Tropicalisation of Temperate Reefs: Implications for Ecosystem Functions and Management Actions

Roskilde University

Tropicalisation of temperate reefs Implications for ecosystem functions and management actions Vergés, Adriana; McCosker, Erin; MayerPinto, Mariana; Coleman, Melinda A.; Wernberg, Thomas; Ainsworth, Tracy; Steinberg, Peter D. Published in: Functional Ecology

DOI: 10.1111/1365-2435.13310

Publication date: 2019

Document Version Peer reviewed version

Citation for published version (APA): Vergés, A., McCosker, E., MayerPinto, M., Coleman, M. A., Wernberg, T., Ainsworth, T., & Steinberg, P. D. (2019). Tropicalisation of temperate reefs: Implications for ecosystem functions and management actions. Functional Ecology, 33(6), 1000-1013. https://doi.org/10.1111/1365-2435.13310

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Download date: 27. Sep. 2021 This article isprotected rights by All copyright. reserved. 10.1111/1365 doi: lead todifferences version between this andthe ofPleasec Version Record. been and throughtypesetting, proofreadingwhich may thecopyediting, process, pagination This article undergone has for and buthas accepted been not review publication fullpeer 2450, Australia 3 2 Earth andEnvironmental Sciences. UNSW Australia, Sydney NSW Australia 2052; 1 Wernberg Vergés actions T Williams Editor: Gareth Ecology Section: Ecosystems typeArticle : DR THOMAS WERNBERG (Orcid ID : 0000 DR MARIANA MAYER DR ADRIANA VERGES (Orcid ID : 0000

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This article isprotected rights by All copyright. reserved. ABSTRACT interactions, tropicalisation Keywords: * Singapore 7 6 Crawley, WA,Australia 5 2450, Australia 4 Corresponding author

Department Science of and Enviro Accepted ArticleSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technical University, UWA Oceans Institute and School Biological of Sciences, University of Western Australia, National Marine Science Centre, Southern Cross University, 2Bay Drive, Coffs Harbour, NSW 2. 1.

productivity ecosystem functions whetherin dominating the seafloor properties and Here, we c profound shift distributiontheir towards polesthe in response to warming. is This already causing Temperate reefs from around world the are becoming anopy seaweeds such kelpas are replaced by

637551, Singapore

Anthropocene, climate change, ecosystem function, herbivory, kelp, shifting species

argue that shifts dominantin foundation species and associated ecological communities as

seaweeds, turf or corals may functions : Adriana: Email:Vergés.

increase increase in

the the

for for some tropicalisation end

. We put forward three potential cascading of warming nment (DSE), Roskilde University, DK some consequences of tropicalisation for the ecosystem

tropicalised reefs become dominant

temperate reefs [email protected]

tropical species. - points. For example, local

as ahigher proportion primaryof depend largely onthe taxa that endup . tropicalis

We highlightWe potential gains tropi calisation

, warm as - 4000 Roskilde, Denmark trajectories, that differ - water species species water benthic to to fish certain

This article isprotected rights by All copyright. reserved. Acceptedeconomies, food These changes are leading to profound alterations in species composition acclimatisation 2017) Worldwide, species are INTRODUCTION Article 3. 4. , changes demographicin processes

steps considering the ethics surrounding interventionist. approaches W like corals or seaweeds assisted evolutio connectivity tropicalised reefs predicted species particularto locations. environmental management ecosystem configurations. This Regardless of which trajectory followed, is tropicalised systems represent largely risks as well as capture potential opportunities essential carbon export. production is directly consumed e highlight

to (Pörtner & Farrell 2008) successfully

supply to to structural and

form

to manage tropicalised reefs ,

the developmentthe of new fisheries that target range important We We argue that u

As technological innovations continue to emerge, h res and health and health n ulate new conservation strategies and . These include

and p onding develop novel management

migration strategies to facilitate dominancethe of large habitat formers .

ecological func

(Pecl to to climate change through geographic range shifts

approaches, which typically onmaintaining focus or returning tional changes make or the most potential of newopportunities We outline management practices that may mitigate either nderstanding these changes flows in of energy andmaterials is pose

, but this , but

and marine protected areas et al. (Selwood, McGeoch & Mac Nally 2015) and interventions s evolutionary adaptation

major challenges

2017) ethical , which

will .

b . challenges associated with developing novel

may to need among broader the community are essential at the expense of other functions approaches.

management approaches

to traditional conservation and to to increase resilience and

become increasingly

(Hoffmann & Sgrò 2011) - expanding invaders, and with aving goals clear and

impact , physiologica s on (Pecl that minimise

novel such assuch our

et al. .

in This article isprotected rights by All copyright. reserved. support over hundreds of kilometres coastlines,of with declines nowdocumented from eastern and 2016) warming, during as such overgrazing new interactions among previously separated taxa emerge, arrivals colonise warming temperate systems, and waters and with intensifying poleward flowing boundary currents water species recede re ecosystem services into the future. changes impact the benefits that humans derive from natural our systems require understanding a typically major challenges to traditional conservation and environmental management approaches 2011) moving from paleoecological studies biological assemblages novel species configurations massive turnover in the systematic biodiversityloss of revealed profound changes global in biodiversity, contrary but expectations to there wasnot a re re increasingly unable to -

Acceptedorganised Article . . Inmarine systems, biological assemblages sitting just outside tropical latitudes are becoming Species redistributions and the A recentanalysis of

These phenomena has greatlyhas accelerated in response to anthropogenic environmental change focus onmaintaining returning or species to particular locations transport

temperate foundation seaweed species or

“ tropicalised larvae from tropics the to temperate reefs (Vergés

the the mechanisms driving novel ecosystem configurations

ir constituentir in in response to marine heatwaves have led protect conserveor historical more than

”

(Hobbs (Blois et al. warm, as (Dornelas

to extensive losses seaweedof forests and the species they 2014a)

et al.et

et et al. species, resulting in global the emergence communities of w 35,000 plant, mammal, bird, fish, and invertebrate species resulting historical - affinity species become increasingly dominant

et al. 2013)

. These changes are linked gradualto warming coupled 2006) , alsocan result

emergence of novel 2014) , changes in the abiotic . but but in

C result in hanges species in distributions and altered (Vergés . Instead, communities are undergoing a

(Wu recent decades

conditions,

for examplefor

sign

in mass die et al.et et al.et

(Vergés i ficant change in the system when

2012) 2014b; Vergés biological assemblages new management approaches the the rate at which species are environment -

, which warm et al.et offs offs kelpof tropical , sothat we secure can

(Hobbs

2014a)

and

herbivor

et al.

et al.et

how these (Wernberg are well known (Chen . Th temperate

2016)

and cool 2017) ese new , which e s

et al. pose . . As we Rapid

et al.et

ith ith

This article isprotected rights by All copyright. reserved. consequence, nutrient cycling and Habitat TRAJECTORIES FORWARMING TROPICALISED REEFS engine of temperate reefs al. potential refugia for corals tropicalas temperatures rise beyond their physiological limits species are shifting across biogeographicmajor boundaries here relating benthic to biomass, energy and flow nutrient cycling dominance of environment. humans derive from temperate reefs ecosystem functions should novelof tropicalised systems 2014) like corals temperate species, production 2014a) Wernberg western Australia to Japan, Korea and the Mediterranean

Accepted Article 2014)

we focus on . Here, wediscuss the Although tropicalisation is a global , the o Thus key a question understandingfor andmanaging systems these is entirely newecosystem be functions expected - forming organisms foundation or species mediate important ecosystem functions

and the contracting edge economically of important kelp forests that are the biogenic

et al. , nutrient cycling (Tuckett verall consequences of these changes for ecosystem functions

Although changes in the identity and relative abundance habitatof cold to warm

2016; Kumagai tropicalised

ropicalisation et a et provision of (sensu Be l. recent studies show that

2017) (Bennett - potential

affinity or fishor in timein become shallow llwood

and the development of novel et al.et refuge, nursery, foraging andbreeding areas also

eries et al.

, and its kelp) consequences of tropicalisation for the

2018) reefs et al. entails the range expansion of

pr 2016)

is is already impacting important ecosystem functions and increasingly visible oduction

in midin . In press) consequences

similar to .

range - latitudes (23

are are poorly understood

? that underpin goodsthe and services that

shifts shifts in

tropical habitats (Denis for managementthe of marineour . These regions (Pessarrodona, Foggo & Smale 2018) coral reef

temperate species (e.g. from -

35 e t al.t phenomenon °N S) or

tropical

- 2013; Vergés formers in tropicalised , such as ecosystems .

also As well theas loss of or services . properties and : In regions, these habitat Will for species. represent both a

(Vergés coral reefs

the

- et al. (Graham forming

functioning like primary

et al.et

(Beger including

2014b; As a , or

species

et al. et

et et

This article isprotected rights by All copyright. reserved. interactions; functional redundancy between habitat forming lost species andgained on The Changes to PREDICTED IMPACTS TO Vergés have replaced seaweeds as the dominant primary producers temperate corals and/ or range ( biomass turf structural complexity and simplified food webs (b) adapt to their new environment andpersist into the future. Terazono (Fig. 2b) (a) trajectories regions, however, differ in wh forests al.et 2016; syst temperate reefs c ) Turf) and coral dominated reefs

Acceptedseveral factors: Article S Turf dominated reefs ems extent of eaweed Globally, tropicalised

as as the domina et et al. , with significant, with knock

replace temperate canopy

et al. identified Wernberg al., et 2016) biodiversity

ing -

and change 2016; Wernberg

dominated reefs biodiversity

2012) can cause algae how fast temperate species contract and tropical ones expand nt habitatnt

for warming temperate reefs (Fig. 2c; Vergés or, hypothetically

in dramatic change

changes to (e.g. eastern Mediterranean) beta beta shallow

et al. et ich -

expanding tropical corals coexist (e.g. Japan) formers - BIODIVERSITY on effects on effects for diversity

taxa taxa end up dominating seafloor, the with three potential . -

formers, as in formers, in as some southern Japan reefs 2016; Tuckett reefs share two

(e.g. Australia Japan, temperate reef

et et al. , , such asystemmay develop if and increases in tropical/ subtropical species. Different . s To date,To –

in thein physical structure and functioning 2014b; Filbee

these systemsmay emerge if associated , canopyas seaweeds become replaced by low

, et al. globally ECOSYSTEM range shift

systems key

– 2017)

phenomena: aloss of temperate seaweed

biodiversit these systems are characterised by low

- , Korea

Dexter &Dexter Wernberg 2018) (Fig (Yamano, Sugihara & Nomura 2011; undergoing .

observations suggest that tropical

. with turf algae

1 ) ):

– FUNCTIONS y

in in these systems warm ( Terazono et al. 2012; Vergés ; changes; in species some

tropicalisation tropical seaweed species

(Tanaka temperate seaweeds

(Fig. 2d) ;

the degree of

& SERVICES&

of theseof

et al. et

will depend , which

2012; - -

This article isprotected rights by All copyright. reserved. shift from kelp to species support significantly different associated communities change provide Loss of species caused by the overall abundance and O directly as or detritus region in the immediate future 2100 could of56% to (including Tasmania), but Australiain ranges where poleward retreat possible.is (Taylor & Cole 1994) short term (e.g. within 50 temporary. implies the inflated biodiversity could bebased on an extinction debt and therefore potentially new individuals contractions al. increase in the total number species of present in tropicalised reefs species bservational and experimental studies have shown substantial declines αdiversityin th wards Antarctica. The GSR

Accepted Article 2016) Seaweed forests support a broad range of organisms through provision habitatof or food, either Tropicalisation

(Martínez disappear . For example, are invertebrates similar . This could bedue differences to in

expanding their ranges (Bennett (Bates

microhabitats et al.et given whereas Sargassum

is unlikelyis to et al.

are found nowhere else globally et al.et 2018) (Krumhansl & Scheibling 2012; Teagle

co and partly because most te currently number -

occurring contractions

2014b) years) ends at 39

2016) , posing acritical threat and substaintal management challenge for

(Tanaka (Coleman & Wernberg 2017) replacement kelp of forests by other seaweeds may beoffset if the ha .

of , partly because many temperate species are habitat generalists predicted s ;

, which be the cause speciesof extinctions extensions only species whe high levelsof endemism

faster than tem cool o

S and requir et al. - water laminarianwater kelps and more warm runs across the entire southern edge of poleward Exceptions to this include

2012; Wernberg e has few stepping stones or connections further

mechanisms underpinning the deaththe n

seaweed forests disappear mperate coastlines extend across broad latitudinal perate ones requir shifts in seaweed forests (Bennett

and disappearance of all individuals e

the the dispersal and establishment a of few ; for example, for ; , though species identity like is

et al.et

are retracting et al.

(Coleman & Wernberg 2017) et al.

2016)

( 2017; Fulton

Vergés

at at a global scale 2016) the the

range extensions Great Southern Reef will likely reflect these up to 77% (Graham Ling 2004; 2008) . Many these of species , leading a to

et al. beyond - the continent

tolerant tolerant

et al.et 2016; Wernberg

of of

the the at least

2019) seaweeds, and n overall r continent Sargassum ough loss of and ly to south .

. This This in thein and a

(GSR) this se

. This article isprotected rights by All copyright. reserved. Accepted Diaz enhancing the competitive strength of press) coral skeletal density increasesto in current reef accretion biodiversity outside abiotic conditions biodiversity Articlecoral cover are not being recorded in for latitudinal expansion of corals howeveris species fauna new ecological niches become available in temperate latitudes, and i The range expansion structuralof (Serrano, Coma & 2012) Ribes & Nomura 2011; Kumagai alternative (Fig. 1 changes. In contrast, where seaweedthe forest replacedis by tightly packed low Changes

‐ - dominated dominated reefs of the future , are already Climate change is also making ocean the more acidic Pulido c which may limit ) ) biodiversity is likely decline to the the tropics habitat . In particular, associated with corals

in biodiversityin et al.et (Barkley

and expanding - such as light formers

(Hooidonk 2011) limit reef construction - driven upwelling; Schaeffer, Roughan & Wood2014)

et al.et associated biodiversity

and kelp of particularin , a

et al.et cidification a process already occurring along the coasts of can

their 2015)

et al. et

(Sommer and Australia

also also be strongly influenced by range the expansion of coral 2018)

ly range are are , and this may

may not

2014) complex corals is likely result to in increases in biodiversity as all turf and also , Korea

tends to

along with coral organisms tropical (Vergés

et al.et , and this may range impact expanding corals and associated (Manzello likely be to highly region

form accreting (Baird, Somm

seaweeds generally (Denis . 2018)

- i O

temperate transition zones. This ncrease

et al. be further accentuated by cean (Linares . -

specific et al.

et al.

2014b) acidification

coral reef bioerosion, preventing effective

et et al. reef , especially in higher latitudes sitting just 2014) 2014) er & Madin 2012; &er Madin Tuckett . (Madin

frame

2015) . , the western Mediterranean This suggestsThis that (Connell & Russell 2010; (Yamano n some instances may limit also coral - specifi

works et al. .

Japan

higher nutrients 2016)

c and (Perry & Alvarez , which can impair coral

et al.et -

lying turfspecies (Yamano, Sugihara suggest , dependent

and 2012) high latitude

the

et al. increases in s s

. associated by

The scope changes in

(e.g. due as 2017)

on - Filip InFilip .

This article isprotected rights by All copyright. reserved. Accepteddistribution of these habitats relative to tropicalised temperate reefs, as well as the presence of coralto reefs as adults assuch seagrasses, mangroves and Further, on many tropical coral reefs, juveniles of reef fishes rely establish (Yamasaki temperate temperate seaweed forests by offering have beneficial effects for some species,facilitat Wernberg 2018) & Speight 2005) substrate. Articlemay onavailability depend of selectivity for specific populations by nursery habitats such as kelp forests, can positively impact recruitment and success of fish groups that rely onspecific refuges which may mortality to lead some of species compos shelter A core function of habitat Provision habitatof on ition (e.g.ition by shifting fromkelp to turf On Tropical Juvenile fishes, for instance, ar will have pronounced a effect on fish recruitment

reefs for a variety of species

et al.et new tropicalised temperate reefs, the time (Carr 1991)

. The replacement of refuge spaces and camouflage

, which in turn are more complex than turf 2014) coral reefs are generally considered more comple

such as

and microhabitats as nursery . (Nagelkerken

. Fish recruits and juveniles are often habitat nursery function - abalone forming species is the creation of will will have negative consequences for habitat settlement cues

flora and

(Serisawa tropical seaweed (Rogers

et al. et seaweed e particularly vulnerable predation, to and the shelter provided

fauna

2002; Wilson s

et al. and implications for fisheries

et al.et (O'Brien

algae forests animalwith ‘forests’ on tropicalised reefs

(Wilson Where tropicalisation causes shifts benthic in grounds ing

needed needed 2018)

2004)

survivorship through protection from predators as as dominantthe taxa), refuges will bemodified, forests as nurseries prior to ontogenetic migration (Dixson, Abrego & Hay 2014)

et al.et

(Tolimieri 1995) , lobster et al.et

for

- (Coker, Wilson & Prat

dominated dominated reefs

2018) physically complex slow growing such species as

2010)

2010; Fulton many economically important

(Johnson substantially

x than seaweed forests or even declines whole of trophic .

- Importantly, specialists , while

et al.et

et al. (Filbee on non

and may have strong 2011) living and space settlement

2019) h chett 2014) owever - Dexter &Dexter

or or settlement - , reef habitatsreef . and fish Hence, the (Gratwicke , coral losses of success .

to may

This article isprotected rights by All copyright. reserved. Accepted(Wernberg (Fig. 1a), primary productivity species of like kelp is patterns of energy andorganic carbon flow differ markedly between Although benthic productivity is systems Food webs and energy fluxes in temperate vs. tropical reefs and implications for tropicalised boulders may offer also abiotic refuge spaces positive (Beck nurseries for some species simple structure and habitat functions 2014) Articlefish populationreplenishment ontropicalised reefs potential mismatches intiming betweencover seaweedrecruitment couldaffect and events high cover/biomass Many temperate not only o tropicalised reefs. (Berkström connectivity corridors facilitateto ontogenetic movements vegetation vegetation

. In to contrast corals, kelps and other The ofkelps consequences potential substitution of by depen seaweeds tropical will et al.et habitats

feedback loop that facilitates tropicalisation of temperate reefs

et al.et

et al. et 2017)

the ,

, whereas tropical including turf

2019) morphology ‘new’ ofthese habitat cover 2013) .

laminarian kelplaminarian This This suggests that , ,

and only asmall proportion of this productivity (< (Fulton may belimiting factors in the su

(Galaiduk

algae dominated habitats (Filbee

et al. extremely seaweeds species arespecies perennial

et al.et the the replacement of kelp forests by -

Dexter &Dexter Wernberg 2018) 2014)

2013) habitat forming high both in temperate and tropical reefs, the overall . .

such such Seasonal declines ascover inseaweed well ,

including as t ypically very high also but very - Sargassum , formers (Terazono

can ccess of many tropical reef fishes on

that seaweeds with persistentlylevels of high

many range shifting tropical species be

promote survivorship of juvenile fish function , but also on , but . Nevertheless, some str

et al. spp. these , turf algae provide minimal , especially areas in where ally important tur

have

2012; Yamasaki2012; 20%) is consumed by systems. In f

algae

their p shorter shorter may a create henology

seasonal temperate reefs as periods of periods of ucturally juvenile

et al.

- fish

This article isprotected rights by All copyright. reserved. redistribution and recycling invertebrate biomass species and beenhas dynamics. move’ 2018) increases primaryin production are M metabolic reefs turf algae anddetritus are major contributors to fish biomass in coral reefs only asmall proportion of total fish biomass in shallow temperate reefs reefs (Wilson 50 ‘turfs’ and associated microbes susta sequestered in sandy beaches and the deep sea production in habitats with no or low primary production, including reefs with no canopy seaweeds, (Filbee 2012) herbivores, with over 80% ending upas detritus/ dissolved organic matter esocosm experiment Accepted Article- 100% of turf of 100% primary production

turf . in herbivoryin anddetritivory reflected are foodin

. . A meta

that that These Kelp detritus - can can - Dexter

Importantly oneof the most knowWe little about how energy and flow websfood situationThis is reversed in feeding invertivores detritivores and et al. the increased abundance and functional diversity herbivorous of fishes rates well as as

characterise tropicalisation play a significant role in the remineralisation of turf algae, small

mesocosm studies analysis ofanalysis 2003; Clements

adjacent et et al.

can becan exported across distances ranging frommeters hundredsto kilometresof

2018) and may be also s ‘ suggest carbon sink more than primary production .

This patterns

et al.

, however, (Filbee that this can lead to ecosystem collapse and simplified websfood if

constitute

converted to

600 2017) tropical coral consistent observation (Carpenter 1986; Hay 1991) in in (Shantz habitats increasing bioavailability the

and - highly Dexter experiments showed .

s typically which can These striking differences

an important trophic subsidy sustaining high secondary ’ et al.et

(Bennett

such such seagrassas meadows and productive habitats

et et al. unpalatable -

consumption dominated reefs (Fig. 1 2015) do incorporatenot the effects ‘speciesof onthe

2018) have important effects on altered food web

web studies, which show that seaweeds support et al.et . The increased availability easily of . s

Alternatively, kelp detritus may 2015) on detritus that ocean warming

are changing tropicalised (Nagelkerken & Connell 2015) , . Here, including . Recent studies suggest t of nutrientsof

and between tropical and temperate (Truong

h (Hill not consumed d erbivor (Krumhansl & Scheibling (McMahon ), where),

temperate reefs in warmingin temperate microbes and detritus - particulate POMparticulate

et al. and impacting

(Vergés et al.et ous fish typically

low biomass 2015)

2017) et al.

(Ullah

et al. consume .

hese increases

globally , while 2016) become

and

2014a) local . et al. .

, This article isprotected rights by All copyright. reserved. (Moreno & Amelung 2009; Marshall losers in marinethe tourism industry temperate reefs coastal tourist destinations photography, being. Nature Bennett2009; T Consequences for tourism activities mostly 1 2015; Krause sequestered in sediments al.et role of in kelp detritus t higher trophic levels, consumed and recycled locally may start the accessible nutrients could fuel additional growth of turf algae and provide a feedback strengthen to he strength d ourism is ) Accepted Articletropicalised dominance of turf would reduce

2017) temperate change detritus Changes in patternthe of energy andmaterial flow

to to resemble coral a ,

of .

recent studies suggest that kelp major component of the economymany of areas coastal - -

is highly dependent onhealthy marine environments and

Jensen based marinebased tourism, et al.et temperate cross may kelp forests as effective long this source blue of

2016) redistribut

habitat et al.

potentially leading increases to inbiomass the (Filbee supply pathways

reefs and

and - 2018) (Biggs dominated system trophic subsidies

- contribut Dexter &Dexter Wernberg 2018) will

benefits society e (Fig. 1c,1d)

tourism flows .

The replacement of low latitude kelps by et al. et also impact the potential for

carbon e.g.

et al.et depending onthe e

. 2015; Bennett meanginfully

scuba diving,scuba snorkelling, eco

2011)

. This , whereas a that

and s - , with term sinks carbon still is more broadly (Weatherdon reach . , in turn,

impacting habitats that are Such c

a higher proportion of primary being production

es to the to et al.et

replacement with tropical seaweeds type and location of tourism activities

. adjacent hanges will require an adaptive response

This suggestsThis that

may in result increased of flow energy to s

2016) brought about by s world’s et al.et through its

carbon depositional areas

. He 2016)

of benthic species ‘blue carbon’ budget

(Kragt, Roebeling & Ruijs nce,

a major sequestration -

filming and underwater under investigation

contribution human to well and create winners both and t corals or ropicalisation of some currently

hifts habitat in source tropicalised reefs can . turf

Although , but reduc of of revenue at subsidised by

(Fig. 1 (Hill would (Howard - formers

et et al. t c he ing

and

This article isprotected rights by All copyright. reserved. Acceptedand reef complexity influencedis by attributes such as healthy habitats, abundance of living marine life, diversity of fish these marine fauna, such as shark diving andwhale watching. pattern higher of trophic groups, with impacts on tourism activities that are based on encounters with recreational fishers. Cascading effects induced by tropicalisation may species of temperate fishes and organisms as such abalone and lobster, may beenhanced for (Nelson warmerwhile conditions may tropicalisation may new opportunities create for recreational fishing value of these reefs that is highly valued by reef tropical reefs, such as high a diversity of corals and reef fishes, lost from these ecosystems. Article2013) (Beaumont and sport fishing highly are profitable sources of income tourist enterprises for revenue for the region and eco AUD$10 billion/year temperate coastlines around world.the In Australia, opportunities from marine tourismmarkets to adjust existing tourism modes andtake advantage emerging of .

B -

A Warmer waters and shifts in temperate reef ecosystems towards communities Kelp forest ecosystems support arange marine of tourism activities along temperate zone filming southern the in Benguela generates an estimated USD$22.4 mi et oth economicthe and ecological value of temperate reefs ttraction ttraction to reef viewing activities Great Southern Reef major a is contributor coastalto economies al.

et al.

(Graham 2013)

2007)

. (Nakamura (Biggs

Conversely, the

(Bennett

(Blamey & 2018) Bolton , with diving activity levels correlated with kelp persistence et al.et

et al.et -

viewers 2014; 2014; Weatherdon enhance

et al.

et al. et

2015)

2016)

(Williams & Polunin 2000) 2013) significance

fitness and thus . While coral tourism, recreational and commer . . Ecotou by tourists For example, species range shifts associated with

. Similarly, recreational scuba diving in et et al.

of rism such activities as recreational scuba diving - catching

dominated tropicalised temperate reefs 2016)

yields of has has strong li .

increasingly rare and highly prized

may , potentially increasing the tourism some may nks ecosystem to condition, which

deliver deliver tourism also alteralso the distribution native temperate species

be impacted

with an estimated value of cial cial fisheries an

(Champion

underwater scenery llion in temperate reefs (Menzel

/year if kelpif forests are more similar to kelp

et al. et

from in tourismin

et al. (Fig forests

2018) the the

1 d , )

This article isprotected rights by All copyright. reserved. higher latitude reefs, MPAs appear to limit the spread of range herbivorous fish that maintain (Babcock ef greater abundance and size higherof order predators functions ecosystems, t reserves within or entire marine parks ( M M approaches. ecosystems, briefly and discuss some the of ethical considerations underlying choices management of traditional (MPAs) and emerging particular locations and environmental management major challenges trajectories are followed, these systems will represent 2015) many Even APPROACHES TO MANAGING reefs revenue associatedlosses with declines healthyin natural temperate reefs, shift a to turf may enhance attractivenessthe of temperate reefs to tourists, thereby compensating any for tourism fects Acceptedarine protected areas ( arine Article

(Fig with rapidwith . decades

F can P undamental to our understanding of tropicalised temperate systems that is regardless whichof

. rotected (Babcock et al.et

1 cascade through webs food

) his protects not only kelp the themselves, can but , is is

and continued impacts on coastal ecosystems are expected globally 2010) reductions in , practically likely to reduce tourism and its be A

(Hobbs et al. reas .

Whether MPAs

to to increase resilience and connectivity 2010)

et al.et , legally

carbon dioxide emissions, tropicalisaed reefs in kelp )

. Cessation of extractive activities within MPAs generally , which typically focus onmaintaining or returning species to increases in predators generally

2017; McDonald (‘ assisted evolution

TROPICALISED REEFS and philosophically, by limiting urchin e . g

limit or . , networks of reserves spanning 100sof km). ban extractive activities either within individual

nefits et al.

(Lester ‘) novel can also limit grazing by range approach

2019) the world’s oceans will continue warmto for

free statesfree grazing andfacilitat to traditionalto

ecosystem configurations et al. - . also extending species and buffer climate Below we consider more both

es es conservationto these of

2009; Edgar

lead to restoration of trophic is , however, approaches to ing

et al.et

largely unknown. kelp recolonisation (Gattuso

2014) - . This expanding conservation - dominated dominated For kelp results in . These

pose et et al. s

- This article isprotected rights by All copyright. reserved. ( consideration, climatic impacts within MPAs will continue dramaticallyto change marine ecosystems project protection prolongto persistence in landscapes degradationof and tropicalisation. Nonetheless, oceanographic conditions allo that be benefit identifin systems functions and that we value anticipate future change and manage beyond extantconditions to Wernberg recolonisation kelp of into areas where it has been lost often are unfavourable (Wernberg assuch term, andeven when stressors are temporary (e.g. marine heatwaves) persistence of tropical biota Such assumptions are recolonization and (iii) dispersal mechanisms are favourable for kelp dispersal into denuded areas. reefs relies on latitudes (Palumbi 2003; Coleman fragmentation and degradation and to act as a source for recolonisation in latitude systems remains to be established. related biological variability AcceptedBruno Article MPAs may play , (ii) the initial stressor is ions of climate impacts within MPAs

et al.et herbivore A goal many of MPAs globally is maintain to connectivity landscapes in of habitat loss,

via facilitation of connectivity andrecolonization kelpof three

et al. et al.et

2018

assumptions

2018)

2016). s ).

will be an enduring indirect climate stressor that limit ying

. rarelymet. greater greater role mediatingin tropicalisation if scientists andmanagers begin to

Moreover, potential thermal refugia

et al. :

(i) healthy kelp forests persist in MPAs (Bates

not permanent and

2011) D w kelp to thrive oceanographic conditions that are required for dispersal and

irect climateirect stressors such as warming often are gradual and long et al. (Coleman .

However, the strategy of

2014a; Bates

across the globe

et al.et

conditions (Ban (Lourenço

2017; Bruno

et al.et et al.et

will 2017)

2016)

suggest that even with such et al.

reversing tropic

become

‘ et al.

future , but whether this applies to lower may bechallenging

. Similarly, 2016) with

2018) - s in a in landscape of degrad

proof

favourable for could be non kelp recoloniz . For example, there may -

(Coleman ’ protected areasprotected areas with

alisation the ecological

prioritise . Th

ation at low et al.et e approach d

for 2017; ed

This article isprotected rights by All copyright. reserved. considered depends on increased fishing will have effort by despite intense exploitation rates remains hypothetical, rabbitfish could effectively control the population and decrease grazing pressure on kelp forests Australia component of fisheries catches (Madin 2016) fishery opportunities and Although s acrossshift local, national, and international boundaries important adaptation strategy climate to change, albeit onewith intrinsic major challenges as species implemented worldwide and be can effective minimising at impacts fishery considered for other invasives like the Atlantic blue crab, which has marine aquaria trade, turning athreat into aprofit already with used examplefor A potential management approach to limit tropicalisation may target beto range C

Accepted Article apturing new opportunities asa management action , the socio

(Mancinelli et al.et In EasternMediterranean, the range The (Gilby, Tibbetts & Stevens 2017; Lenanton . hifts thein distribution of commercially important fish stocks has already to led

by developing a development of new fisheries as species shift their distributions is emerging an as

2012) - economic consequences of range many

. et al.

given that invasive

2017) positive economic impacts new fishery . (El

T ra (Robinson species. For example, argeted removals of the invasive lionfish are - bbitfi Haweet 2001; Bariche 2005) s

h have fast life histories and or cullingor programs

et al. expanding rabbifishes have become important an - catch implicationscatch

- 2018) (Calado 2012) shifting species ar in some high latitude regions

et al.et i .

nvasive alien crabs (Gaines

Further, any management action that

2017)

for specific for species

, and similar strategies are being et al.et and are increasingly being . However, whether targeting

that will also need to be (Frazer substantial potential e still largely under can can sustain high fishery yields

2018; Pinsky

are are being et al.

also - expanding invaders, .

2012) This approachThis is (Jansen

being et al. et

used in in used the . -

explored

as new a

2018)

et et al. new targeted .

in in This article isprotected rights by All copyright. reserved. tolerance kelpsin many seaweeds and our limited understanding of yet u to ranges communities is largely unexplored. This could potentially bedone at the low latitude ecosystem services preferableis to other new higher latitude habitats change (e.g. more thermally or tolerant), (3) accelerate movement the or moving polewards seaweeds ( thesein systems: (1) enhance the persistence and resilience of the resident, dominant temperate systems dominated by turf alone 1 individuals have both been contemplated. individuals (assisted migration) or using CRISPR/Cas9 o range from selective breeding more of resilient individuals to the creation of genotypes are introduced and propagated through the target population. For the former, possibilities change and (b) assisted (enhanced) gene flow genetic adaptation (resilience) of a species to current or future environmental stressors such climateas Monaco 2009; van Oppen Assisted evolution is the acceleration of evolutionary processes to enhance certain traits Assisted evolution and migration ) rganisms Accepted, Article we , argue thatsystems with large

ndergo change. Both have significant challenges which are already experiencing tropicalisation, in or more central, “core” populations that are Trying to Of the

e.g. via direct genetic manipulations (

kelp), (2) enhance other canopy forming seaweeds, either those which themselves are three broad possible community configurations for tropicalised temperate

(Wernberg

slow downslow or halt (tropical range expanders) - ge n o m

et al. , for , for example if decidedit is that e editing e editing

et al. et

2015)

(Fig. 1c)

‘ 2018) seeding habitat

(Cleves tropicalisation by gene .

Conceptually, the idea includes o potential . Moreover, kelp historieslife . This implies threepossible strategies for assisted evolution

’ -

formers van Oppen challenged populations with propagules from enhanced

, or , or temperate residents which may bemore resilient to et al. ( Aitken & Whitlock 2013) the genesthe and heritability underlying thermal system configurations.

2018)

corals or seacorals

et al.et

linked to the complex biphasic life history of . For the later, transplanting adapted tically enhancing the resilience kelp of

coral functioning or provision of

2015

) weeds ,

which has recently piloted been often

ne or both (a) of enhancing

adaptation corals of theirto

by which superior genes or

are more desirableare than

genetically modified result in margins limited (Jones & reefs

of of their (Fig. This article isprotected rights by All copyright. reserved. capabilities also have maximumof growth seaweed susceptible to herbivores, they nevertheless can form extensive forests somein habitats during periods physical conditions of similar functional roles expanding tropical canopy forming algae (primarily assisted adaptation. A more realistic scenario may consider beto assisting colonisation of range herbivory kelps than fucoids) are also of temperate affinity, andmay actually beeven more susceptible warmingto and adaptation. However, most canopy algae that co similar also be the case th enhancing resilience warmingas poleward. advances However, this strategy relies on the assumption thermally tolerant genotypes from low latitude populations to central populations, potentially enhancing their resistance 2014a; Vergés as affected by both within the target population dis at low latitude kelps are better adapted and have been selected for thermal tolerance, which may not increased Sargassum Accepted Article persal come the at cost otherof important traits, such as

functional Laminarian kelp For kelp,

(Durrant simple historieslife and (Wernberg (Deysher & Norton 1981) herbivory due theto poleward movement tropical of herbivorous fishes

are generally morpholog

et al. the direct physiological effects

an alternative

roles et al. (Loffler & Hoey 2018)

2016) (Smale & Wernberg 2013; Martínez

et al.et

to those of (Steneck & Johnson 2013) 2014) often occur to . Thus enhancing kelp forests in the face of tropicalisation may require

– 2018; Donelson2018; biotic effects such herbivoryas

is is likely to be slow for most kelps. . Thus the second stage assistedof evolution (Doropoulos

option may “future beto

some species that float once dislodged have kelp canopies in

mixed with other temperate canopy forming seaweeds . Hence, assisted gene or flow dispersal maybe sufficient to ically plastic

. et et al.

Although

et al.

- as well as the

occur occur with 2013; Fulton

2019) and may alternative present targets for assisted

tropicalised and Sargassum tro growth

resilient to awide range of abiotic and - . pical proof” core populations by moving

P et al.et otential increase

kelp at lower latitudes (particularly

(McAfee, O’Connor & Bishop 2017) indirect effects of ocean warming, such Sargassum et al.

parallel to 2018) spp.) that could maintain systems It

is is

2019) , presenting poorer targets for also

(Fulton

. species generallyare temperature clear that the loss of kelp – Fucoids like s in

gene and flow uptake good dispersal

thermal tolerance may

et al. (Vergés

. 2019)

Sargassum relatively that . Species

et al.

play

is is This article isprotected rights by All copyright. reserved. Acceptedsystems implement interventions literature generally, including development the of logical structures for where/when/how to mitigate and view ethically appropriate to consider 2017) historical state low,is the underlying logic for managi coastl variability and represent novel ecosystems mostnot systems in terrestrial and marine environments have moved beyond historical limits of restoringor systems some to presumed The traditional focus conservationof Ethical considerations Article symbionts (van Oppen however, there are still major knowledge gaps including heritability the traits of in corals and/or migration more of thermally tolerant corals may bebeneficial coralto persistence higher at still besusceptible to bleaching during warm thermal events reefs adaptation/movement corals of into cooler waters. tropicalisation, rather than assisted evolution per se. promote colonisation of canopies of tropical

areas appear tolerant to coolerwaters including spells cold ines, and i . What, then, are our ethical obligations regarding management the these of new ecosystems Given thathumans have played major a role in creating these novel ecosystems, it is our in The third option maintainingfor more desirable ecosystem than states turf is accelerateto (van Oppen manage tropicalising marine ecosystems. view This gaiis f

we accept that

et al.

–

2017; Filbee ‘ decision trees 2015). these systems

and management marine of ecosystems active - ‘ Dexter &Dexter Smajdor 2019) natural ’

(Barnosky (sensu Hobbs(sensu Sargassum ecological

are are novel, and the potential for restoring them a to ’

or historicalor state. However, we argue thatmany if

Naturally recruited c

et al. et ng systems these changes

interventions spp. in spp. in areas underg

et et al.

2017) (Hughes

2006) (Tuckett & Wernberg 2018) . Such studies indicate that the ethics

–

for terrestrial as well as .

when considering how to et al. This includesThis tropicalising ning traction in scientificthe orals inhabiti

2017) oing climate has beenhas onmaintaining (Barnosky .

Assisting the ng high latitude - mediated

et al. et

latitudes marine ,

but but can

, This article isprotected rights by All copyright. reserved. Accepted andbeds cor systems aimed rehabilitating at adegraded system, even if it is tonot ahistorical state. For tropicalised ethical and community anxiety. desirability or ethics of the based approaches, happeningis well advancein of community understanding or acceptance of the example, the adoption of new approaches by specialists and community acceptance of these innovations. approaches approaches, be critical for scientists and managers focus on to the community’s acceptance of more interventionist context of the general community,managers politicians and Schwartz 2007) Articleintervention are likely to differ both among scientists and practitioners equally achieved by any given intervention ecosystem structure and function are reasonable targets, but these three goals are also unlik ecosystems returning ecosystems to 2017) interventionof and outsideis of historical limits and/or unlikelyis return to a to historical state in t moreof interventionist approach .

considerations

Tropicalising marine coastlines are particularly a interesting Who then decides Another important consideration is howto settle on desired management goals. choices may to need bemade between two highly valuable andvalued ecosystems . . This needsThis beto done a in timely fashion, given the and work towards building Maximising biodiversity, maximising ecosystem or services mimicking historical al reefs. science and technology development of , and these differences are likely be to even greater once one includes the broader associated That is,That doweuse the techniques described above tryto and enhance the . In most instances where historical states, we must have some other target criteria for managing

what se

technologies risks unknown of consequences

thes es

depend on factors e

targets the (Baltimore

social license ( Barnosky

should be ecological interventions are considered, they are

stem

such as the

et al. et al.et ? Attitudes to the desirability andethics of necessary cell therapiescell or more recently, CRISPER

2015) 2017) (Filbee

( Barnosky time

degree of confidence that the system , .

contributing to disruption uptakein

- for imple Dexter &Dexter Smajdor 2019) and challenging - lag between experimental (McLachlan, Hellmann &

et al. et m

he future e 2017 n tation ; case van Oppen

of of these If ,

and we are not for ely be to – As an

. kelp the the type these

It will

et al.et

This article isprotected rights by All copyright. reserved. Accepted develop novel management approaches. surrounding interventionist approaches technological innovations continue emerge,to h management approaches flowsin of energy andm productivity), but at the expense of other functions (e.g. carbon export) tropicalisation end that potential trajectories of tropicalisation theto warming andtropicalised drivers instead of long 2018) Article strongis Temperate reefs and their diverse ecological communities have long supported human there and use, CONCLUSIONS that arise from tropicalisation are novel, like the ecosystems themselves. managers have yet confronted spread declinethe of corals in the core parts of their distributions encroachment of tropical communities including corals into persistence of kelp forests at their warm edges, dowe do nothing end up dominating the seafloor

. functioning of these systems, devise to and adequate responses.

Like coral reefs, temperate ree of corals into former kelp systems economic and cultural reliance on these coastlines

- points may gains in result someto ecosystem functions (e.g. local fish - term naturalterm biophysical gradients aterials is aterials is essential that minimise risks well as as capture potential opportunities. temperate reefs depends onour capacity to accurately understand changes , and thus in

(seaweeds, turf or cor fs arefs however becoming increasingly shaped by human for warming temperate reefs worldwide among broader the community also essential are steps to

? These are questions thatwe believe few scientists or

many ways, management the andethical considerations to formulate new conservation strategies and aving cleargoals als (Williams –

(Bennett at least some even try andenhance polewardsthe ; Fig.; 1

, anticipating the and )

. We speculate thatsome et al.et et al.

consider Here wehave presented three . Understanding these changes

system

2019) 2016; Blamey & Bolton ing the ethics

that differ in the . s Adapting to , gradual

or doweor

As –

- given induced induced taxa This article isprotected rights by All copyright. reserved. Ban, S.S.,Alidina, H.M., Okey, Gregg, T.A., R.M. & Baltimore, D.,Berg, P.,Botchan, M.,Carroll, D., Charo, R.A., Church, G., Corn, J.E., D A.H.,Baird, Sommer, B. & Madin, J.S. (2012) Pole Babcock, R.C., Shears, N.T., Alcala, A.C., Barrett, N Aitken, S.N. & Whitlock, M.C. (2013) Assisted gene flow facilitateto local adaptation climateto REFERENCES This a is conceptual review article and includes no data to DATA ACCESSIBILITY theof manuscript AV led the overall conceptualization of the paper and all authors contributed AUTHORS DP Research Council (TW, AV, PDS: issue thankWe Dr Gareth Williams Nick Prof and Graham their for invitation to contribute this to ACKNOWLEDGEMENTS

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This article isprotected rights by All copyright. reserved. Accepted indicat transitional phases between the various scenarios by (b) tropical seaweed, (c) turf algae, or (d) coral. We illustrate here extreme projections, however temperate reefs, and three potential scenarios for future Figure 1. Article FIGURES es es the relative

Representation of key ecosystem functions in (a) current state

importance

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This article isprotected rights by All copyright. reserved. Adriana Vergés, (d) Brigitte Sommer. temperate transition zone, eastern Australia. Photo credits: (a) JohnTurnbull, (b) Fulton, Chris (c) dominated dominated by kelp;(b) Tropical fucoid seaweed forest Ningaloo,in western Australia; (c) AcceptedFigure Article 2 .

Photographs depicting system in Aksaki, Turkey; and (d) coral (a)

Warming temperate reef in Sydney, eastern Australia,

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