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Coastal ecosystems on a tipping point global warming and parasitism combine to alter community structure and function N., Mouritsen Kim; M., Sørensen Mikkel; Robert, Poulin; Fredensborg, Brian Lund

Published in: Global Change Biology

DOI: 10.1111/gcb.14312

Publication date: 2018

Document version Publisher's PDF, also known as Version of record

Citation for published version (APA): N., M. K., M., S. M., Robert, P., & Fredensborg, B. L. (2018). Coastal ecosystems on a tipping point: global warming and parasitism combine to alter community structure and function. Global Change Biology, 24(9), 4340- 4356. https://doi.org/10.1111/gcb.14312

Download date: 09. Apr. 2020 Accepted Article Phone: +4560202726 [email protected]. Email: Denmark. Aarhus, University, Aarhus Biology, Aquatic Biosciences, of Department Mouritsen, N. Kim CORRESPONDENCE: This by is protectedarticle reserved. Allrights copyright. doi: 10.1111/gcb.14312 lead to differences between this version and the throughbeen the copyediting, pagination typesetting, which process, may and proofreading hasThis article been accepted publicationfor andundergone peerfull but review not has 3 1 Mouritsen Kim N. synergy climate-parasite of impact Community HEAD: RUNNING function and combineto alter communitystructure and parasitism on a Coastaltipping ecosystems point:globalwarming Articles Research Primary : type Article DR. KIM NØRGAARD MOURITSEN (Orcid ID :0000-0003-3564-8328) Zoology, Otago University,Dunedin, New Zealand Fredensborg Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark Denmark Copenhagen, Copenhagen, of University Sciences, Environmental and of Plant Department Denmark Aarhus, University, Aarhus Biology, Aquatic of Biosciences, Department 3

1,* , Mikkel M. Sørensen M. , Mikkel 1 Version of Record. Please Version as this cite ofRecord. article , Robert Poulin , Robert 2 , Brian L. , Brian 2 Department of of Department Accepted Article This by is protectedarticle reserved. Allrights copyright. of26°C temperature Theheat-wave pressure. parasite under lower 21°C at seen as emerged structure community on impact synergistic temperature-parasite a similar 19° at addition, In 26°C. at community amphipod the prolonged heat-wave scenario, resulted in ancomplete almost parasite-inducedextermination of a simulating andparasitism, (19-26°C) temperatures elevating Further community. amphipod the on influence limited had parasitism of inabsence temperatures higher 4-degree contrast, leaving infaunal species largely untouched. In effect, species diversity dropped significantly. In but species epibenthic affecting species-specifically, decreased abundances amphipod changes: pr to 21°Cin However, temperature elevatingthe temperature (17°C) andparasitism, level of the parasite had littleimpact on the community.host microphallidpathogenic trematode, infected by the supported by field surveys to elucidate this questi approach mesocosm outdoor an apply we Here, warming. global of face the in community temperature and parasitismcombine may shapto how addressed yet has study no However, decline. to population host their causing temperatures, Mounting evidence suggests that transmission the certain of parasites is facilitated by increasing ABSTRACT article research primary TYPE: PAPER temperature-parasitism synergy, sensitivity temperature experiment,microphallid trematode, parasite vulnerability, species diversity, species richness, KEY WORDS: Amphipod community,host climatechange, communitycomparable ina way: species diversity declined and infaunal the specieswere favoured esenceof parasites induced massive structural on in a diverse intertidal community of amphipods amphipods of community intertidal diverse a in on e the functional structure of a whole host host whole a of structure functional the e Maritrema novaezealandensis Maritrema C, just two degrees above the present average,C, two present degreesabovethe just Maritrema novaezealandensis Maritrema per se per affected the amphipod amphipod the affected . Under present present Under . , mesocosm Accepted Article This by is protectedarticle reserved. Allrights copyright. key-stone a of phenotype or alteringabundance the by or indirectly populations, host specific regulating by directly either role community-structuring a play many and biosphere of the components areubiquitous Parasites parasite. and host between questioned. be can models single-species of validity general the communities, Walther, species 2010). amongdecisive Given are interactions the forces that ecologicalstructuring interactionsLuoto, (Araújo & Tylianakis 2007; etal., Gilman 2008; etal., 2010; Traill etal., 2010; across temperature ecosystems significantly that influences the strength outcome and of species fact that global climate change is not solely a tolerances,temperature seemingly forecasts robust their and species individual of ecology basic the distributions, species present of knowledge respond to these alreadyongoing climatechanges major is a scientific challenge.Based on will ecosystems ultimately and communities populations, how exactly predicting However, 2006). properties and function 2014; (IPCC Walther et al., 2002;Parmesan &Yohe, Harley2003; etal., worldwide, inturn changingcomposition the of organisms distribution and performance the affect to bound is warming global The forecast INTRODUCTION species. infaunal by dominated be to them changing functionally warming, global anticipated of face in diversity and abundance of terms in deteriorate will communities amphipod coastal that predicts our study and parasitism, of level relationship negative strong a demonstrating data field by corroborated are findings experimental Our species. epibenthic of expense the at Maritrema One species-interaction havethat received increasing attention inyears recent that is parasitism acrossowing 12sites. Hence, tothe synergisticof impact temperature matter of temperature, there is mounting evidence evidence thereismounting temperature, of matter of species assemblages and modifying ecosystem between current amphipod species richness and the the and richness species amphipod current between could be elaborated. However, aside from the the from aside However, be elaborated. could host specieshost (Minchella & Scott, 1991;Tompkins Accepted Article This by is protectedarticle reserved. Allrights copyright. Dangal et al., predation 2016), (e.g., Miller, Matassa & Trussell, 2014) andcompetition (e.g., (e.g., grazing of case the in recently beendocumented have properties community on interactions coastalcommunities crustaceans.of Additive and synergisticclimate effects of change and species unpreced willwarming cause associated global with raise the intriguing hypothesis that microphallid parasitism in concert with temperature increases (2) the absence of strong host specificity, and species-specific (3) parasite susceptibility, one may transmission, parasite temperature-dependent (1) Given 2011). Mouritsen, & Jensen Larsen, 2011; Poulin, & Gonchar Koehler, 2010; Poulin, & Koehler 1998; Mouritsen, & Jensen (Jensen, parasites bythe inflicted pathology dependent infection-intensity the or in infection to susceptibility in their evidence suggest that of addition, lines different that possess an importantecological role incoastal ecosystems (Mouritsen &Poulin, In 2002b). infecting of capable being alike), host definitive intermediate host. They show little host specificity towards their second host intermediate (and vertebrate definitive host,a gastropod crustacean firstintermediate host, second and a 2005; Studer, Poulin Tompkins, & 2013). Microphallids are engaged in 3-host cycles life including a intermediate hosts to the of extinctionbrink global under warming (Mouritsen, Tompkins &Poulin, been have hemispheres southern and northern the both from trematodes microphallid coastalpathogenic ecosystems where Hernandez, Poole &Cattadori, Poisot2013; al et (Marcogliese, 2001; Mouritsen &Poulin, 2002a; Poulin, 2006; Paull, Lafonte & Johnson, 2012; interaction and inturnparasites’ the ecologicalwill rolesbe sensitive toclimate fluctuations which temperature-dependent, highly is stages flat some particular in parasites, of range wide Mouritsen &Haun 2008; Hatcher, Dick Dunn, & Larsen2012; &Mouritsen, 2014). Interestingly, for a et al., 2002; Mouritsen & Poulin, 2005; Thomas, Renaud Guégan,& 2005;Woodet al., 2007; forecast to drive populations of their main crustacean second second crustacean main their of populations drive to forecast worms(Trematoda), the transmissionof infective means that the that ofmeans strengthhost-parasite the a taxonomically very diverse group of crustaceans crustaceans of group diverse very taxonomically a ., 2017). This has been evidenced especially in the guildsecondary of hostspeciesdiffer markedly ented changes to the structure and function of of function and thestructure to ented changes Accepted Article This by is protectedarticle reserved. Allrights copyright. novaezealandensis novaezealandensis Maritrema attention. of level same the received yet not has hand, other the on Parasitism, al., 2015). et Stenseth community structure and diversity. We hypothesised that elevated temperatures and parasitism andparasitism temperatures elevated that hypothesised We diversity. and structure community amphipod influence to combine and infection temperature of levels different how assess – to investigations field by supported – design experimental mesocosm a utilized We 2013). Tompkins, & 2005; Poulin, & Mouritsen (Fredensborg, dependent Maritrema of transmission The droppings. birds’ the via habitat intertidal the in distributed are snails, the shorebirds’ the within occurs reproduction Sexual de as serve bird) crustacean-eating other (or any crustacean second intermediate host (Martorelli etal., Red-billed 2004). gulls species from where infective larvae (cercariae) with released are the purposeof infecting the Island, New Zealand. Experiments Experiments Zealand. New Island, were conducted during australthe summer 2006/2007 in Otago Harbour and adjacent inlet, South Mesocosm experiments, associated field investigations and collection of experimental organisms sites Study AND METHODS MATERIALS community. host diverse a on warming global and of parasitism effect combined the unravel tocreation the of differently structuredcommunity. a attempt provides Our tostudy first the leading manner, species-specific highly a in but amphipods the to detrimental particularly be would Here we explore the above hypothesis by using the intertidal microphallid trematode trematode microphallid intertidal the using by hypothesis above the explore we Here cercariae tofrom first second intermediate hostknown is tobe strongly temperature- usesthe mud snail and its amphipod host community as a model system. system. model a as community host amphipod its and were performed at the Portobello Marine Laboratory (45°49’41’’S, (45°49’41’’S, Laboratory Portobello Marine the at were performed Zeacumantus subcarinatus finitive hosts reached by trophic transmission. transmission. trophic by reached hosts finitive digestive tract, and trematode eggs, trematode tract, to and digestive infective Studer, Thieltges & Poulin,2010; Studer, Poulin asonly its intermediate first host Larus novaehollandiae Larus Maritrema

Accepted Article This by is protectedarticle reserved. Allrights copyright. Harbourwere sampledduring 2001/2002 and 2003/2004 to test for an (45°49’55’’S, 170°40’15’’E). In addition, 12well-separated bayswithin c. the 20km long Otago on the nearby intertidal sand flats of Hoopers Inlet (45°51 170°38’29’’E),whereas field investigations and collec 2004; Bryan-Walker, Leung &Poulin, 2007). novaezealandensis that servesas the only firstintermediate hostmicrophallid tothe trematode experimental crustaceanswere collected in Hoopers Inlet. mudThe snail community, amphipod uninfected occurring naturally a on be based to experiments the for In order Amphipods material experimental of Collection parasitism. and structure community amphipod associated with sea lettuce only ( ( ( species free-swimming abundant highly were two which of densities significant in found were of amphipods species Six it. supporting microhabitats the and community amphipod occurring naturally a of structure the exactly match to constructed were mesocosms experimental the each within species each of density relative the lettuce, of sea beds and sand bare (unvegetated microhabitats of distribution relative the present, species amphipod of range the establish to aiming Heterophoxus stephenseni Heterophoxus Paracalliope novizealandiae Prior toexperimental collections, athorough investigationconducted was Hoopers in Inlet is absent here, and hence, also the parasite (Fredensborg, Mouritsen & Poulin, Poulin, & Mouritsen (Fredensborg, parasite the also hence, and here, absent is and and and and Paracorophium lucasi Paracorophium Aora Paramoera chevreuxi sp. and and sp. Lembos microhabitat (Appendix S1). Based on this survey, survey, this on Based S1). (Appendix microhabitat Ulva lactuca Ulva tions of experimental material were carried outcarried were material experimental of tions ), and), two were rare tube-building species sp.) (Table Appendix1, S1). Allsix species ), two were benthic mainly sedentary species species sedentary mainly benthic were two ), ′ 33 ″ ) ) whichwithin they found, were and S, 170°40 ′ in situ 10 Zeacumantus subcarinatus Zeacumantus ″ E) and Lower Portobello Portobello Lower and E) Maritrema relationship between

Accepted Article This by is protectedarticle reserved. Allrights copyright. of amount large a byrinsing collected were S1), Appendix sampling inHoopers The Inlet.remaining four specie Gonchar this Poulin, study). & 2011; serve as second hosts intermediate for trematodes and all were found uninfected. To establish the overall size distribution of the of the distribution size overall the establish To uninfected. found were all and trematodes for were dissected species amphipod each of individuals chosen haphazardly 30 community, seawater. running were stored animals processed laboratory, in the not When pipettes. using done was handling all experiments, the for hand by out sorted eventually microscope. minimize To mechanical damage tothe more than 23,000 amphipodindividuals a dissection under identification species and sorting for laboratory the to werebrought subsequently cases, a allwater. In thenstraining the until further processing. To establish their infection status, snails were placed individually in in individually placed were snails status, infection their establish To processing. further until and seawater filtered running 16-17°C with aquaria supplied relatively high (seeFredensborg, MouritsenPoulin, & 2004, 2005). Snails were kept in laboratory were collected byhand in amid-intertidal area Lower Portobello at where the infectionprevalence is ( snails mud medium-sized experiments, the for parasites of As asource Snails 4% formaldehyde in preserved were animals experimentation and measured from rostrum to telson under a dissection microscope (Table 1). All to prior just extracted was species of each subsample another amphipods, experimental Almost pure cultures of both both of cultures pure Almost To verify the absence of microphallid trematode infections in the collected amphipod collected amphipod the infections trematode in microphallid To of verify theabsence H. stephenseni H.

M. M. novaezealandensis 500 µmwas500 used sieve to prior to measurements and dissection. and dissection. measurements to prior in containers supplied with 16-17°C filtered filtered 16-17°C with supplied containers in and s, mostly associated with lettuce sea (Table 1, P. lucasi P. U. lactuca U. ad libitum (Koehler & Poulin, 2010; Koehler, Koehler, 2010; Poulin, & (Koehler could be obtained by core core by obtained be could extract the animals that that animals the extract in aseawater-filled bucket and

U. lactuca lactuca U. Zeacumantus subcarinatus Zeacumantus as food a source )

Accepted Article after seven days as well as immediately prior to experimentation. experimentation. to prior immediately as well as days seven after verify absence of infection, snails scored as uninfectedcercarial (no emission)were screened again stage of the parasite (Keeney, Waters & Poulin, 2007;Fredensborg, Mouritsen &Poulin, 2005). To This by is protectedarticle reserved. Allrights copyright. m weight wet (g Inlet Hoopers in lettuce sea of abundance the snails, and amphipods of case the in As seawater. running filtered with supplied containers in stored then and organisms faunal rinsed thorough thallus was the laboratory. Here, the experiments Table(see Appendix1, S1), sea lettuce was collected inHoopers Inlet and brought to the during of amphipods species some and forsnails substrate as well as food of asource As Sea lettuce S1). Appendix (see was eelgrass lettucesea collection investigated bedand prior bed) experimental specimens to of the Zeacumantus measured on average 13.1mm inshell height (range: 10.5-16.0 mm, snails These experiments. the in used were snails uninfected as well as latter the harbouring species than trematode other by occasionally infected found mature with snails conditions, these Under hours. five of minimum for a illumination under 25°C at dishes Petri seawater-filled S1). (Appendix amounts field-relevant with mesocosms supplying of purpose the with collection, to prior estimated To guide establishment of realistic snail densities in the mesocosms, the density of of density the mesocosms, the in densities snail realistic of establishment To guide across the various microhabitats present on Maritrema- infections start sheddingcercariae, theinfective larval ly with associatedly seawater toremove filtered the Lower Portobello sand flat (bare sand, sand, (bare flat sand Portobello Lower the M. novaezealandensis novaezealandensis M. Zeacumantus subcarinatus Zeacumantus n = 224). = but only snails -2 was was ) was Accepted Article This by is protectedarticle reserved. Allrights copyright. Gyrosigma (genera abundance high in diatoms of epipelic a range of presence the confirmed quality food source Table(see 1for relevant species).Light microscopy smallof sediment samples high- a with amphipods grazing epibenthic and detritus-feeding the provide to was mesocosms Paracorophium was alsocollected Hoopers from Inlet sieved and (m sediment base this to Inaddition seawater). running filtered (16-17°C storage for laboratory the to andbrought present organisms macrofaunal other any remove to mesh µm 500 a through sieved was substrate collected The individuals. juvenile of risk the excluded which absent, be largely Port Lower of area high-intertidal from sandy the amphipods, burying two the for As asubstrate Sediments rotifers), thus providing the predatory predatory the providing thus rotifers), present werealso groups meiofaunal of range to be precisely fixed (see next section). section). next (see fixed be precisely to experiment). outdoor provided greaterThe setting under scenario heat-wave or warming extreme (standa pressure parasite moderate under scenario warming global standard a simulating at aimed experiment Thefirst out. carried were days 14 lasting both experiments mesocosm outdoor separated temporally two February, and January During and protocol design Experimental , Navicula present. The purpose of including this fine and diatom-rich sediment in the the in sediment diatom-rich and fine this of including purpose The present. , Nitzschia , Plagiogramma H. stephenseni H. contaminating the experimental mesocosms with with mesocosms experimental the contaminating (ciliates, nematodes, copepods, ostracods and and ostracods copepods, nematodes, (ciliates, ). Aside from the community of microphytobenthos, a microphytobenthos, of community the from Aside ). H. stephenseni H. edium-fine sand), diatom-rich silty surface sediment sediment surface silty diatom-rich sand), edium-fine high parasite pressure (extreme-scenario (extreme-scenario pressure parasite high through a 250 meshµm 250 through a removeto juvenile obello. Here, these benthic species were found to to werefound species benthic these Here, obello. realism but did not allow for temperature levels levels temperature for allow not did but realism rd-warming experiment). The second aimed at an at aimed second The experiment). rd-warming with food items. and P. lucasi P. , sediment was collected collected was , sediment Amphora , Accepted Article below). (see experimentation to prior mesocosms replicated the establishing in involved labour substantial structure rather thanmultiple treatment-levels (see Rohr was al., 2011) et dictated by the parasites and higher temperatures withwithout and parasites. dichotomousThe treatment This by is protectedarticle reserved. Allrights copyright. sufficient to establish the two temperature treatments in the first standard-warming experiment. experiment. standard-warming first the in treatments temperature two the establish to sufficient was set-up This valve. float a by controlled was rate inflow which seawater, filtered running water Both seawater. unheated with containers 200 approx. contained m) 0.5 = d 1.0 m, = tank (h wa heater thermostat-controlled experiments, a the containers. experimental the of half and supplied heated and one unheated. The heated seawater tank =1.0m,d (h contained= m) 0.8 approx. L 500 animals. as serving organisms planktonic of supply steady temperature treatments, keepwater body the (2) relative This hour. every half water of full exchange cm 1 c. (each holes evenly dispersed 4 container, the of top the cm below Three S1). (Figure diameter and 21 cmin height resulting 491cm in a organisms. A constant flow rate of 18 L hour L 18 of rate flow constant A organisms. planktonic occurring naturally small contained andtherefore gravel through solely filtered was supply seawater The below). (see temperature experimental desired the at 33-34) (salinity: seawater filtered running with container each supply to used were mm, of5 diameter inner and an covered witha 500

The experimental mesocosm unit was atransparen was unit mesocosm The experimental Both experiments involved four treatments each: temperatures lower with without and The water supply system consisted of two large PVC tanks used as seawater reservoirs, one one reservoirs, seawater as used tanks PVC large two of consisted system supply The water μ m polyethylene mesh functioned as water outflow. Silicon tubes, 1 m in length length in m 1 tubes, Silicon outflow. water as functioned mesh m polyethylene -1 was established in each container, corresponding to a a to corresponding container, each in established was tanks were supplied with the same source of of source same the with supplied were tanks a food source for some of the experimental experimental the of some for source food a To maintain the desired water temperature during during temperature water desired the maintain To L and supplied the other half of the experimental experimental the of half theother supplied L and and sediment fully oxygenated, and (3) secure a a secure (3) and oxygenated, fully sediment and 2 ly high flow rate served to (1) obtain the required therequired (1)obtain served to rate high flow ly bottom surface area and a water volume of 9 L L 9 of volume water a and area surface bottom s submerged into the tank. The second seawater The submerged intothetank. s t circular PVC container, 25 cm in inner inner cmin 25 container, PVC circular t 2 ) Accepted Article This by is protectedarticle reserved. Allrights copyright. of shortage to Due S1). (Appendix Inlet Hoopers in densities natural their to corresponded 1) (Table mesocosm each added to eventually species species mainly associatedwith sea lettuce (Table The 1).number of individualsof each amphipod four remaining the by followed containers, experimental the to added simultaneously and out sorted were species amphipod benthic two the Firstly, days. two over performed was mesocosms the °C). (16-17 seawater unheated filtered of flow a with supplied were units mesocosm point this From organisms. experimental of the addition to prior settle to particle sediment suspended for left and supply water their to connected experime the some of for source food a added as then was sediment surface diatom-rich silty the of mmlayer a1-2 this, of Ontop substrate. cm 2 the flow. one unheated the into reservoir heated from the beincr to had also reservoir seawater unheated previously of the temperature extreme-scenario the experiment, However,subsequent the for experimental container. Alongwith the addition of snails, 10g column, of grease was layerthin a water out smeared just above top atof surface each the the (standard-warming experiment: One-way ANOVA, F ANOVA, One-way experiment: (standard-warming aver in difference any significant were there Lower at density natural their to corresponding mesocosm. extreme-scenario th of sixinstead experiment, experiment: One-way ANOVA, F Because of the large amount of amphipods processed, addition of the different species to to species different the of addition processed, amphipods of amount large the of Because each to added was sediment ofbase One litre After addition of the amphipod community, eight mud snails were placed in each container container each in placed were snails mud eight community, amphipod the of addition After 27/196 = 0.121, age snail shell height between mesocosm units p e planned ten individuals were added to each each to added were individuals ten planned e = 1.000). = To avoid escape of snails fromwater the and until commencement of the experiments, the until all commencement of and eased. This was accomplished by directing water water directing by accomplished was This eased. Portobello (Appendix S1). In neither experiments experiments neither In S1). (Appendix Portobello Lembos ntal amphipods. The containers were subsequently were subsequently containers The amphipods. ntal through a shunt equipped with a valve to control control to valve a with equipped shunt a through 23/168 mesocosm container equivalent to a depth of a depth to equivalent container mesocosm specimens during establishment of the the of establishment during specimens = 0.161, U. lactuca p = 1.000; = extreme-scenario thalluswas also placed in Accepted Article This by is protectedarticle reserved. Allrights copyright. 26.5°C) in the high temperature treatment (Student’s t-test, t reached 16.9°C (range: 14.6-25.4°C) in the low temperature treatment and 21.2°C (range: 17.8- warm loggers.temperature Hence, thestandard in bysubmerged the recorded as mesocosms’ temperature water the in variation day-to-day as well as diurnal overlying created This sun-radiation. and temperature ambient in variation diurnal meso the experiments, both for outside placed Otago Harbour &Poulin, (Studer 2012). However, the entire because experimental wasset-up pr evenat frequently encountered 25°C thatare and 19 of treatments temperature at aimed we experiment, extreme-scenario subsequent In the 2012), and higher temperaturea treatment of in21°C light of ongoingclimate changes (IPCC, 2014). 17°C, approximating present sea surface summer temperature in Otago Harbour (Studer & Poulin, of treatment temperature lower a at we aimed experiment mesocosm standard-warming In the settings treatment Experimental experiment. extreme-scenario subsequent treatment was replicated times the firststandard-warming 6 in experiment times the and in 7 Each ground. the from elevated PVC-trays drained in grid quadratic a in arranged mesocosms temperature treatments just prioronsetexperiments. the the to of temperature-logger was in a haphazardl submerged a Finally, S1). (Appendix Inlet Hoopers in abundance its to corresponding each mesocosm, 25.1°C (range: 22.7-29.0°C), respectively (Student’s t-test, t subsequent extreme-scenario experiment, figuresthese equalled 19.4°C (range:16.8-26.5°C) and The four experimental treatments (see next (see treatments The four experimental cosms were subject to uncontrolled but natural natural but uncontrolled to weresubject cosms esent in tide pools during low summer tides in ing experiment the realized mean temperature temperature mean realized the ing experiment section) were fully randomized across the across were fullyrandomized section) y chosen mesocosm at each of the two applied applied two of the each at mesocosm chosen y 154 1427 =24.50, = = 53.64, p <0.0005). that Note these p <0.0005). In the Accepted Article Lower Portobello Mouritsen Bay (Fredensborg, of 75%. This high level of parasitism corresponds ro sixof eight the mud were snails infectedpa inthe Fredensborg, MouritsenPoulin, & 2006;Studer &Po (see sites study our of vicinity immediate the in bays Harbour Otago across mean grand the to roughly corresponds infection of prevalence The37.5% treatments. no-parasite in infected was snail This by is protectedarticle reserved. Allrights copyright. parasite-induced mortality, and at elevated temperatures, any excess mortality will be ascribed to to be ascribed will treatments non-exposed to relative treatments exposed parasite in abundance 2010; Studer, Poulin Tompkins, & 2013). Consequently,post-experimental lower amphipod Jensen, 1997; Mouritsen, 2002; Fredensborg, Mouritsen &Poulin, Studer,Thieltges 2005; & Poulin, positive functions temperature of within experimental temperature the range (Mouritsenused we & expect the rate ofthat cercarial emission snail from hosts and in turn the transmission rate are mortality. microphallid previous trematodestudies with transmission,of agreement In also we intensity-dependent causing hosts secondary amphipod the to transmitted is larvae infective of these apart that is premise Afurther snails. infected of abundance the to proportional numbers the experimental design that infective is parasite larvae are released towater the column in of premise the parasitism, of source the as hosts snail intermediate first infected of number a using total numberof metacercariae successfully establis tr measure to made was attempt no undisturbed, data). mud snails (37.5%) were infected by simplicity, these treatments temperature four denotedwill 17, be and 19 25°C,21, respectively. measured within values rangesareall experimental temperature Owing tothe technical difficulties involved added eight the of three experiment, standard-warming the in parasitism of levels Regarding M. novaezealandensis & Poulin, 2006; Studer Studer 2006; Poulin, & ansmission success during the experiments (i.e. (i.e. experiments the during success ansmission rasite-treatments creating an infection prevalence prevalence aninfection creating rasite-treatments and the need to keep experimental units keep experimental to theneed and hed in the amphipod populations). Hence, by by Hence, populations). amphipod the in hed ughly to values recorded in the highly parasitized parasitized highly the in recorded values to ughly ulin In extreme-scenario2012). the experiment, inthe parasite-treatments whereas no in situ & Poulin 2012;unpublished (Studer &Poulin, (Studer For 2012). Accepted Article measured in the standard-warming experiment (31-200 ind. species ind. (31-200 experiment standard-warming the in measured were specimens amphipods 841 In total, possible. as perunit of amphipods number even a 1 This by is protectedarticle reserved. Allrights copyright. ind. metacercariae (no. loads parasite establish to dissected and telson) to (rostrum were measured treatments experimental four the of each from species each of individuals of a number Furthermore, andenumerated. species to according sorted then were amphipods Theretrieved formaldehyde. separately container each from µmmesh 500 a through sieved were then andsediment Water animals. attached any release to each mesocosms After termination of the experiments, remaining pieces of sea lettuce werethoroughlywithin rinsed protocol Post-experimental the contrast parasite between in treatments pressure comparable.bewill than the sharp rise used especially in the extreme-warming experiment (see MorleyLewis, & 2013), output cercarial of patterns different slightly in resulted have may experiments our of beginning exacerbation of infection pathology). Note althoughthat gradual a increase in at temperature the parasite in increase temperature-dependent only carried out in the standard-warming experiment ( experiment thestandard-warming in carriedonly out transmission. scenario experiment (36-180 ind. species few amphipod individuals ( individuals few amphipod the value of parasite loads as a measureof transm extraordinarily high mortality in extreme-warmingthe experiment,which samplelimited sizes and ). These specimens were haphazardly chosen across individual mesocosm units aiming to process as as process to aiming units mesocosm individual across chosen haphazardly were specimens ). These

≤ 5 ind. species ind. 5 -1 -1 ). Systematic dissections of ) were scored positive for infection to verify presence of presence verify to positive infection for were scored ) -transmission (and/or temperature-dependent temperature-dependent (and/or -transmission and retained animals were preserved in 4% 4% in preserved were animals and retained ission success emphasis (see Results),onlyin a n = 323; 31-60 =323;31-60 ind. species -1 ) and 722in the extreme- amphipods for infections were infections for amphipods -1 ). Due to to ). Due - Accepted Article This by is protectedarticle reserved. Allrights copyright. sediment core samples (0.012m within Otago Harbour during 2001/2002 and 2003/2004. Amphipods werecollected by sieving snails mud of population sympatric the in prevalence infection and structure community amphipod on Combined data parasitism and community amphipod between Field relationship (Appendix S2).Their distributional pattern may influence amphipods’the vulnerability toinfection. the unravel to conducted was experiment laboratory a protocol, above the to Inaddition of distribution vertical collecting surface sediment inhaphazardly chosenm 0.1 & Poulin, Similarly, 2010). mature species identification and enumeration inthe labora and dissection for trematode infections in the laboratory ( laboratory the in infections trematode for and dissection (Student’s t-test or Mann-Whitney test) because error-variances could not be stabilized through through stabilized be not could error-variances because test) orMann-Whitney t-test (Student’s contrasts pairwise of favour in abandoned was ANOVA two-way planned the experiment, scenario transformed assumptionsto meet the non-parametricor statisticsFor applied. were the extreme- byevaluation werepreceded tests parametric Statistical analyses wereperformed using Statistical Package for the Social Sciences (SPSS). All analyses Data & Poulin for(2006) namesand locations of theHarbour Otago bays sampled. Mouritsen Fredensborg, See results. experimental the with contrasted and analysed was population amphipod species richness/diversity and infection the prevalence inthe first intermediate host Mouritsen &Poulin 2005, 2006for details). Basedon data, these the relationship between M. novaezealandensis M. Z. subcarinatus Z. 2 , Zeacumantus n =15bay were obtained from intertidal flats of 12 separate bays bays separate of 12 flats intertidal from obtained were -1 cercariae when released to the water column when to cercariae released the ) through a500 of assumptions.violated, If datawere rank- snails snails mmin shell(>6 height)were by retrieved tory (for methodological details, see Mouritsen Mouritsen see details, methodological (for tory 2 followedareas sieving, preservationby n = 98-442 snails = bay μ m mesh, followed by preservation, -1 ; see Fredensborg, see ; Accepted Article do not necessarily reflect realized parasite parasite realized reflect necessarily do not or similar between treatmentstemperature (Table Note S1). recordedthat infection characteristics This by is protectedarticle reserved. Allrights copyright. expressed in units of species (2 ANOVA’s. Calculationof species diversity inde both experiments. Inall other cases,post Turkey hoc test were applied following successful standard transformations (log, square-root or rank). This applied also species to richness data from Paramoera indicative for excellent two-dimensionalvisualization. performed inPRIMER on square-root transformed data, resulting in values stress below 0.05that are of 3.8and 7.8individual chevreuxi species, free-swimming two The amphipod. of species the parasite treatments, where parasite loads va As expected, surviving amphipods were found infected by abundance Infection experiment Standard-warming RESULTS (metacercarial prevalence and load) were either gr were either load) and (metacercarial prevalence parameters infection main Statistically, temperature. high at none and temperature low at 6) levels were found in the benthic tube-builder tube-builder benthic the in werefound levels had no metacercarial infections at all, whereas whereas all, at infections metacercarial had no infected: weakly were lettuce sea with associated species amphipod two The uninfected. Th 0-7). respectively; range: ,

were themost heavily infected. reached 40.1 and 28.4 individualand 28.4 reached40.1 -1 (range: 0-15) at low and high temperature, respectively, temperature, high atlowwhereas and 0-15) (range: e e other infaunal species, H’ ; H’ = - ; H’ = Σ (p i )(log p )(log Paracalliope pressure/transmission at two the temperature -1 (range: 3-96), respectively. More moderate infection infection moderate More respectively. 3-96), (range: x (Shannon-Wiener) followed Krebs (1999)and is Paracorophium lucasi Paracorophium Lembos ried according to experi to according ried i )). Multidimensional)). scaling analyses were (MDS) eatest inthehightemp eatest Heterophoxus stephenseni Paracalliope novizealandiae novizealandiae Paracalliope sp. had 1.3 individual 1.3 had sp. harboured a mean metacercarial abundance abundance metacercarial mean a harboured Maritrema novaezealandensis Maritrema (0.93and 2.5 individual mental temperature and temperature mental erature treatment (21°C) treatment erature -1 on average (range: 0- (range: average on , was entirely entirely , was and and Paramoera solely in solely Aora Aora -1 , sp. Accepted Article This by is protectedarticle reserved. Allrights copyright. temperature/parasite main or interaction parasite temperature- significant statistically No manipulations. experimental to resilient remarkably proved 1c,d). (Figure treatment parasites temperature/no low the to comparison in 60% under just by reduced was treatment temperature/parasites high the in abundance their as species swimming temperature/parasite combination.However, were so they toa lesserextent the free- than Hence, thetwo itself. The effect wasnotlatter statistically significantof species two in any the (Figure 1c,d). though temperature increased from benefit to tendency a by also but treatment temperature/parasites high the in mortalities high byespecially driven 2), Table 1c,d, (Figure interaction parasite de combined are andparasitism temperatures elevated that underlining 2) (Table interactions temperature-parasite significant highly creates but of the two species, 1a,b).Elevatedtemperatures (Figure than 80% bothin wereeliminated species relative to low the temperature/noparasites treatment to whenexposed rates mortality high particularly 1, free-swimming 2).Thetwo Table amphipods, The six species of amphipods responded differently abundance Amphipod to species amphipod different the of susceptibility relative of the indication veryrough a as betaken solely can loads parasite species-specific Similarly, recruitments. and/or mortality host intensity-dependent by skewed be heavily may figures the as treatments, Contrary tothe epibenthicspecies, two the infaunal species, Aora and and Ulva Lembos -residing aoriidswere also particularlyvulnerable tothe high P. novizealandiae P. associated withvegetation the likewise showed significant temperature- per se per was clearly was most clearly the sensitive. temperature this Together had in comparison limited negative impact on survival, survival, on impact negative limited comparison in had trimental to these two amphipod species. P. novizealandiae P. parasites at elevated atelevated temperatures where more parasites effects were evident (Figure 1e,f, Table 2). Albeit 2). effects 1e,f, Table (Figure Albeit were evident to the temperature-parasite treatments (Figure M. novaezealandensis M. and H. stephenseni H. P.chevreuxi , showed , showed and and .

P. lucasi P. , Accepted Article different species’vulnerability relative to tr parasites temperature/no high the to relative in th mortality recorded The additional amphipod vulnerability Parasite stochasticityinvolved.be may on impact positive have a to tended parasites of presence the Strangely, 1). (Figure 17°C low the at by parasitism influenced parasites.temperature/no lucasi Paracorophium th in than treatment temperature/parasites

This by is protectedarticle reserved. Allrights copyright. index clearly identifies each succe thepathology and hosts encountered) are hence encompasses behavioural aspects (the parasites access hosts),the to infection success (when especially so species; all of least the affected were amphipods benthic the synergy, temperature-parasite regardless of parasite level(particularly (particularly regardless temperature of non-significant, both species showed consistently lowerabundances in parasite treatments the mean body size (see Table 1;mean r bodysize(seeTable stephenseni H. the aoriids,whereas the two sediment dwellers stand out as least the vulnerablespecies, especially Notably,viewed amphipodacross six all but species, none H. stephenseni H. (Figure 2).This pattern was entirely unrelated to experimental the amphipod species was somewhat more affected, reduced by 50% relative to the low low the to relative 50% by reduced affected, more somewhat was

P. novizealandiae P. Aora that attained only 18% lower abundance in the high high the in abundance lower 18% only attained that s = 0.143, = abundance at this temperature. However, numbers are low and and low are numbers However, temperature. this at abundance P. lucasi P. p H. stephenseni H. and = 0.787). = Maritrema e low temperature/no parasites treatment. treatment. parasites e low temperature/no P. chevreuxi ) as well as lower abundances at high temperature temperature high at abundances lower as well as ) eatment (%) provides an useful measure of the of usefulmeasure an provides eatment (%) e high temperature (21°C)/parasites treatment (21°C)/parasites high temperature e infection. This mortality-based measure will ssful trematode larva inflicts.vulnerability This ) (see Table 2for ) (seeTable as the most exposed species followed by Aora sp. appeared markedly markedly sp.appeared p -values). In terms of Accepted Article sensitive species in the standard-warming experiment disappeared. This could not be substantiated besubstantiated not could This disappeared. experiment standard-warming the in species sensitive 5). Owingnotable tothe latter, the two-way temperature-parasitism interaction evident in most the temperature/parasites treatment, and influencednegatively by high temperature on its own (Figure the high temperature/parasites treatment, reducednumbersgreatly already 19°Clow in in the community inall treatments. Most specieswere entirely eliminated frommesocosm several units in parasitism and temperature both up Stepping abundance Amphipod Extreme-scenario experiment community. host different uniquely a create to synergistically act parasitism and temperatures elevated Hence, communitiescluster markedly form a the separated communities from the remaining in treatments. summarizedvisually inFigure 4a. Here, isclear that the it high temperature/parasites mesocosm This by is protectedarticle reserved. Allrights copyright. and temperature/parasites treatment is owing largely to extinction the two ofthe species rare statistically variance(no all in butone treatment) (Figure The3b). lowspecies richness in high the be verified not could this although richness species for emerged pattern overall Asimilar 3a). (Figure However, elevatedtemperatures treatmen temperature/parasites interaction (Figure 3a, Table 3)resulting from aparticularly species diversitylow in the high temperature-parasite significant highly a showed index Shannon-Wiener The structure. community trea experimental the of impact The differential structure community and Diversity Lembos The impact of the experimental treatments on amphipod community structure is is structure community onamphipod treatments experimental the of The impact sp. in some mesocosm units. units. mesocosm some in sp. t whereas the other treatments otherthe whereas t per se per negatively influenced the Shannon-Wiener index somewhat somewhat index Shannon-Wiener the influenced negatively had severe consequences for the amphipod amphipod the for consequences severe had tments on species abundances influenced overall overall influenced abundances species on tments showed very limited impact. Aora sp. sp. Accepted Article 19°C. Interestingly, the previously parasite-resistant species, benthic two and This by is protectedarticle reserved. Allrights copyright. and temperatures high of effect synergistic the to contrary that indicates which 3d), (Figure retained appears interaction temperature-parasitism the contrasts pairwise on based However, error-variance. heterogeneous to due performed be not could analysis two-way richness, species of case In diversity. species amphipod on effects negative isolated have andparasitism temperature both scenario experimental extreme underthis that demonstrating 3), (Table significant 3c, evident main ef the Table Instead, 3). (Figure was interaction temperature-parasitism notwo-way treatment, parasites temperature/no high The pattern in species diversity mirrors that of abundance: owing to significant reductions also in the structure community and Diversity uninformative. considered was measure synergy latter the experiment, warming to almost mortality 100% in highthe temperat Note percentages that inserted in of the Figure 5(effect twostatistical size contrasts) differ qualitatively from in those inserted Figure 1(effec persisted in significantany numbers this in temperature/parasite high treatment. at 25°C (Figure 5e). mortality parasite-induced massive suffered and 19°C at already levels parasite high bythe affected ( species epibenthic four the in particularly high, rather Mortality inrates parasite relative to treatments the low temperature/no parasites were treatment experiment. standard-warming the in seen as patterns same the follow to tended responses specific vari instable error to due though, statistically, Lembos sp.), and these were also greatly influenced by temperature were temperature influenced these alsogreatly by and sp.), Heterophoxus P. lucasi was the most parasite-sensitive show parasite-sensitive most the was

stephenseni

ance regardless of data-transformations. Species- of data-transformations. regardless ance was, however,only the species of the six that ure/parasites present tr present ure/parasites fectsof temperature and parasitism were highly t size of the parasite-temperature synergy). Owing synergy). parasite-temperature of t size the H. stephenseni H. P. novizealandiae ing quite high mortality already at Figure 1e)(see was strongly eatment intheextreme- and per se per P. P. chevreuxi (Figure 5a-d).Ofthe , Aora sp. sp. Accepted Article This by is protectedarticle reserved. Allrights copyright. amphipod species. ranges temperature experimental applied the parasitism, between amphipod species richness (see Table S6 for S6 Table (see richness species amphipod between Across the 12investigatedOtago Harbourwas bays, there ahighly significant negative relationship evidence Field ways. different in so do they intriguingly, that both temperatureelevated and community ownparasitism on their affect structure, most and scenario, the remainingthree treatments alsocluste amph different uniquely a creating in parasitism and temperature of impact synergistic the demonstrates further This 4b). (Figure treatments other experiment, the high temperature/parasites that mesocosmscluster together the and away from (with other species of trematodes) results in significanta total regression (r filholi chlorophyll- sediment diameter, particle sediment predictors) (as corrected statistically are prevalence infection than species richness.negative This relationship remains ifeven potentially influentialpredictors other in the local mud snail population (Figure 6). Infection prevalence explained 74.1%of variation the in infection prevalence in mud snails the emerges statistically as sole significant predictor (r = 0.014) S7). (Table

abundance, New Zealand cockle cockle Zealand New abundance, The MDS-visualization of these structural pa

Austrovenus stutchburyi Austrovenus ipod community. Furthermore, under this extreme extreme this under Furthermore, community. ipod for. A multiple regression analysis entering also also entering analysis regression multiple A for. tterns shows,in as standard-warming the r apart from each other (Figure 4b), emphasizing (Figure each other from r apart species involved) and the infection prevalence per se density and cockledensity infection and intensity are are unable to eliminate any of the a content, ghost shrimp 2 = 0.922; = p = 0.033) but = 0.033) p Callianassa 2 =0.810; p

Accepted Article This by is protectedarticle reserved. Allrights copyright. A marginal significant negative relationship also exists between amphipod species diversity (r prevalence infection snail and index Shannon-Wiener of in terms other than prevalence, eroded this negative correlation correlation thisnegative (r prevalence, othereroded than diversity of predictors potential for correcting analysis, regression multiple a However, shown). ongoing climate changes. changes. climate ongoing the under ecosystems intertidal Zealand in New community-engineer very potent an emerging, temperature-parasitism scenarios. highlights trematode study thus the The complete risk amphipods dwelling sediment these diversity declines, and functionallydevelop into assemblages dominated by infaunal species. Even and changes structural major face will They communities. amphipod intertidal to detrimental particularly be will andparasitism temperature increasing of action combined the present, warming sc future under that suggests Our study DISCUSSION as a whole. However, the common common the However, whole. a as detrimental parasite transmission stressin nor severetemperature the amphipodcommunity taken fluctuatio diurnal natural were superimposed levels 3a,b 1, (Figure unaffected largely community host about 4degreeshigh exposure temperature mean to a surface summer temperature in(c. 17°C) absencewell as as presencemoderate of parasitism, and sea mean present to Exposure clear. remarkably was and parasitism temperature of manipulation experimental the to reaction community’s amphipod The variations. temperature to responses naturally mirrored a Themesocosm experiments their and interactions interspecific and intra- existing integrated thus and possible experimentally Paracalliope novizealandiae Paracalliope enarios as well as short-term heat-waves at at heat-waves short-term as well as enarios and Although and 4a). the temperature experimental elimination under more extreme, yet possible, possible, yet extreme, more under elimination ns peaking around 25-26°C, this did not result in in result not did this 25-26°C, around peaking ns er in absence of parasitism, left the amphipod theamphipod left of parasitism, er inabsence occurring intertidal ec intertidal occurring 2 p =0.445, showed signs of temperature 2 =0.0.336, p = 0.377). = M. novaezealandensis M. p osystem as as osystem as much = 0.048; data not as as Accepted Article whole. Only the infaunal theinfaunal whole. Only a as extinction of brink the to it bringing and 5), 4b 3c,d, (Figure community amphipod the on impact S2). Figure and 4a 1, 3a,b, (Figure amphipods byinfaunal dominated become to structurally shifted and richness, species also and marginally Ineffect, 1). (Figure rareaoriids speciesthe and common species-specific free-swimming affecting highly especially the manner, a latter to in die-off This by is protectedarticle reserved. Allrights copyright. community, evidenceddifferent clustering by of mesocosm units totreatmentsaccording in the amphipod the on effects structural different inherently have andparasitism temperature impa the exacerbate simply not does parasitism similarity, do simp not increasing temperatures the structuralchanges alsocombined forseen the temperature-parasite synergy. Regardless of this impa temperature aswell. Thisisolated measures novizealandiae temperatures by themselves deteriorated the community, having negative particularly effects on of extr the soaring4b). Under temperatures the (Figure parasites without 19°C at that from different structurally community amphipod an leaving 5), and 3c,d (Figure richness and diversity species in reductions marked in resulted abundance host in species-specific parasite-induced Again, declines present sea temperature. surface community manifested itself already at amean temperature of c. 19°C, just two degrees above extreme temperature-parasite synerg scenario the this under Interestingly, richness. and diversity species both in decreases substantial causing elicited significant temperatures higher the Likely, community. host the for consequences profound with synergism apotent created parasitism and 21°C) (c. temperatures elevated combining However, and 3a). 1a (Figure index diversity Shannon-Wiener the of decline modest a into translated which sensitivity, Further elevating parasi temperature levelsFurther and and and Maritrema Paramoera chevreuxi Paramoera Heterophoxus stephenseni Heterophoxus transmission from snails to amphipods (see Introduction) causing the the causing Introduction) (see amphipods to snails from transmission but also the aoriids (Figure 5a-d), and in turn on diversity diversity on turn in and 5a-d), (Figure aoriids the also but ly exacerbate the impact of parasitism, and and of parasitism, impact the exacerbate ly eme-scenario experiment peaking at 29°C, high 29°C, at eme-scenario experimentpeaking ct of increasing temperature. On their own, own, their On temperature. ct increasing of the communitythe deteriorated diversity in terms of ct favouring the benthic species hence resembles resembles hence species benthic the ct favouring istic impact of the two factors on the host host on the factors two the of impact istic remained in any significant numbers, obviously te pressure only exacerbated the synergistic synergistic the exacerbated only pressure te P. P. Accepted Article This by is protectedarticle reserved. Allrights copyright. vulnerabilitycomparison in tothe free-swimming species (Figure 2). parasite lower somewhat their for argue rate, contact host-parasite and rate ventilation low turn Maritrema mayperiodically individuals some that means which incontrast, live intubes attached tosea lettuce dr aoriids, The 1997). Jensen, & Mouritsen (see parasites and host between rate contact ahigh ensures high their where S2), (Appendix surface sediment withcontactrepeatedly bring specimens into these are particularly active and likely thus expressto highestthe metabolic rates. Together, this may free-swimming the species, amphipod six the Of S2). (Appendix vulnerabilities relate to speciesthe overallbehaviour 1)in (Table relationof to the that parasites re Such beexpected. also would species amphipod positive relationship between vulnerability and the However, size-dependent if parasite susceptibility sole is the operating process across species, a S3). (Appendix treatments temperature/parasitism high in the smallest be to tend that amphipods hosts constitute Themaylarger latter targets. be Larsen &Mouritsen, 2014). occursThis either as asimple function of time(age) orbecause larger rate (Fredensborg, Mouritsen &Poulin, 2004;Bates, Poulin & Lamare, 2010; Koehler &Poulin, 2010; larvae tend toaccumulate larger in host the theindividuals population high of a die-off then that at Maritrema as (such trematodes microphallid by induced Mortality clear. entirely not are vulnerability However, 2). (Figure temperature increasing at species differential vulnerability tothe increased number parasiteof larvae expected tobe released influence. separate factors’ these from beanticipated easily cannot structure whose community aunique creates factors two of the action combined the Consequently, 4b). (Figure MDS-plot The structural changes of the amphipod community are for the main part a result of the host host ofthe result a part main forthe are community amphipod the of changes The structural ) in amphipod second intermediate hosts is intensity-dependent, and the trematode trematode the and intensity-dependent, is hosts intermediate second amphipod in ) cercariae. This, together with their sluggish the processes leading species-specific tothis reflected in the body sizes of post-experimental sizesof body in the reflected ventilation rate (abdominal appendage beating) beating) appendage (abdominal rate ventilation ifting across sediment the surface (see Figure S1), lationship notdid exist. Rather, different the the bulk of swimming cercariae just above the the above just cercariae swimming of bulk the pre-experimental mean body length of different different of length body mean pre-experimental be elevated above the highest of concentrations highest above the be elevated behaviour indicating low metabolism and in in and metabolism low indicating behaviour P. novizealandiae P. Heterophoxus stephenseni and and P. chevreuxi P. is, as as is,

Accepted Article vulnerability inpresent the ecosystem. as of behavioural importance the emphasizes clearly susceptible to environment, sedimentary protective its outside This by is protectedarticle reserved. Allrights copyright. Clausen, On other the 2014). hand, migratory some shorebird populationsdecrease may owing to (Hughes, 2004;Maclean al.,et 2008;Godet, Devictor, Jaffré & 2011; Ausden, 2014; Clausen & densities bird elevate may rise level sea to due squeeze coastal addition, in species; resident a to due shorebirds migratory of times residence & Poulin In 2006). intertidal ecosystems, climate changes can be envisaged toresult inlonger Mouritsen (Fredensborg, eggs parasite the supply that hosts bird definitive of density the of function Zeacumantus the in prevalence infection the Inherently, changes. climate by influenced may be hosts snail has yet attempted topredict infection how the prevalence byfirst trematodes intermediate in the average.Likelyexperiment present clearly above is 2014), the choice of an infection prevalence in the snail population of 75% in the extreme-scenario globalwarming and anticipated increases in frequency, duration and severityof heat-waves (IPCC, also have been inplay. observed overall parasite vulnerability, species-specificvariation in internal defence systems may the for account may considerations behavioural above the Although infection. to vulnerability and aoriids the between behaviourally usually case. the In comparison, the sediment tube-building temperature means high activity, bringing these individuals tothe sediment than surface often more in temperature/parasitism the high treatmen low vulnerability expectable.therefore is Interestingly, directlychallenged by en burrower, sediment a free-living Whereas the mesocosmsWhereas the ongoing regimes can the justified by temperature be experimental snail population, and probably all other snail host populations alike, is a positive positive a is alike, populations host snail other all probably and population, snail Maritrema infection than tirely beyond the reach of the swimming parasite larvae and its its and larvae parasite swimming of the reach the beyond tirely It could also explain the marked marked the explain also could It H. stephenseni H. P. novizealandiae P. t high theextreme-scenario of t experiment: H. stephenseni milder winter climate, which could also benefit benefit also could which climate, winter milder owingcomplexity tothe topic, of the no study pects inshaping the species-specific parasite andintermediatetherefore displays an (Koehler, Gonchar Poulin, & 2011). This Paracorophium lucasi Paracorophium turns out to be even more to out turns be Heterophoxus Maritrema can be placed placed can be decline seen seen decline cercariae cercariae Accepted Article This by is protectedarticle reserved. Allrights copyright. novaezealandensis Maritrema exterminating am than the rather the trematode intermediate hosts are drivenor more less extinction, to the parasite cyclelife will be disrupted, thus second the if that consequence logic the by challenged maybe hosts amphipod of community regime. present temperature experime our that underlines 6) (Figure parasitism relati negative strong a of existence the Indeed, parasitism. increasing with diversity amphipod decreasing of findings experimental our of relevance field the test to opportunity unique a provided bays, across populations snail local in prevalence future, local well a now then at future. as the scale as in making our extreme scenario-experiment highly relevant,if not on abroad spatial scale inthe 2006), Poulin, & Mouritsen (Fredensborg, Harbour Otago within bays some in occur presently extreme-scenarioparasitism of level experiment’s populationcould well increase rather than decrease ina future warmer world, justifying the qualitative considerations tentatively suggest that in purely these Combined, droppings. bird in surface sediment the on deposited eggs and parasite the activity theof poikilothermic host,snail couldwhich turn in increase contact between rates host infected of trematode greater heat-tolerance by offset a presentsystemlatter, be however, may in the related summer mortalities (Fredensborg, Mouritsen& Poulin 2005, Mouritsen &Poulin The 2002). heat- greater suffer also but survival, winter greater through temperatures winter from higher Wauchope et al., The 2017). snail hosts themselves, and hence the trematodes within,could benefit reproductive failurerapidly inthe warming arctic andsubarctic breeding grounds (IPCC, 2014; This field-validated experimental prediction of a future deterioration of the intertidal intertidal the of deterioration future a of prediction experimental field-validated This The fact Otago presentlythat Harbour supportsvariation great trematode infection in Zeacumantus snails Bates etal., (see Agenerally2011). milderclimatebound is toincrease utilizes a particularly wide spectrum of secondary host species, species, host secondary of spectrum wide aparticularly utilizes onship between amphipod species richness and snail snail and richness species amphipod between onship phipods. This scenario is unlikely, though. though. unlikely, is scenario This phipods. . In any case, the applied high prevalence does prevalence does high theapplied any case, . In ntal predictions are in play already under the the under already play in are predictions ntal fection prevalence in host firstintermediate in the prevalence fection Accepted Article This by is protectedarticle reserved. Allrights copyright. 1984). (Hoenicke, manner temperature-dependent a in species dominant the targeting by zooplankton freshwater of a community alter to seems that fungus a involves assemblage host multi- a on study only The phage. a of presence the in bacteria of species two for same the found two of frequency Similarly, showed Fleuryetal. (2004) the that impact parasitoid of a on the relative species. sibling parasite-resistant but abundant less a for way the paved cit.) (op. heat-wave Little comparable evidence appears toexist. Larsen, Jensen &Mouritsen (2011) a during amphipod corophiid abundant an of elimination parasite-induced the that demonstrated S2). (Figure amphipods infaunal eventually repopulate flats. intertidal the In nearer however, future, the ecosystemthis belongs to & Poulin, 2007; Bates, PoulinLamare, & 2010) – and high temperatures they over may evolutionary time adapt resistparasite-infections tobetter (seeBryan-Walker, Leung Zeacumantus where bays intertidal or habitats sublittoral in pockets low-parasitism to particular in species increase in frequency of prolonged heat-waves is trematodes duringweekheat-wave a3 (Jensen &Mouritsen, Hence, 1992). anticipated the future microphallid by out wiped was amphipods corophiid of population dense wherea hemisphere synergycan act veryshort on timescale a indeed. hosts. definitive eating Maritrema parasite loads (Koehler &Poulin, Therefore, 2010). absence in of a dense amphipodcommunity the Larger decapods inparticular are tolerant of microphallid infections, generally supportinghigh ranging from amphipods overisopods todecapods and alliedcrustaceans (Koehler &Poulin, 2010). The mere 2 week duration of our experiments indicates that the temperature-parasitism temperature-parasitism the that indicates experiments our of duration week The mere2 life cycle maycontinue to exist, shunted through the decapod secondary hosts to crab- snails are few. Owing to tremendous the selection pressure this poses on the animals, Drosophila specieswas temperature-dependent, and Brockhurst etal. (2006) bound to increasingly limit epibenthic amphipod amphipod epibenthic limit increasingly to bound Similar evidence is available fromnorthern the per se per that –and matter for Accepted Article echinostomatid trematodes may tend to counte to tend echinostomatidmay trematodes and microphallid by played roles engineering ecosystem the hence, and 2006), (Poulin, dependent (Mouritsen & Poulin, 2005, 2010). transmissionThe trematodes of these is likelyalso temperature- impactcockles’ on the burying behaviour, tofacilitate theintertidal crustaceancommunity Zealand cockle sole key-stone trematodehaunting intertidal animals. Echinostomatid trematodes infecting the New novaezealandensis of predictions precise for beimperative will hosts snail intermediate first infected of density the determining processes complex the disentangling Also, future. the for a challenge is game temperature-parasite this in losers and winners of set full the unravel To species. trematode single this by modified be to likely is community crustacean intertidal entire the amphipods: novaezealandensis by used spectrum host wide the experiments, mesocosm present the in community amphipod diverse a of inclusion Despite scrutiny. further for potential a bearing ecosystems, across together withpresent the results emphasize itsgeneral importancecommunity for structuring communities. natural for consequences serious likely but unpredictable with interactions, interspecific other and parasitism modulate also can warming global with concurrently occurring changes environmental additional Several 2015). success of its snail-to-amphipod transmission (Harland, MacLeodPoulin, & 2015; MacLeod & Poulin, negatively snail intermediate host the the of first trematode affect (Fabry (Kroeker organisms of individual recognised major threat a marine to as ecosystems itsimpactsthrough onlyon performance not the with parasitism to community alter structure. For instance, ocean acidificationincreasingly is This by is protectedarticle reserved. Allrights copyright. et al. Although a limited list indeed, the above studies on temperature-parasitism synergy synergy temperature-parasitism on studies above the indeed, list alimited Although interact may that change environmental of aspect one only is temperature rising Of course, , 2008; Allan , 2008; Austrovenus stutchburyi Austrovenus ’ future role as an ecosystemrole Finally,’ as an engineer. future suggests the that identified temperature-parasitism synergymay beyond reach et al. et , 2013). In, 2013). our study system, reduced seawater pH has been shown to et al. , but2010), also on the strengthof interspecific interactions as secondary hosts have been shown, solely through their their through solely shown, been have hosts secondary as ract each other as temperatures increase. increase. temperatures as other each ract M. novaezealandensis M. M. novaezealandensis M. M. M. M. is not the is and the the and Accepted Article This by is protectedarticle reserved. Allrights copyright. paper. the finalizing for environment necessary the providing for Dunedin, Department to debt in is author leading The input. and invaluableneed technical assistance whenever We wish Portobelloat staff tothank Marine the ACKNOWLEDGEMENTS across systems. climate variability Mouritsen (e.g. &Poulin 2002a), such non-linear response widespreadmay be ma Because ondiversity negative. turns influence po tipping or threshold a temperatures, increasing parasite the as However, diversity. crustacean novaezealandensis competitive elevates diversity. releasethat U 2014). By targeting the often dominantcompetitor or keystone species, parasites the will induce a & Lafferty, 2006;Fenton &Brockhurst, 2008; Hatcher,Dick &Dunn, Larsen 2012; & Mouritsen, guildbelieved are tomaintain or even boost biodiversity (Dobson &Hudson, Hudson,1986; Dobson investigations. contextclimate of change willbe amost challengingbut also very interesting endeavour for future Unravelling the parasite full community’s integrated impact on the communityintertidal inthe host on the impact asymmetrical with parasites generalist and parasites specialist Generally, may indeedmay occupy such structuring and role participate in maintaining nder average conditions, the generalist parasite parasite generalist the conditions, nder average pressure on the host community increases with Laboratory, Dunedin, for access to their facilities theirfacilities to access for Dunedin, Laboratory, ny host-parasite system int will beint reached where initially the positive of Zoology, Otago University, and Graeme Sykes, Sykes, Graeme and University, Otago Zoology, of ed. Thanks also to the reviewers for valuable s appear sensitiveto M.

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oia Macroalgae, Aoridae Macroalgae, Aoridae Benthic, Corophiidae tube- Benthic, Phoxocephaliidae free- Macroalgae, Eusiridae Macroalgae, Paracalliopiidae tube-building tube-building building living free-swimming swimming free- epibenthic, and ecotype tube-building tube-building Omnivore, highlyOmnivore, active mobile grazer, highly active and Epiphytic/epibenthic behaviour Feedingand type moving and sedentary feeder, slow detritus grazer, Epiphytic moving and sedentary feeder, slow detritus grazer, Epiphytic Sedentary and grazer microalgae detritus feeder, Surface moving slow Infaunal predator, and mobile Clason etal. Hewitt (1995) Thrush & Pridmore, Cummings, (1972) Barnard Source Body Moore (1997)Moore Dixon & (1997)Moore Dixon & Hewitt (2004) & Gibbs (2004) al. et Ellis Broyer (2001) Chapelle & De Scailteur, Dauby, (2003) SE , n ) (this 4.3 (0.20, 50) 3.5 (0.12, (mm) length 15) 5.4 (0.23, 45) 3.9 (0.19, 50) 2.9 (0.19, 50) 3.8 (0.09, 50) 10 25 34 83 103 205 mesocosms No. in Accepted Article stephenseni Heterophoxus Lembos This by is protectedarticle reserved. Allrights copyright. A lucasi Paracorophium chevreuxi Paramoera novizealandiae Paracalliope Species F mesocosm (no. abundance amphipod post-experimental including Table 2 remaining cases term. In latter the case, the degrees of freedom F- and requirements. but species all for untransformed are Data variables. independent as (17/21°C) andtemperature (present/absent) parasitism factors dichotomous ora s. .5 084369001 8.015 0.071 3.649 0.814 0.057 sp. * p The standard-warming experiment. Summary statistics of full-model Two-way ANOVAs ANOVAs Two-way of full-model statistics Summary experiment. standard-warming The s. .3 008142022 7.903 0.242 1.452 0.058 4.032 sp. -values originate from a reduced model ANOVA excluding the non-significant interaction interaction non-significant the excluding ANOVA model reduced a from originate -values * p -values in bold denote statistically significant effects and *denotes that main effect df =3/20 .0 .8 .6 .0 0.746 0.100 0.107 0.782 0.075 0.079 2.969 3.308 0.083 3.508 2.679 0.117 Interaction 131.528 55.674 Temperature Parasitism Source of Sourcevariation of <0.0005 <0.0005 p

are 2/21 (treatments/error), whereas inthe (treatments/error), whereas 2/21 are 112.716 110.298 F Aora sp. that were rank-transformed to meet meet to rank-transformed were that sp. -1 ) as dependent variable and the the and variable dependent ) as <0.0005 <0.0005 p 91.824 91.824 26.118

F <0.0005 <0.0005 0.011 0.010 p Accepted Article This by is protectedarticle reserved. Allrights copyright. 46.072 Extreme-scenario 58.384 Standard-warming F Experiment statistically significant effects freedom ( of Degrees variables. independent as 19/25°C) extreme-scenario: 17/21°C; (standard-warming: factors dichotomous the and variable dependent as 2H') index, (Shannon-Wiener diversity amphipod post-experimental including ANOVAs Two-way Table 3 Standard-warming and extreme-scenario experiments. Summary statistics of full-model full-model of statistics Summary experiments. and extreme-scenario Standard-warming df ): 3/20 (standard-warming) and 3/24 (extreme-scenario). (extreme-scenario). 3/24 and (standard-warming) 3/20 ): aaiimTmeaueInteraction Temperature Parasitism Source of variation <0.0005 <0.0005 p parasitism (present/absent) and temperature andtemperature (present/absent) parasitism 104.267 50.106 F p -values in bold denote denote bold in -values <0.0005 <0.0005 p 44.434 008 0.848 0.038 F <0.0005 p Accepted Article Lembos parasites treatment. recorded relative treatment the to 21°C/parasites the in abundance the 21°C/no recorded in vulnerability to Figure 2 highlight level the interactionof Appendix for S1 details). that Note inserted lines do not indicate linear relationships but serveto swimming; green: tube-building on vegetation free- (blue: microhabitat for affinity species amphipod the indicate bars Colour parasitism. and temperature of impact synergistic of the measure standardized a i.e. treatment, absent number 21°C/parasites present individuals of in the compared treatment 17°C/parasites to the for exact Table S2 0.001); see This by is protectedarticle reserved. Allrights copyright. according totemperature-parasite treatmentsind. (mean mesocosm Figure 1 Figure captions Figure 3 1 Figure in inserted those as same the not are proportions tests of treatment pairs are indicated asterisks by between markers (* extreme-scenariono. species (c,d). mesocosm Values mean experiment are according totemperature-parasite in treatment the standard-warming experiment and (a,b) the ○ : parasites absent; full line and line full absent; : parasites sp.; Standard-warming experiment. The six experimental amphipods species’ relative relative species’ amphipods experimental six The experiment. Standard-warming Standard-warming experiment. The post-experimental abundance of amphipod species species amphipod of abundance post-experimental The experiment. Standard-warming Post-experimental amphipod diversity (Shannon-Wiener index [2 index (Shannon-Wiener diversity amphipod Post-experimental Hs : Maritrema novaezealandensis Heterophoxus stephenseni Heterophoxus Pn : Paracalliope novizealandiae Paracalliope p -values. Inserted percentages indicate proportional reduction in the the in reduction proportional indicate percentages Inserted -values. ● : parasites present.Signi ; Pl : ; brown: sediment burrowers; see Table 1 and 1 Table see burrowers; sediment ; brown: infection (%) as judged bythe excess mortality Paracorophium lucasi Paracorophium ; Pm : Paramoera chevreuxi Paramoera fi cancelevels accordinghocpost Tukey to . Note that the here depictured depictured here the that Note . -1 ± p < 0.05, ** <0.05, ** SE H’ ; ] and species richness) -1 n ± = 6).Dashed = line and SE ; A ; : p n Aora

= 6 (standard- 6 = ≤ 0.01, *** sp.; sp.; L : p

≤

Accepted Article This by is protectedarticle reserved. Allrights copyright. and warming) (extreme-scenario) post hoc tests of treatment pairs are indicated by asterisk between markers (* (* markers between byasterisk indicated are pairs treatment of tests hoc post (extreme-scenario) of interaction. Significancelevels according toTurkey (standard-warming) and Mann-Whitney present. Note that inserted linesnot do indicate linear relationshipshighlight but serve to level the present and the 25°C/parasites absent treatments compared 19°C/parasites absentthe to 19°C/parasites in the individuals of number the in reduction proportional the indicate percentages against 19°C/parasites present and 25°C/parasites absent; see Table for S5 exact 0.001). Note that onlystatistical two contrasts were performed: 19°C/parasites absent treatment (* markers between asterisks by indicated are data) transformed rank- or (raw pairs treatment of t-tests Student’s on based levels significance hence, and data, ○ according totemperature-parasite treatmentsind. (mean mesocosm 5 Figure treatments inserted keys) (see scenario experiment. of Clusters mesocosm units extreme- the (b) and experiment standard-warming the (a) in structure community amphipod Figure 4 species the 25°C/parasites in present treatment compared to the 19°C/parasites absent treatment of number the in reduction proportional the d indicate cand panel in percentages Inserted 1. Figure see b: aand panel in percentages Inserted redundant. were hoc tests post 3) (Table experiment temperature-parasite interaction caseof in the < 0.05, ** : parasites absent; full line and line full absent; : parasites Multidimensionalscaling plots) (MDS visualising treatment-dependent displacement of Extreme-scenario experiment. The post-experimental abundance of amphipod species species amphipod of abundance post-experimental The experiment. Extreme-scenario p

≤ 0.01, *** *** 0.01, n = 7 (extreme-scenario). Dashed line and line Dashed (extreme-scenario). 7 = p

≤ 0.001); and see Table S3 S4for exact ● : parasites present. No two-way ANOVAs were performed on these on these performed were ANOVAs two-way No present. : parasites Shannon-Wiener index from the extreme-scenario the from index Shannon-Wiener are encircled according to temperature-parasite totemperature-parasite according encircled are ○ : : parasites absent; full line and p p -values. Owing to absence of of absence to Owing -values. < 0.05, ** <0.05, ** -1 ± SE ; n = 7).Dashed = line and p

≤ 0.01, *** 0.01, *** p -values. Inserted ● : parasites p

≤

p

Accepted Article This by is protectedarticle reserved. Allrights copyright. by prevalence (%) Figure 6 highlight level the interactionof Appendix for S1 details). that Note inserted lines do not indicate linear relationships but serveto swimming; green: tube-building on vegetation treatment. Colour indicate bars the amphipod affinity microhabitat for species’ free- (blue: statistics: Richness =-0.076Prevalence 7.212; + r subcarinatus species Field relationship between amphipod species richness and arcsine-transformed infection population across 12 bays in Otago Harbour. Trendline and linear regression summary summary regression linear and Trendline Harbour. inOtago bays 12 across population Maritrema

novaezealandensis ; brown: sediment burrowers; see Table 1 and 1 Table see burrowers; sediment ; brown: 2 in the sympatric inthe mud snail =0.741, p < 0.0005. See Table S6 forS6 amphipodTable 0.0005. See < Zeacumantus Accepted Article This by is protectedarticle reserved. Allrights copyright. 1 FIGURE (a) (e) Abundance Abundance (c) Adundance 100 120 140 100 20 40 60 80 20 40 60 80 10 12 14 0 0 0 2 4 6 8 Paracalliope novizealandiae novizealandiae Paracalliope Heterophoxus stephenseni Heterophoxus 93% 59% 18% 7C21°C 17°C 7C21°C 17°C 7C21°C 17°C Temperature Temperature Temperature *** Aora ** ** sp. *** *

(f) (b) Abundance Abundance (d) Abundance 3.5 0.5 1.5 2.5 10 20 30 40 50 60 70 80 10 15 20 25 30 35 0 0 1 2 3 0 5 57% 50% 84% Paramoera chevreuxi Paracorophium lucasi Paracorophium 7C21°C 17°C 7C21°C 17°C 7C21°C 17°C Temperature Temperature Temperature Lembos *** ** sp. *** ** Accepted Article This by is protectedarticle reserved. Allrights copyright. 2 FIGURE Parasite vulnerability (%) 100 20 40 60 80 0 nP sPl Hs L A Pc Pn Species

Accepted Article This by is protectedarticle reserved. Allrights copyright. 3 FIGURE (a) Species (c) Species 1.1 1.2 1.3 1.1 1.2 1.3 1.4 1 1 Shannon-Weiner index Shannon-Weiner Shannon-Weiner index 15% 20% 9C25°C 19°C 7C21°C 17°C Temperature Temperature *** * ***

(d) (b) Species Species 4.5 5.5 6.5 1 2 3 4 5 6 5 6 67% 11% 9C25°C 19°C 7C21°C 17°C ** Species richness Species richness Temperature Temperature *** ***

Accepted Article This by is protectedarticle reserved. Allrights copyright. 4 FIGURE No parasites Parasites Parasites No parasites Parasites Parasites No parasites No No parasites ̶ ̶ ̶ ̶ 21°C 17°C 25°C 19°C ̶ ̶ ̶ ̶ 17°C 19°C 21°C 25°C 2D stress:0.04 2D stress:0.03 (b) (a)

Accepted Article This by is protectedarticle reserved. Allrights copyright. 5 FIGURE (a) (e) Abundance Abundance (d) Adundance 10 20 30 40 50 60 70 80 10 20 30 40 50 60 0 0 1 2 3 4 5 0 28% Paracalliope novizealandiae novizealandiae Paracalliope 42% 82% Heterophoxus stephenseni Heterophoxus 9C25°C 19°C 9C25°C 19°C 9C25°C 19°C *** * Temperature Lembos Temperature Temperature 18% *** * sp. 59% 86% (b) (f) Abundance Abundance (c) Abundance 10 20 30 40 50 60 70 10 15 20 25 30 10 12 0 0 5 0 2 4 6 8 72 73% 69% Paramoera chevreuxi Paracorophium lucasi Paracorophium 9C25°C 19°C 9C25°C 19°C 9C25°C 19°C *** *** * Temperature Temperature Temperature Aora 0.6% * sp. *** 55% 86%

Accepted Article This by is protectedarticle reserved. Allrights copyright. 6 FIGURE Species richness 2 3 4 5 6 7 10203040500 Infection prevalence (%) prevalence Infection