Journal of Sea Research 70 (2012) 32–41

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Journal of Sea Research

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Thermal tolerance and potential impacts of climate change on coastal andestuarine organisms

Diana Madeira a,⁎, Luís Narciso b, Henrique N. Cabral a, Catarina Vinagre a

a Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugalb Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Laboratório Marítimo da Guia, Avenida Nossa Senhora do Cabo, 939, 2750-374 Cascais, Portugal

⁎ Corresponding author. Tel.: +351 21 750 08 26; faE-mail addresses: dianamadeira@netcabo.pt (D. Mad

(L. Narciso), hncabral@fc.ul.pt (H.N. Cabral), cmvinagre

1385-1101/$ – see front matter © 2012 Elsevier B.V. Alldoi:10.1016/j.seares.2012.03.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 8 December 2011Received in revised form 24 February 2012Accepted 3 March 2012Available online 16 March 2012

Keywords:Global ChangeCritical Thermal MaximumTemperate SpeciesTropical SpeciesIntraspecific Variability

The study of thermal tolerance is the first step to understanding species vulnerability to climate warming.This work aimed to determine the upper thermal limits of various fish and crustaceans in a temperateestuarine ecosystem and an adjacent coastal area. Species were ranked in terms of thermal tolerance andintraspecific variability was evaluated. The method used was the Critical Thermal Maximum (CTMax). TheCTMax was found to be higher for species typically found in thermally unstable environments, e.g. intertidal,supratidal, southern distributed species and species that make reproduction migrations because they areexposed to extreme temperatures. Subtidal, demersal and northern distributed species showed lowerCTMax values because they live in colder environments. Species from different taxa living in similar habitatshave similar CTMax values which suggests that they have evolved similar stress response mechanisms. Thisstudy showed that the most vulnerable organisms to sea warming were those that occur in thermallyunstable environments because despite their high CTMax values, they live closer to their thermal limitsand have limited acclimation plasticity. Among the demersal species studied, two sea-breams (Diplodusbellottii and Diplodus vulgaris) are potentially threatened by sea warming because their CTMax values arenot far from the mean water temperature and they are already under thermal stress during current heatwaves.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Temperature is one of the most important factors affectingorganisms because it impacts the kinetic energy of molecules andbiochemical reactions. Hence, the animal's physiology and behavior(e.g. Fry, 1971; Mora and Ospina, 2001; Somero, 1969) might bealtered. Consequently, fitness and performance may be affected bythe thermal regime and other physical and chemical variablesoperating in the habitat. Dynamic fluctuations of these abioticvariables can interfere and dominate the life history, demographicsand competition between species (Christian et al., 1983; Huey,1991; Huey and Berrigan, 2001; Munday et al., 2008; Porter,1989) explaining a diversity of adaptations among organisms(Lutterschmidt and Hutchison, 1997a). Individual parameters suchas growth rate, longevity, excretion rate, food intake and basic metab-olism as well as population parameters such as mortality, reproduc-tive rate, recruitment and population size/distribution all depend ontemperature (e.g. Brey, 1995; Kröncke et al., 1998; Perry et al.,2005; Pörtner et al., 2008; Shaw and Bercaw, 1962; Southward et

x: +351 21 750 02 07.eira), lfnarciso@fc.ul.pt@fc.ul.pt (C. Vinagre).

rights reserved.

al., 1995). Temperature is a heterogeneous variable both in time andspace (Re et al., 2005), structuring marine community assemblagesand ecosystems at the ultimate level (Glynn, 1988).

Aquatic ectotherms do not physiologically regulate their bodytemperature; their body temperature follows the environmentaltemperature. Due to water properties such as high heat conductivity,water absorbs a lot of heat leading to a temperature increase. Consid-ering global warming scenarios, the increase in temperature maymake aquatic ectotherms as vulnerable organisms to thermal stress.Additionally, there is still a considerable lack of knowledge abouttheir thermal limits, especially for temperate species, pelagic andschooling fish and even for some crustacean species that are widelydistributed and easy to handle (Freitas et al., 2010). Therefore, furthertolerance studies are needed. The tolerance window for each speciesis described as a favorable range of temperature or performancebreadth. It includes an optimal zone and a suboptimal zone. Aboveor below that range, performance is negatively affected and thespecies cannot survive unless it is for a limited period of time.Moreover, ectotherms are only able to carry out behavioral thermo-regulation (Neill and Magnuson, 1974; Neill et al., 1972; Rozin andMayer, 1961) which can imply habitat selection based on the habitat'sthermal characteristics. Therefore, according to climate changescenarios, it is reasonable to expect inter and intraspecific competi-tion to occur if the thermal microhabitat is scarce.

33D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

Facing current concerns about climate change scenarios, theknowledge of thermal tolerance is the first step to understandinghow vulnerable species are. However, not only there is a great diver-sity of responses but also global warming tends to vary regionally(Rivadeneira and Fernández, 2005) so there is a need to do regionaland population studies (McFarlane et al., 2000). Most literature hasfocused on tropical regions perhaps not only because models suggestthat impacts will be severe in the tropics (Tewksbury et al., 2008) butalso because predictions for temperate regions are the hardest tomake due to the diversity of life history patterns, complexity of tro-phic relations, habitat variability and over-fishing (IPCC, 1997;Roessig et al., 2004).

Impacts of climate warming should be greatest on thermal special-ists that have limited acclimation potentials (Hoegh-Guldberg et al.,2007) and those that live in aseasonal environments (Tewksbury etal., 2008). The thermal limits of an organism are set genetically but inevolutionary terms the rate at which temperature is increasing mightnot allow the organisms to adapt genetically (Cuculescu et al., 1998).Thereby, the ecosystems that have evolved in stable conditions for along time e.g. cold environments or tropical habitats are especially atrisk. Additionally, some tropical species are said to live close to theirupper thermal limits (Jokiel and Coles, 1977; Sharp et al., 1997)although other authors present contradictory evidence (Mora andOspina, 2001). It has also been suggested that warm-adapted speciesof the intertidal/supratidal zone may be particularly at risk since theylive closer to their upper thermal limit and have limited acclimationcapacity (Hopkin et al., 2006; Somero, 2010). Despite the fact thatthey are more thermally tolerant there is a high probability thatmaximum habitat temperatures surpass their upper thermal limit(Somero, 2010) because they live in a hot and unstable environmentwith wide daily and seasonal thermal amplitudes.

Therefore, environmental variation has large ecological andevolutionary consequences. It exerts a strong selective pressure leadingto the development of specific strategies which may be related notonly to reproductive strategies, growth and maturation but also tophysiological and cellular mechanisms to deal with stressful conditions.Environmental variability also sets life history patterns, influences bio-logical interactions (e.g. Sanford, 1999; Townsend, 1991) and createsgaps for new colonization (Karr and Freemark, 1985; Levin and Paine,1974). In fact, Richter et al. (1997) stated that ‘the full range of naturalintra- and interannual variation of hydrological regimes, and associatedcharacteristics of timing, duration, frequency and rate of change, arecritical in sustaining the full native biodiversity and integrity of aquaticecosystems’. This may apply not only to rivers but also to other aquaticecosystems, in which environmental variation also occurs. Thisis important in the integrity and disturbance of the habitats andcommunities.

Research on the impacts of climate change onmarine fauna shouldfocus on marine coastal waters and estuaries. They are amongst themost productive ecosystems, they are nursery areas and depurationsystems. Furthermore, coastal waters and estuaries are shallowhabitats with little thermal inertia and will, along with inhabitingcommunities, be the first to reflect a rise in atmospheric temperature.Thus, they are indicators of climate change. Applying an integratedand holistic approach to tolerance studies, by considering severaltaxonomic groups and food chain levels may help understand whichcommunity components are more vulnerable to warming.

The aim of this work was to determine the Critical Thermal Maxi-mum (CTMax) of various temperate and subtropical species, fish andcrustaceans that are important in the temperate estuarine/coastalecosystem studied. The approach included species with differentniches and habits, such as intertidal, supratidal, subtidal, demersal,as well as coastal and estuarine enabling the comparison of theCTMax of species inhabiting different environments. Moreover, theaim was to cover the most commercially important and the mostabundant species of the assemblage. The species were then ranked

in terms of temperature tolerance and hypotheses about the potentialimpacts of climate warming on the species studied were put forward.Another target of this work was to evaluate and compare intraspecificvariability of the CTMax in order to discuss the species' potential toadapt to ongoing global climate changes. Also, it was investigatedwhich species live closer to their upper thermal limits and com-parisons with tropical species were made.

2. Materials and methods

2.1. Temperature data

2.1.1. Atmospheric and water temperature for the intertidal zoneAtmospheric temperature data for the intertidal zone was obtained

from theMOHID database (open acess at www.mohid.com). In this da-tabase, field data from the meteorological station of LaboratórioMarítimo da Guia (38°41′42.91″ N; 9°27′08.52″ W — under 3400mfrom the sampling site) was available. Temperature was recordedevery half an hour during the day and night. For the purpose of thisstudy data from January 2010 to December 2010 were used. A detailedgraph was drawn for July 2010, concerning only temperatures between7 am (sunrise) and 9 pm (sunset).

2.1.2. Estuarine temperaturesEstuarine water temperatures were obtained from the Centro de

Oceanografia database. Mean values from 1978, 1979, 1980, 1995,1996, 1997, 2001, 2002, 2005 and 2006 were used to calculate andplot the general mean±SD temperature for each month in theTagus estuary.

2.1.3. Coastal temperaturesCoastal water temperatures were obtained from the Centro de

Oceanografia database, Levitus and Boyer (1994) and Mohid database.Thermal images of the Portuguese coast from the Mohid database wereobtained every 10 days throughout 2010.

2.2. Study area and sampling method

This study was carried out in the Tagus estuary and along the coast(from Vila Franca de Xira to Cascais), at an approximate latitude of38°N (Northeast Atlantic). This estuary is located on the midwestcoast of Portugal, and has an area of 320 km2, a length of 34 km anda maximum width of 15 km. During July, the Tagus estuary and theintertidal pools of the adjacent coast have a mean surface tempera-ture of 24 °C (Centro de Oceanografia database).

This research focused not only on marine and estuarine species ofcommercial importance but also on species that play an importantrole in the food web. The fish species studied were Diplodus bellottii(Steindachner 1882), Diplodus vulgaris (Geoffroy St. Hilaire 1817),Diplodus sargus (Linnaeus 1758), Pegusa lascaris (Risso 1810),Dicentrarchus labrax (Linnaeus 1758), Gobius cobitis (Pallas 1814),Lipophrys trigloides (Valenciennes 1836), Gobius niger (Linnaeus1758) and Liza ramada (Risso 1827). The crustacean species studiedcan be divided in two groups: the crabs Liocarcinus marmoreus (Leach1814), Lophozozymus incisus (Milne-Edwards 1834), Carcinus maenas(Linnaeus 1758), Pachygrapsus marmoratus (Fabricius 1787) and theshrimps Palaemon longirostris (Milne-Edwards 1837), Palaemon elegans(Rathke 1837) and Crangon crangon (Linnaeus 1758). Most of thesespecies have a distributional range from Northern Europe to NorthAfrica, occurring in both cold and moderately warmwaters. The excep-tions are Crangon crangon, Palaemon longirostris and Liocarcinusmarmoreus which occur mainly in cold waters in northern temperateregions (Froese and Pauly, 2011; Palomares and Pauly, 2011). Samplesizes, total lengths, environment and sampling area for each speciesare shown in Table 1. Sample sizes were similar to Mora and Ospina

Table 1a

Sample size, mean total length, environment and sampling area for each species in the present study.

Species Sample size Total length (mm)Mean±SD

Environment Habitat Depth (m); Mostcommon depth (m)

Distribution Samplingarea

Dicentrarchus labrax 7 86.00±6.19 Demersal Estuary, coast,river mouths

10–100 Temperate/subtropical Estuary

Diplodus bellottii 17 103.71±8.91 Benthopelagic/demersal Estuary, coast,upwelling

0–100; 30–50 Temperate/subtropical Estuary

Diplodus sargus 28 33.89±9.07 Demersal Estuary, coast 0–50 Temperate/subtropical EstuaryDiplodus vulgaris 13 74.62±7.76 Benthopelagic/demersal Estuary, coast 0–90; 0–30 Temperate/subtropical EstuaryLipophrys trigloides 9 67.33±28.26 Intertidal Coast 0–1 Temperate/subtropical CoastGobius cobitis 4 46.00±29.41 Intertidal Coast 0–10 Temperate/subtropical CoastGobius niger 9 98.70±6.36 Subtidal/intertidal Estuary, lagoons,

inshore waters1–75; 1–50 Temperate/subtropical Estuary

Liza ramada 6 44.00±3.90 Pelagic/demersal Estuary, coast,rivers

0–? Temperate/subtropical Estuary

Pegusa lascaris 8 184.38±39.70 Demersal Estuary, coast 50–350; 20–50 Temperate/subtropical EstuaryCarcinus maenas 25 28.65±5.80 Intertidal Estuary, coast 0-200; 0-60 Temperate/subtropical EstuaryLiocarcinus marmoreus 17 22.35±2.74 Subtidal/demersal Estuary, coast 0–200 Temperate/polar EstuaryPachygrapsus marmoratus 26 17.32±6.24 Supratidal Estuary, coast −1.5–2 Temperate/subtropical CoastLophozozymus incisus 16 34.38±6.09 Subtidal Estuary, coast 0–40 Temperate; Northeast Atlantic EstuaryCrangon crangon 16 36.50±4.84 Demersal Estuary, coast 0–50 Temperate; Northeast Atlantic EstuaryPalaemon elegans 25 32.52±7.34 Intertidal Coast 0–30; 0.5–10 Temperate/subtropical CoastPalaemon longirostris 14 43.79±8.94 Subtidal Estuary, rivers 0–40; 0–10 Temperate;Eastern Atlantic Estuary

aThis table was constructed based on the references Alvarez (1968), Bauchot and Hureau (1986), Quéro et al. (1986), Tortonese (1986), Boddeke (1989), Sauriau et al. (1994),Barnes (1994), Hayward and Ryland (1995), Hayward et al. (1996), Ingle (1997), Cannicci et al. (1999), Flores and Paula (2001), La Mesa et al. (2004), Łapińska and Szaniawska(2006), Bilgin et al. (2008), Vinagre et al. (2008, 2009, 2010), FAO (2011).

34 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

(2001) for comparable analysis. The species were caught during July of2010 using hand nets, dip nets, beam trawl and beach seine.

2.3. Thermal tolerance method

The thermal tolerance of these species was determined by thedynamic method described in Mora and Ospina (2001). The aim wasto determine the Critical Thermal Maximum (CTMax), which is definedas the “arithmetic mean of the collective thermal points at which theend-point is reached” (Mora and Ospina, 2001). The end-point wasloss of equilibrium.

After having been captured, organisms were transported to the lab-oratory and were placed in a re-circulating system with aquaria with acapacity of 70 L with aerated sea water, a constant temperature of24 °C and salinity 35‰. The water dissolved O2 level varied between95% and 100%. The organisms were acclimated for 2 weeks, being fedad libitum twice a day. They were starved for 24 h before theexperiments. To determine the CTMax, the organisms were placed ina thermostatized bath. During the trial, animals were exposed to a con-stant rate of water-temperature increase of 1 °C.h−1, and observedcontinuously, until they reached the end-point. The temperature atwhich each animal reached its end-point was measured with a digitalthermometer, recorded and then the CTMax and its standard deviationwere calculated for each species. All experiments were carried out inshaded day light (15L;09D). To prevent any additional handling stress,the total length of all individuals was measured at the end of each trialusing a slide caliper ruler.

All known environmental variables that might have influencedthe results (e.g. oxygen levels, salinity, food, pH, photoperiod,acclimation temperature) were monitored during the acclimationand trials, thus it is believed that the observed results are due totemperature.

2.4. Data analysis

The upper thermal limits for each species were calculated usingthe equation:

CTMspecies ¼ ∑ Tend−pointn

� �=n

Where Tend-point is the temperature at which the end-point wasreached for individual 1, individual 2, individual n, divided by the nindividuals that were in the sample.

To determine intraspecific variability of the CTMax, the coefficientof variation (in percentage) was calculated for each species:

SD=Meanð Þ � 100:

In order to evaluate which species live closer to their upperthermal limits, the difference between CTMax and mean surfacewater temperature (24 °C) was calculated for each species (fish andcrustacean). Using the work of Mora and Ospina (2001), the samedifference was calculated for tropical species living with a meansurface temperature of 27 °C. Then, the results for temperate/subtropical and tropical fish were compared through a Student'st-test, since the data showed normal distribution (Shapiro Wilk'stest) and homoscedasticity (Levene's test). A significant level of 0.05was considered in all test procedures. Additionally, the differencebetween CTMax and Maximum Habitat Temperature (MHT) wascalculated for intertidal fish species from temperate/subtropical andtropical regions (Mora and Ospina, 2001). The crustaceans were notincluded in the analysis because comparable data was only availablefor fish. MHT was considered to be 35 °C according to the meanmaximum air temperatures for the hottest days of July 2010 (4th,5th, 25th, 26th).

3. Results

3.1. Temperature data

3.1.1. Atmospheric and water temperature for the intertidal zoneTemperature results showed that the intertidal zone was highly

variable, with steep seasonal and daily variations in temperature(Fig. 1a). In winter, temperature can drop to approximately 5 °C,mainly during the night, and can go up to 10–15 °C during the day.Around springtime temperatures begin to rise, reaching >35 °Cduring the hottest summer days. Minimum temperatures during thesummer were around 17–19 °C.

During July (2010), the sampling month, the minimum tempera-ture registered during daylight was 17.2 °C and the maximum was

a)

b)

Days

Tem

per

atu

re o

C

1 5 9 13 17 21 25 2915

20

25

30

35Tmax

Tmin

Tmean

July 2010

Fig. 1. Atmospheric temperature data for the intertidal zone a) from January to December 2010 and b) in July 2010.

35D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

36.6 °C (Fig. 1b). Mean daily temperatures ranged from 19.6 °C on the31st to 31.8 °C on the 5th.

3.1.2. Estuarine temperaturesThe mean estuarine water temperature was lowest in January,

with a mean of 12 °C and it was highest in July, with a mean of24 °C (Fig. 2).

3.1.3. Coastal temperaturesWater temperatures in the coastal area were usually in the range

of 15 °C to 18 °C during the summer season and 10–16 °C during

Fig. 2. Estuarine temperatures (mean±SD) for each month based on data from 1978,1979, 1980, 1995, 1996, 1997, 2001, 2002, 2005 and 2006.

winter. However, in July 2010 (sampling period) water temperaturesreached up to 20 °C–23 °C.

3.2. Interspecific differences depending on habitat (intertidal, subtidal,demersal)

Species from intertidal/supratidal zones showed higher CTMaxvalues (e.g. Pachygrapsus marmoratus, Carcinus maenas, Gobius niger,Palaemon elegans, Lipophrys trigloides, Gobius cobitis) (Fig. 1). Subtidaland demersal species showed lower CTMax values (e.g. Diplodusspecies, Liocarcinus marmoreus, Solea lascaris, Dicentrarchux labrax,Lophozozymus incisus, Crangon crangon) (Fig. 1). The exceptionswere migratory species Liza ramada and Palaemon longirostris(Barnes, 1994; Cartaxana, 1994; Paula, 1998; Sauriau et al., 1994)(Fig. 1).

3.3. Interspecific differences depending on geographic distribution

Species from Northern/Eastern Atlantic and originally fromupwelling systems showed lower CTMax values (e.g. Diplodusbellottii, Liocarcinus marmoreus, Lophozozymus incisus, Crangoncrangon). Species with more southern and wide distributions showedhigher CTMax values.

3.4. Differences between taxonomic groups

The CTMax values obtained for all species ranged from 27.4 °C forD. bellotti to 38.0 °C for L. ramada (Fig. 1). Among crabs, the lowestCTMax value was observed in L. marmoreus (32.2 °C), followed by L.

Table 3Differences between CTMax (Critical Thermal Maximum) andmean surface water tem-perature for temperate/subtropical and tropical fish species. First of all, the differenceswere calculated for all the species included in this work and in Mora and Ospina(2001). Following, differences were tested dividing the fish in two groups: demersaland intertidal. Significant differences (p-valueb0.03) are presented in bold.

Mean difference (°C) Mean difference (°C) Mean difference (°C)

All species Demersal species Intertidal species

Temperate/subtropical

9.16 9.84 9.95

Tropical 9.73 9.17 12.00

36 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

incisus and C. maenas. Finally, the highest CTMax observed in crabswas for P. marmoratus (35.7 °C). Among shrimps, C. crangon had thelowest CTMax (33.8 °C) and Palaemon longirostris had the highest(34.4 °C). Among fish, the lowest CTMax values were observed fortwo Diplodus species (D. bellottii and D. vulgaris) and the highestCTMax values, besides L. ramada, were observed for G. niger(34.1 °C) and B. trigloides (34.0 °C). Additionally, Diplodus sargusshowed a higher CTMax when compared to other Diplodus species.The CTMax was the most variable between fish species (10.6 °C), fol-lowed by crabs (3.5 °C) and the least variable between shrimp species(0.7 °C).

3.5. Intraspecific differences

Intraspecific variability, given by %CV, was generally low. The spe-cies with the lowest %CV were S. lascaris and L. ramada. The specieswith the highest variability were D. labrax, D.vulgaris and D. bellottii(Table 2).

3.6. Climate change: temperate versus tropical species

The species living closer to its thermal limits was D. bellottiiwith adifference of only 3.4 °C between the summer mean surface watertemperature and its CTMax. Next comes D. vulgaris with a differenceof 7.1 °C. The species living the farthest from its thermal limits wasL. ramada with a difference of 14.0 °C between summer mean watertemperature and its CTMax. In between these values were the demer-sal and intertidal/supratidal species, with approximately 8 to 10 °Cand 9 to 11 °C of a difference between the mean water temperatureand the CTMax (Fig. 1).

After analyzing the differences between the CTMax and the meansurface temperature for temperate/subtropical and tropical fish spe-cies (Table 3), no significant differences were found (p-value>0.53).However, when differences were analyzed by dividing the fish intwo groups (demersal and intertidal) significant differences werefound for intertidal species (p-valueb0.03), but not for demersalones (p-value>0.71).

Maximum Habitat Temperature (MHT) can reach up to a mean of35 °C in the study area (Portugal's Meteorological Institute databaseand open access Mohid database — www.mohid.com) so organismsin the intertidal area can be subjected to very high temperatures.For tropical areas, the MHT was 36 °C for tidal pools (Mora andOspina, 2001). The results show that the CTMax of tropical intertidalspecies was 2 to 5 °C higher than the MHT while the CTMax of

Table 2CTMax (Critical Thermal Maximum) intraspecific variability given bythe coefficient of variation (in percentage).

%CV Species

0 Pegusa lascarisLiza ramada

1≤%CV≤2 Liocarcinus marmoreusCrangon crangonGobius cobitisDiplodus sargusLipophrys trigloides

2b%CV≤3 Carcinus maenasPachygrapsus marmoratus

3b%CV≤4 Lophozozymus incisusPalaemon elegansGobius nigerPalaemon longirostris

4b%CV≤5 Diplodus bellottiiDiplodus vulgaris

>5 Dicentrarchus labrax

temperate/subtropical species was 1 to 2 °C lower than the MHT inthe present study (Table 4).

4. Discussion

4.1. Temperature data

As expected, the most variable environment studied was the inter-tidal zone with steep variations in temperature, both daily andseasonally. Changes are in the order of >20 °C seasonally and 15 °Cdaily. The estuary studied is also a relatively variable environmentwith a difference of 12 °C between the coldest and the hottest months(January and July). However, comparing it to the intertidal zone, it is aless variable environment. Coastal environments are the leastvariable out of the habitats studied. Nevertheless they also showedseasonal variations of 5 °C. Therefore, the results showed that thermalstress is higher in the intertidal zone, followed by in the Tagus estuaryand lastly in the coastal subtidal zone. In this habitat, temperaturesare lower and less variable, and thus it is a more stable habitat forthe species.

4.2. Interspecific differences depending on habitat (intertidal, subtidal,demersal)

Results showed that intertidal species had the highest CTMaxvalue (Fig. 3, Table 5). This habitat is an extremely variable one atseveral levels such as temperature, salinity and dissolved oxygen.Our results and Tomanek's (2010), show that intertidal areas canexperience changes of >20 °C. The abiotic factors are crucial andpartially responsible for littoral zonation of the organisms living inthat habitat, depending on how adapted they are to water loss andheat. Species inhabiting such an environment, especially the residentones, have evolved specific adaptations that allow them to cope withenvironmental stress due to exposure to terrestrial conditions(Stillman, 2002). These adaptations lead to a higher CTMax hencethe reason why organisms living in variable environments havehigher tolerances (e.g. Badillo et al., 2002; Mora and Ospina, 2001;Shaefer and Ryan, 2006) than those living in more stable environ-ments, e.g. the subtidal zone. Additionally, species that also explorethe supratidal zone (e.g. Pachygrapsus marmoratus) showed an even

Table 4Differences between CTMax (Critical Thermal Maximum) and MHT (Maximum HabitatTemperature) for temperate/subtropical and tropical intertidal fish. The difference wascalculated for each species and then a mean difference and SD was calculated for eachlatitudinal group. CTMaxs of tropical fish used in these calculations were obtained fromMora and Ospina (2001).

Temperate/subtropical Tropical

Gobiuscobitis

Gobiusniger

Lipophrystrigloides

Malacoctenuszonifer

Bathygobiusramosus

Mugilcurema

CTM-MHT (°C) −1.25 −0.90 −1.00 2.1 3.5 4.8Mean±SD (°C) −1.05±0.18 3.46±1.35

Tem

per

atu

re o

C

Gobius c

obitis

Lipophry

s trig

loid

es

Palaem

on eleg

ans

Carcin

us mae

nas

Pachyg

rapsu

s mar

mora

tus

Gobius n

iger

Lophozozy

mus i

ncisus

Palaem

on longiro

stris

Lioca

rcin

us mar

more

us

Diplo

dus bell

ottii

Diplo

dus vulg

aris

Pegusa

lasc

aris

Dicentra

rchus l

abra

x

Crangon cr

angon

Diplo

dus sar

gus

Liza ra

mad

a20

22

24

26

28

30

32

34

36

38

40Intertidal

Subtidal

Demersal

M

M

Fig. 3. Critical Thermal Maxima (“arithmetic mean of the collective thermal points at which the end-point is reached”Mora and Ospina, 2001) of nine fish species, four crab speciesand three shrimp species from the Tagus estuary and adjacent marine coastal waters. Straight line represents the mean water temperature during the summer (24 °C) for the studyarea (estuary and coastal intertidal pools) and the dotted line represents the temperature during heat waves in estuary and coastal intertidal pools (28 °C). The dashed line repre-sents the maximum temperature for intertidal zone (35 °C). Dot icons are used for fish, triangle icons are used for crabs and square icons are used for shrimps. Migratory species aretagged with M.

37D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

greater CTMax as they are exposed to terrestrial conditions most ofthe time. Our results, along with other studies (e.g. Davenport andDavenport, 2005; Davenport and McAlister, 1996) follow the ideathat organisms living in higher shore are more tolerant than thosein the lower shore. Other authors, however, did not find such aconnection (e.g. Clarke et al., 2000).

Subtidal and demersal species had lower CTMax values (Fig. 3,Table 5). These species live in relatively variable or more stablehabitats (e.g. estuaries, coastal waters, coastal upwelling, deepwaters) so they are exposed to lower temperatures, having physiolog-ical set-points lower in the temperature gradient. The exceptions tothis pattern were migratory species (Palaemon longirostris and Lizaramada). These species have to pass through several habitat typesand thermal regimes to be able to reproduce and keep the populationnumbers up, so higher tolerances were expected for these species.

4.3. Interspecific differences depending on geographic distribution

Species which have a distributional range in the Northern/EasternAtlantic or live in upwelling systems are characteristically from colderwaters (e.g. Diplodus bellottii, Liocarcinus marmoreus, Lophozozymusincisus, Crangon crangon). Therefore, they showed lower CTMaxvalues when compared to species with wider and more southerndistributional ranges. A wide distributional area means that speciesneed to function over a wide range of temperatures, so their physiol-ogy allows them to withstand very different temperatures by havingmore extreme thermal limits. In order to address local adaptation/acclimation of CTMax in wide distributed species we compared ourresults for Carcinus maenas with the results obtained by Ahsanullahand Newell (1971) and Cuculescu et al. (1998) for the same species.The analysis showed that the CTMax was very similar for northernand southern crabs (around 35 °C). Some authors report thatorganisms suffer local adaptation or acclimation to the temperature

range on a regional scale, so crabs from the North Sea would beexpected to have lower CTMax values than their conspecifics livingmore to the south (e.g. Beitinger et al., 2000; Eme and Bennett,2009; Freitas et al., 2010; Lutterschmidt and Hutchison, 1997a;Mora and Ospina, 2001; Re et al., 2005; Shaefer and Ryan, 2006).However, this was not the case. Results suggest that this speciesdoes not adapt or acclimate locally, which is in agreement withTomanek (2005) and Tomanek and Somero (1999, 2002).

Among species with a temperate/subtropical distribution, resultsshowed that species with a wide continuous distribution (e.g.Diplodus sargus) had higher CTMax values than species with a widebut discontinuous distribution (e.g. Diplodus vulgaris). A continuousdistribution means that species can also occur in tropical areaswhile a discontinuous distribution means that they are absent fromthe warmer zones. Thus, if discontinuous species are absent fromthe warmer areas, they are not capable of withstanding very hightemperatures. Hence, they showed lower CTMax values.

4.4. Differences between taxonomic groups

The analysis of CTMax values over several taxonomic groupsshowed that species from different taxa living in identical habitattypes had similar upper thermal limits (Fig. 1). As they have evolvedin similar abiotic conditions, they have probably developed identicalphysiological and cellular adaptations. At first, we expected a greaterdiscrepancy as the mean genetic distance increased but this wouldonly occur if ecological niches were very dissimilar. This was not thecase because we analyzed fish, crabs and shrimps from every typeof habitat. Thus, the observed differences are mainly due to habitattype, distributional depth and geographic distribution. Nevertheless,each species has its own genetic traits and set-points for physiologicalperformance (see Dent and Lutterschmidt, 2003) which may also setthermal limits.

Table 5Main findings of the present study.

Results Rationale

4.2 Interspecific differences depending onhabitat (intertidal, subtidal, demersal)

Higher CTMax in intertidal/supratidal species Highly variable environment, extreme temperature valuesHigher CTMax in migratory species They have to pass through several thermal regimes in order

to reproduceLower CTMax in subtidal/demersal species More stable habitats with lower temperatures

4.3 Interspecific differences dependingon geographic distribution

Lower CTMax in Northern/Eastern Atlantic species Colder watersLower CTMax in species from upwelling areas Colder watersHigher CTMax in species with southern distribution Warmer watersHigher CTMax in eurythermal species They have to perform across a broad range of temperatureHigher CTMax in species with a wide continuous distribution They can occur in warmer stretches of the globeLower CTMax in species with a wide discontinuous distribution They are absent from the warmer stretches of the globe

4.4 Differences between taxonomicgroups

Species from different taxa living in similar habitats havesimilar CTMax

They evolved in similar abiotic conditions so they probablydeveloped identical physiological and cellular adaptations

CTMax was more variable between fish than between crabsand shrimps

Fish have a great locomotory capacity and colonize all kindsof habitats

4.5 Intraspecific differences Generally low intraspecific variability Specific genetic features and the previous influence ofenvironmental variables

D. labrax, D. bellotti and D. vulgaris appear to have the highestvariability

They possibly have the highest genetic variability concerningthe genes involved in the stress response

4.6 Climate change: temperateversus tropical species

D. bellotii and D. vulgaris might be threatened by sea warming Their CTMaxs are really close to mean water temperature (24°)and they are already in stress during heat waves (28°) or will bestressed in a climate change scenario of a plus 2 °C increase inwater temperature (24+2=26 °C; 28+2=30 °C)

Intertidal temperate/subtropical fish have an upper thermallimit on average 9.95 °C above mean water temperature (24°)Tropical intertidal fish have an upper thermal limit on average12 °C above mean water temperature (27 °C).Temperate/subtropical fish have CTMaxs on average 1.05 °Cunder the maximum habitat temperature

May rely on a strategy of escaping extreme conditions throughbehavioral thermoregulation

Tropical species have CTMaxs on average 3.46 °C abovemaximum habitat temperaturesHigher vulnerability of intertidal/supratidal organisms towardsclimate change

CTMax is high but they live closer to their thermal limits.Maximum Habitat Temperatures may reach or exceed theirCTMax

Eurythermal species may be vulnerable even though theyperform in a wide range of temperatures

Eurythermal species show limited acclimatory plasticity whencompared to stenothermal ones

38 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

In addition, the CTMax was more variable between fish than be-tween crabs and shrimps. This is probably because fish have a greatlocomotory capacity and colonize all kinds of habitats. Therefore, ifthe CTMax and optimal temperatures are co-adapted (Huey andKingsolver, 1993), the diversity of habitats (i.e. thermal regimes)accounts for the variation in CTMax.

4.5. Intraspecific differences

Intraspecific variability was generally low, which is in concor-dance with Mora and Ospina (2001). According to Cuculescu et al.(1998), thermal tolerance is subjected to phenotypic alterationwithin a genetically fixed range. This phenotypic plasticity is depen-dent upon several factors but thermal history of individuals andparental effects (e.g. epigenetic changes) seem to be the mostimportant ones (Cossins and Bowler, 1987; Shaefer and Ryan, 2006).These factors induce irreversible changes to thermal tolerance(Shaefer and Ryan, 2006). Then, variability found for each speciesrelates not only to specific genetic features but also to the previousinfluence of environmental variables. Although genetic variability islow in general, this does not mean that organisms will not be able toadapt to further warming due to climate change. If thermal history in-fluences CTMax then it is possible that in each generation phenotypeswith higher CTMax values are being produced due to sea warming.Nevertheless, there are no certainties yet so further research is neededon the capacity to adapt. Our data shows that D. labrax, D. bellotti and D.vulgaris appear to have the highest variability in the response to tem-perature and thus possibly have the highest genetic variability in thegenes involved in such a response.

There are various untested factors that can potentially influence thespecies' upper thermal limits. These factors can be sex, reproductive

state, nutritional condition, diseases and parasites, inter-populationvariability, age/size (Becker and Genoway, 1979; Copeland et al.,1974; Cox, 1974; Hutchison, 1976; Lutterschmidt and Hutchison,1997b) and seasonal variation (Cuculescu et al., 1998; Hopkin et al.,2006). Yet, there seems to be a certain degree of controversy on theinfluence of these factors as some authors found significant differencesfor instance between different sized individuals (e.g. Copeland et al.,1974; Cox, 1974; Peck et al., 2004, 2007, 2009) while others did not(e.g. Ospina and Mora, 2004), nor for males versus females (Badilloet al., 2002). Even though we limited the influence of some of thesefactors by, for example, restricting sampling to July and testing individ-uals of approximately the same size, this might have the disadvantageof missing important intraspecific variability patterns. Further studiesshould address this issue and the CTMax should be tested at differentlife stages, for different sexes, different seasons and different habitatsused by conspecifics.

4.6. Climate change: temperate versus tropical species

In order to know which species might be more vulnerable to tem-perature and further sea warming, we calculated the differencebetween thermal limit and mean water temperature for each species.Mora and Ospina (2001) conducted a similar study on tropical reeffish and concluded that the CTMax of the least tolerant species was8 °C above the current mean sea temperature, while in the presentstudy the CTMax of the least tolerant species, D. bellottii, is only 3 °Cabove the average summer estuarine temperature (it is in summerthat this species' juveniles occur in estuaries). In fact, this species isalready under stress during current heat waves because the watertemperature can reach 28 °C, and last for more than 2 weeks.D. bellottii's CTMax is 27.4 °C, which is very close to 28 °C. Thus, its

39D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

presence in estuarine nursery areas (where juveniles are veryabundant nowadays) is possibly threatened by climate warming, asobserved by Vinagre et al. (in press) during experimental studies. In aclimate warming scenario, if we add 2 °C (Miranda et al., 2002) to thecurrent temperature attained by the waters during heat waves (28 °C+2 °C), it is clear that another seabream, D. vulgaris (CTMax 31.1 °C),may also face thermal stress.

After comparing mean differences between CTMax and meanwater temperature for temperate/subtropical and tropical fish, no sig-nificant differences were found considering all species. When weevaluated demersal and intertidal species separately, demersal onesdid not show significant differences either, but intertidal speciesdid. The intertidal temperate/subtropical fish had an upper thermallimit on average 9.95 °C above mean water temperature (24 °C)while tropical intertidal fish had an upper thermal limit on average12 °C above mean water temperature (27 °C). This suggests thattemperate/subtropical intertidal species might be more vulnerableto further increases in temperature.

In addition, we calculated the difference between CTMax andMaximum Habitat Temperature (MHT) for temperate/subtropical andtropical intertidal fish. Results showed that temperate/subtropical fishhave CTMax values on average 1.05 °C under the maximum habitattemperature while tropical species have CTMax values on average3.46 °C above maximum habitat temperatures. Therefore, maximumhabitat temperatures in temperate/subtropical regions may exceedthe upper thermal limits of intertidal fish species, making them espe-cially vulnerable to high temperatures and climate warming. However,further studies should focus on obtaining more comparable data inorder to reveal patterns in temperate and tropical organisms.

In general, results show that although organisms that occur inthermally unstable environments, e.g. intertidal/supratidal habitats,have higher CTMax values, they live closer to their thermal limits.This occurs because maximum habitat temperatures may reach orexceed their CTMax. Subtidal species are in less danger since theyrarely encounter temperatures near their CTMax. These results arein accordance with Somero, 2010.

In temperate regions, the variability in environmental factors ismuch greater than in tropical areas, which maintain similar valuesall year long. In temperate regions, temperature can reach reallyextreme values in the hottest years (e.g. 2010) and these valuesexert the most selective pressures (Lutterschmidt and Hutchison,1997a). So, intertidal/supratidal organisms may be exposed to thestrongest selection. As they already live close to their thermal limits,any further increase in temperature is probably going to push thembeyond those limits (Tomanek, 2010). In this study some intertidalspecies had a CTMax lower or really close to MHT (e.g. Gobius cobitis,Lipophrys trigloides, Palaemon elegans, Carcinus maenas). Althoughthis might be worrying, these species can perform behavioralthermoregulation and take refuge in colder spots. It is only if theycannot escape extreme conditions that the population might bejeopardized. The final CTMax value for each species is a mean, and ifwe analyze individual limits for instance in C. maenas, we see thatthere are individuals loosing righting response at 34 °C and othersloosing it at 37 °C. Thus, facing increasing temperatures, less resistantindividuals which cannot adapt will be wiped out while more resis-tant ones will be selected. Nevertheless, in the sampling area, themaximum temperature registered in the last 8 years was 37.7 °C(Mohid database — open acess at www.mohid.com), which is stillhigher than the limits for the most resistant individuals. In addition,species from highly variable environments have limited acclimationplasticity (Somero, 2010; Tomanek, 2010). Eurythermal species alsoshow limited acclimation plasticity when compared to their steno-thermal congeners (Tomanek, 2005; Tomanek and Somero, 1999,2002). Besides, the range of temperatures over which acclimationchanges occur appears to be narrower than the range of habitat tem-peratures (see Dahlhoff and Somero, 1993; Tomanek and Somero,

1999). Thus, intertidal/supratidal and eurythermal organisms maybe more vulnerable to further temperature increases, and have torely on behavioral thermoregulation to survive these extremeconditions.

4.7. Conclusions

Predicting the impacts of climate change on particular species is nota simple task and requires in depth knowledge on several subjects frommolecular biology, physiology, ecology and evolution. Thus, realisticpredictions will essentially be the result of multidisciplinary andintegrative approaches. Since sea warming effects are already clearthroughout ecosystems and base studies are urgently needed, the find-ings of the present study (summarized in Table 5) are considered anecessary first step in the investigation of climate change impactsupon marine biota and ecosystems.

Role of the funding source

This study was entirely supported by ‘Centro de Oceanografia,Faculdade de Ciências, Universidade de Lisboa’. Study design,collection, analysis and interpretation of data, report writing, and thedecision to submit the article for publication were carried out solelyby the authors and not by the sponsor.

Acknowledgments

Authors would like to thank everyone involved in the field work,maintenance of the experimental tanks and in the feeding of theorganisms. Authors would like to express their gratitude to “AquárioVasco da Gama” for the collaboration in the sampling andmaintenance of organisms, in particular to Dr Fátima Gil. Authorswould like to thank Zara Reveley for the English revision. This studyhad the support of the Portuguese Fundação para a Ciência e aTecnologia (FCT) through the grant SFRH/BPD/34934/2007 awardedto C. Vinagre and the funding of projects.

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