be less than what most considerations currently allow. We tested whether herbivory can compensate for the expansion of weedy algae triggered by CO2 enrichment and warming. Using a six-month mesocosm experiment, we show that increasing per capita herbivory by gastropods absorbs the boosted effects of CO2 enrichment on algal production in temperate systems of weak to moderate herbivory. However, under the combined effects of acidification and warming this compensatory effect was eroded by reducing the diversity, density and biomass of herbivores. This loss of functionality combined with boosted primary productivity drove a fourfold expansion of weedy algal species. Our results demonstrate capacity to buffer ecosystems against CO2 enrichment, but loss of this capacity through ocean warming either in isolation or combined with CO2, driving significant algal turf expansion. Identifying compensatory processes and the circumstances under which they prevail could potentially help manage the impacts of ocean warming and acidification, which are further amplified by local disturbances such as habitat loss and herbivore over-exploitation.

Resilience of a harvested gastropod, Turbo militaris, to marine heatwaves

Article

Aug 2019
MAR ENVIRON RES

Marine heatwaves (MHW) are predicted to occur with increased frequency, duration and intensity in a changing climate, with pervasive ecological and socioeconomic consequences. While there is a growing understanding of the ecological impacts of warming and marine heatwaves, much less is known about how they influence the underlying physiology and health of species, and the nutritional properties of tissue. We evaluated the effects of different heatwave scenarios and ocean warming on the nutritional properties and immune health of the harvested gastropod Turbo militaris. Neither heatwave scenarios nor elevated temperatures had significant impacts on morphometrics, proximate composition or inorganic content of T. militaris. However, an increased moisture content and non-significant trends, such as elevated amount of lipids, and an increased number of hemocytes in the blood of T. militaris in the heatwave treatments were suggestive of mild stress. Overall, our study suggests that T. militaris is resilient to marine heatwaves and warming, although delayed, additive or synergistic stress responses cannot be ruled out. Understanding the possible effects of ocean warming and heatwaves on fisheries species could improve management actions to avoid species impacts, socio-economic losses and negative effects to ecosystem service provision in a changing climate.

Long-term thermal acclimation drives adaptive physiological adjustments of a marine gastropod to reduce sensitivity to climate change

Abstract

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