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 and estuarine 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, Portugal b Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Laboratório Marítimo da Guia, Avenida Nossa Senhora do Cabo, 939, 2750-374 Cascais, Portugal article info abstract

Article history: The study of thermal tolerance is the first step to understanding species vulnerability to climate warming. Received 8 December 2011 This work aimed to determine the upper thermal limits of various fish and crustaceans in a temperate Received in revised form 24 February 2012 estuarine ecosystem and an adjacent coastal area. Species were ranked in terms of thermal tolerance and Accepted 3 March 2012 intraspecific variability was evaluated. The method used was the Critical Thermal Maximum (CTMax). The Available online 16 March 2012 CTMax 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 are Keywords: Global Change exposed to extreme temperatures. Subtidal, demersal and northern distributed species showed lower Critical Thermal Maximum CTMax values because they live in colder environments. Species from different taxa living in similar habitats Temperate Species have similar CTMax values which suggests that they have evolved similar stress response mechanisms. This Tropical Species study showed that the most vulnerable organisms to sea warming were those that occur in thermally Intraspecific Variability unstable environments because despite their high CTMax values, they live closer to their thermal limits and have limited acclimation plasticity. Among the demersal species studied, two sea-breams (Diplodus bellottii and Diplodus vulgaris) are potentially threatened by sea warming because their CTMax values are not far from the mean water temperature and they are already under thermal stress during current heat waves. © 2012 Elsevier B.V. All rights reserved.

1. Introduction al., 1995). Temperature is a heterogeneous variable both in time and space (Re et al., 2005), structuring marine community assemblages Temperature is one of the most important factors affecting and ecosystems at the ultimate level (Glynn, 1988). organisms because it impacts the kinetic energy of molecules and Aquatic ectotherms do not physiologically regulate their body biochemical reactions. Hence, the animal's physiology and behavior temperature; their body temperature follows the environmental (e.g. Fry, 1971; Mora and Ospina, 2001; Somero, 1969) might be temperature. Due to water properties such as high heat conductivity, altered. Consequently, fitness and performance may be affected by water absorbs a lot of heat leading to a temperature increase. Consid- the thermal regime and other physical and chemical variables ering global warming scenarios, the increase in temperature may operating in the habitat. Dynamic fluctuations of these abiotic make aquatic ectotherms as vulnerable organisms to thermal stress. variables can interfere and dominate the life history, demographics Additionally, there is still a considerable lack of knowledge about and competition between species (Christian et al., 1983; Huey, their thermal limits, especially for temperate species, pelagic and 1991; Huey and Berrigan, 2001; Munday et al., 2008; Porter, schooling fish and even for some crustacean species that are widely 1989) explaining a diversity of adaptations among organisms distributed and easy to handle (Freitas et al., 2010). Therefore, further (Lutterschmidt and Hutchison, 1997a). Individual parameters such tolerance studies are needed. The tolerance window for each species as growth rate, longevity, excretion rate, food intake and basic metab- is described as a favorable range of temperature or performance olism as well as population parameters such as mortality, reproduc- breadth. It includes an optimal zone and a suboptimal zone. Above tive rate, recruitment and population size/distribution all depend on or below that range, performance is negatively affected and the temperature (e.g. Brey, 1995; Kröncke et al., 1998; Perry et al., species cannot survive unless it is for a limited period of time. 2005; Pörtner et al., 2008; Shaw and Bercaw, 1962; Southward et Moreover, ectotherms are only able to carry out behavioral thermo- regulation (Neill and Magnuson, 1974; Neill et al., 1972; Rozin and Mayer, 1961) which can imply habitat selection based on the habitat's thermal characteristics. Therefore, according to climate change ⁎ Corresponding author. Tel.: +351 21 750 08 26; fax: +351 21 750 02 07. fi E-mail addresses: [email protected] (D. Madeira), [email protected] scenarios, it is reasonable to expect inter and intraspeci c competi- (L. Narciso), [email protected] (H.N. Cabral), [email protected] (C. Vinagre). tion to occur if the thermal microhabitat is scarce.

1385-1101/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2012.03.002 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41 33

Facing current concerns about climate change scenarios, the in terms of temperature tolerance and hypotheses about the potential knowledge of thermal tolerance is the first step to understanding impacts of climate warming on the species studied were put forward. how vulnerable species are. However, not only there is a great diver- Another target of this work was to evaluate and compare intraspecific sity of responses but also global warming tends to vary regionally variability of the CTMax in order to discuss the species' potential to (Rivadeneira and Fernández, 2005) so there is a need to do regional adapt to ongoing global climate changes. Also, it was investigated and population studies (McFarlane et al., 2000). Most literature has which species live closer to their upper thermal limits and com- focused on tropical regions perhaps not only because models suggest parisons with tropical species were made. that impacts will be severe in the tropics (Tewksbury et al., 2008) but also because predictions for temperate regions are the hardest to 2. Materials and methods make due to the diversity of life history patterns, complexity of tro- fi phic relations, habitat variability and over- shing (IPCC, 1997; 2.1. Temperature data Roessig et al., 2004). Impacts of climate warming should be greatest on thermal special- 2.1.1. Atmospheric and water temperature for the intertidal zone ists that have limited acclimation potentials (Hoegh-Guldberg et al., Atmospheric temperature data for the intertidal zone was obtained 2007) and those that live in aseasonal environments (Tewksbury et from the MOHID database (open acess at www.mohid.com). In this da- al., 2008). The thermal limits of an organism are set genetically but in tabase, field data from the meteorological station of Laboratório evolutionary terms the rate at which temperature is increasing might Marítimo da Guia (38°41′42.91″ N; 9°27′08.52″ W — under 3400 m not allow the organisms to adapt genetically (Cuculescu et al., 1998). from the sampling site) was available. Temperature was recorded Thereby, the ecosystems that have evolved in stable conditions for a every half an hour during the day and night. For the purpose of this long time e.g. cold environments or tropical habitats are especially at study data from January 2010 to December 2010 were used. A detailed risk. Additionally, some tropical species are said to live close to their graph was drawn for July 2010, concerning only temperatures between upper thermal limits (Jokiel and Coles, 1977; Sharp et al., 1997) 7 am (sunrise) and 9 pm (sunset). although other authors present contradictory evidence (Mora and Ospina, 2001). It has also been suggested that warm-adapted species 2.1.2. Estuarine temperatures of the intertidal/supratidal zone may be particularly at risk since they Estuarine water temperatures were obtained from the Centro de live closer to their upper thermal limit and have limited acclimation Oceanografia database. Mean values from 1978, 1979, 1980, 1995, capacity (Hopkin et al., 2006; Somero, 2010). Despite the fact that 1996, 1997, 2001, 2002, 2005 and 2006 were used to calculate and they are more thermally tolerant there is a high probability that plot the general mean±SD temperature for each month in the maximum habitat temperatures surpass their upper thermal limit Tagus estuary. (Somero, 2010) because they live in a hot and unstable environment with wide daily and seasonal thermal amplitudes. Therefore, environmental variation has large ecological and 2.1.3. Coastal temperatures evolutionary consequences. It exerts a strong selective pressure leading Coastal water temperatures were obtained from the Centro de fi to the development of specific strategies which may be related not Oceanogra a database, Levitus and Boyer (1994) and Mohid database. only to reproductive strategies, growth and maturation but also to Thermal images of the Portuguese coast from the Mohid database were physiological and cellular mechanisms to deal with stressful conditions. obtained every 10 days throughout 2010. Environmental variability also sets life history patterns, influences bio- logical interactions (e.g. Sanford, 1999; Townsend, 1991) and creates 2.2. Study area and sampling method gaps for new colonization (Karr and Freemark, 1985; Levin and Paine, 1974). In fact, Richter et al. (1997) stated that ‘the full range of natural This study was carried out in the Tagus estuary and along the coast intra- and interannual variation of hydrological regimes, and associated (from Vila Franca de Xira to Cascais), at an approximate latitude of characteristics of timing, duration, frequency and rate of change, are 38°N (Northeast Atlantic). This estuary is located on the midwest critical in sustaining the full native biodiversity and integrity of aquatic coast of Portugal, and has an area of 320 km2, a length of 34 km and ecosystems’. This may apply not only to rivers but also to other aquatic a maximum width of 15 km. During July, the Tagus estuary and the ecosystems, in which environmental variation also occurs. This intertidal pools of the adjacent coast have a mean surface tempera- is important in the integrity and disturbance of the habitats and ture of 24 °C (Centro de Oceanografia database). communities. This research focused not only on marine and estuarine species of Research on the impacts of climate change on marine fauna should commercial importance but also on species that play an important focus on marine coastal waters and estuaries. They are amongst the role in the food web. The fish species studied were Diplodus bellottii most productive ecosystems, they are nursery areas and depuration (Steindachner 1882), Diplodus vulgaris (Geoffroy St. Hilaire 1817), systems. Furthermore, coastal waters and estuaries are shallow Diplodus sargus (Linnaeus 1758), Pegusa lascaris (Risso 1810), habitats with little thermal inertia and will, along with inhabiting Dicentrarchus labrax (Linnaeus 1758), Gobius cobitis (Pallas 1814), communities, be the first to reflect a rise in atmospheric temperature. Lipophrys trigloides (Valenciennes 1836), Gobius niger (Linnaeus Thus, they are indicators of climate change. Applying an integrated 1758) and Liza ramada (Risso 1827). The crustacean species studied and holistic approach to tolerance studies, by considering several can be divided in two groups: the crabs Liocarcinus marmoreus (Leach taxonomic groups and food chain levels may help understand which 1814), Lophozozymus incisus (Milne-Edwards 1834), Carcinus maenas community components are more vulnerable to warming. (Linnaeus 1758), Pachygrapsus marmoratus (Fabricius 1787) and the The aim of this work was to determine the Critical Thermal Maxi- shrimps Palaemon longirostris (Milne-Edwards 1837), Palaemon elegans mum (CTMax) of various temperate and subtropical species, fish and (Rathke 1837) and Crangon crangon (Linnaeus 1758). Most of these crustaceans that are important in the temperate estuarine/coastal species have a distributional range from Northern Europe to North ecosystem studied. The approach included species with different Africa, occurring in both cold and moderately warm waters. The excep- niches and habits, such as intertidal, supratidal, subtidal, demersal, tions are Crangon crangon, Palaemon longirostris and Liocarcinus as well as coastal and estuarine enabling the comparison of the marmoreus which occur mainly in cold waters in northern temperate CTMax of species inhabiting different environments. Moreover, the regions (Froese and Pauly, 2011; Palomares and Pauly, 2011). Sample aim was to cover the most commercially important and the most sizes, total lengths, environment and sampling area for each species abundant species of the assemblage. The species were then ranked are shown in Table 1. Sample sizes were similar to Mora and Ospina 34 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

Table 1a Sample size, mean total length, environment and sampling area for each species in the present study.

Species Sample size Total length (mm) Environment Habitat Depth (m); Most Distribution Sampling Mean±SD common depth (m) area

Dicentrarchus labrax 7 86.00±6.19 Demersal Estuary, coast, 10–100 Temperate/subtropical Estuary river mouths Diplodus bellottii 17 103.71±8.91 Benthopelagic/demersal Estuary, coast, 0–100; 30–50 Temperate/subtropical Estuary upwelling Diplodus sargus 28 33.89±9.07 Demersal Estuary, coast 0–50 Temperate/subtropical Estuary Diplodus vulgaris 13 74.62±7.76 Benthopelagic/demersal Estuary, coast 0–90; 0–30 Temperate/subtropical Estuary Lipophrys trigloides 9 67.33±28.26 Intertidal Coast 0–1 Temperate/subtropical Coast Gobius cobitis 4 46.00±29.41 Intertidal Coast 0–10 Temperate/subtropical Coast Gobius niger 9 98.70±6.36 Subtidal/intertidal Estuary, lagoons, 1–75; 1–50 Temperate/subtropical Estuary inshore waters Liza ramada 6 44.00±3.90 Pelagic/demersal Estuary, coast, 0–? Temperate/subtropical Estuary rivers Pegusa lascaris 8 184.38±39.70 Demersal Estuary, coast 50–350; 20–50 Temperate/subtropical Estuary Carcinus maenas 25 28.65±5.80 Intertidal Estuary, coast 0-200; 0-60 Temperate/subtropical Estuary Liocarcinus marmoreus 17 22.35±2.74 Subtidal/demersal Estuary, coast 0–200 Temperate/polar Estuary Pachygrapsus marmoratus 26 17.32±6.24 Supratidal Estuary, coast −1.5–2 Temperate/subtropical Coast Lophozozymus incisus 16 34.38±6.09 Subtidal Estuary, coast 0–40 Temperate; Northeast Atlantic Estuary Crangon crangon 16 36.50±4.84 Demersal Estuary, coast 0–50 Temperate; Northeast Atlantic Estuary Palaemon elegans 25 32.52±7.34 Intertidal Coast 0–30; 0.5–10 Temperate/subtropical Coast Palaemon 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).

(2001) for comparable analysis. The species were caught during July of Where Tend-point is the temperature at which the end-point was 2010 using hand nets, dip nets, beam trawl and beach seine. reached for individual 1, individual 2, individual n, divided by the n individuals that were in the sample. 2.3. Thermal tolerance method To determine intraspecific variability of the CTMax, the coefficient of variation (in percentage) was calculated for each species: The thermal tolerance of these species was determined by the dynamic method described in Mora and Ospina (2001). The aim was ðÞSD=Mean 100: to determine the Critical Thermal Maximum (CTMax), which is defined as the “arithmetic mean of the collective thermal points at which the In order to evaluate which species live closer to their upper end-point is reached” (Mora and Ospina, 2001). The end-point was thermal limits, the difference between CTMax and mean surface loss of equilibrium. water temperature (24 °C) was calculated for each species (fish and After having been captured, organisms were transported to the lab- crustacean). Using the work of Mora and Ospina (2001), the same oratory and were placed in a re-circulating system with aquaria with a difference was calculated for tropical species living with a mean capacity of 70 L with aerated sea water, a constant temperature of surface temperature of 27 °C. Then, the results for temperate/ 24 °C and salinity 35‰. The water dissolved O level varied between 2 subtropical and tropical fish were compared through a Student's 95% and 100%. The organisms were acclimated for 2 weeks, being fed t-test, since the data showed normal distribution (Shapiro Wilk's ad libitum twice a day. They were starved for 24 h before the test) and homoscedasticity (Levene's test). A significant level of 0.05 experiments. To determine the CTMax, the organisms were placed in was considered in all test procedures. Additionally, the difference a thermostatized bath. During the trial, animals were exposed to a con- between CTMax and Maximum Habitat Temperature (MHT) was stant rate of water-temperature increase of 1 °C.h−1,andobserved calculated for intertidal fish species from temperate/subtropical and continuously, until they reached the end-point. The temperature at tropical regions (Mora and Ospina, 2001). The crustaceans were not which each animal reached its end-point was measured with a digital included in the analysis because comparable data was only available thermometer, recorded and then the CTMax and its standard deviation for fish. MHT was considered to be 35 °C according to the mean were calculated for each species. All experiments were carried out in maximum air temperatures for the hottest days of July 2010 (4th, shaded day light (15L;09D). To prevent any additional handling stress, 5th, 25th, 26th). the total length of all individuals was measured at the end of each trial using a slide caliper ruler. 3. Results All known environmental variables that might have influenced the results (e.g. oxygen levels, salinity, food, pH, photoperiod, 3.1. Temperature data acclimation temperature) were monitored during the acclimation and trials, thus it is believed that the observed results are due to 3.1.1. Atmospheric and water temperature for the intertidal zone temperature. Temperature results showed that the intertidal zone was highly variable, with steep seasonal and daily variations in temperature 2.4. Data analysis (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. The upper thermal limits for each species were calculated using Around springtime temperatures begin to rise, reaching >35 °C the equation: during the hottest summer days. Minimum temperatures during the summer were around 17–19 °C.  During July (2010), the sampling month, the minimum tempera- CTM ¼ ∑ T =n species end−pointn ture registered during daylight was 17.2 °C and the maximum was D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41 35 a)

b) July 2010 Tmax 35 Tmin

C Tmean

o 30

25 Temperature

20

15 1 5 9 13 17 21 25 29 Days

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

36.6 °C (Fig. 1b). Mean daily temperatures ranged from 19.6 °C on the winter. However, in July 2010 (sampling period) water temperatures 31st to 31.8 °C on the 5th. reached up to 20 °C–23 °C.

fi 3.1.2. Estuarine temperatures 3.2. Interspeci c differences depending on habitat (intertidal, subtidal, The mean estuarine water temperature was lowest in January, demersal) with a mean of 12 °C and it was highest in July, with a mean of 24 °C (Fig. 2). Species from intertidal/supratidal zones showed higher CTMax values (e.g. Pachygrapsus marmoratus, Carcinus maenas, Gobius niger, Palaemon elegans, Lipophrys trigloides, Gobius cobitis)(Fig. 1). Subtidal 3.1.3. Coastal temperatures and demersal species showed lower CTMax values (e.g. Diplodus Water temperatures in the coastal area were usually in the range species, Liocarcinus marmoreus, Solea lascaris, Dicentrarchux labrax, – of 15 °C to 18 °C during the summer season and 10 16 °C during Lophozozymus incisus, Crangon crangon)(Fig. 1). The exceptions were 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 from upwelling systems showed lower CTMax values (e.g. Diplodus bellottii, Liocarcinus marmoreus, Lophozozymus incisus, Crangon crangon). Species with more southern and wide distributions showed higher CTMax values.

3.4. Differences between taxonomic groups

The CTMax values obtained for all species ranged from 27.4 °C for Fig. 2. Estuarine temperatures (mean±SD) for each month based on data from 1978, D. bellotti to 38.0 °C for L. ramada (Fig. 1). Among crabs, the lowest 1979, 1980, 1995, 1996, 1997, 2001, 2002, 2005 and 2006. CTMax value was observed in L. marmoreus (32.2 °C), followed by L. 36 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41 incisus and C. maenas. Finally, the highest CTMax observed in crabs Table 3 was for P. marmoratus (35.7 °C). Among shrimps, C. crangon had the Differences between CTMax (Critical Thermal Maximum) and mean surface water tem- perature for temperate/subtropical and tropical fish species. First of all, the differences lowest CTMax (33.8 °C) and Palaemon longirostris had the highest were calculated for all the species included in this work and in Mora and Ospina fi (34.4 °C). Among sh, the lowest CTMax values were observed for (2001). Following, differences were tested dividing the fish in two groups: demersal two Diplodus species (D. bellottii and D. vulgaris) and the highest and intertidal. Significant differences (p-valueb0.03) are presented in bold. CTMax values, besides L. ramada, were observed for G. niger Mean difference (°C) Mean difference (°C) Mean difference (°C) (34.1 °C) and B. trigloides (34.0 °C). Additionally, Diplodus sargus showed a higher CTMax when compared to other Diplodus species. All species Demersal species Intertidal species The CTMax was the most variable between fish species (10.6 °C), fol- Temperate/ 9.16 9.84 9.95 lowed by crabs (3.5 °C) and the least variable between shrimp species subtropical Tropical 9.73 9.17 12.00 (0.7 °C).

fi 3.5. Intraspeci c differences temperate/subtropical species was 1 to 2 °C lower than the MHT in the present study (Table 4). Intraspecific variability, given by %CV, was generally low. The spe- cies with the lowest %CV were S. lascaris and L. ramada. The species with the highest variability were D. labrax, D.vulgaris and D. bellottii 4. Discussion (Table 2). 4.1. Temperature data

3.6. Climate change: temperate versus tropical species As expected, the most variable environment studied was the inter- tidal zone with steep variations in temperature, both daily and The species living closer to its thermal limits was D. bellottii with a seasonally. Changes are in the order of >20 °C seasonally and 15 °C difference of only 3.4 °C between the summer mean surface water daily. The estuary studied is also a relatively variable environment temperature and its CTMax. Next comes D. vulgaris with a difference with a difference of 12 °C between the coldest and the hottest months of 7.1 °C. The species living the farthest from its thermal limits was (January and July). However, comparing it to the intertidal zone, it is a L. ramada with a difference of 14.0 °C between summer mean water less variable environment. Coastal environments are the least temperature and its CTMax. In between these values were the demer- variable out of the habitats studied. Nevertheless they also showed sal and intertidal/supratidal species, with approximately 8 to 10 °C seasonal variations of 5 °C. Therefore, the results showed that thermal and 9 to 11 °C of a difference between the mean water temperature stress is higher in the intertidal zone, followed by in the Tagus estuary and the CTMax (Fig. 1). and lastly in the coastal subtidal zone. In this habitat, temperatures After analyzing the differences between the CTMax and the mean are lower and less variable, and thus it is a more stable habitat for surface temperature for temperate/subtropical and tropical fish spe- the species. cies (Table 3), no significant differences were found (p-value>0.53). However, when differences were analyzed by dividing the fish in 4.2. Interspecific differences depending on habitat (intertidal, subtidal, two groups (demersal and intertidal) significant differences were demersal) found for intertidal species (p-valueb0.03), but not for demersal ones (p-value>0.71). Results showed that intertidal species had the highest CTMax Maximum Habitat Temperature (MHT) can reach up to a mean of value (Fig. 3, Table 5). This habitat is an extremely variable one at 35 °C in the study area (Portugal's Meteorological Institute database several levels such as temperature, salinity and dissolved oxygen. and open access Mohid database — www.mohid.com) so organisms Our results and Tomanek's (2010), show that intertidal areas can in the intertidal area can be subjected to very high temperatures. experience changes of >20 °C. The abiotic factors are crucial and For tropical areas, the MHT was 36 °C for tidal pools (Mora and partially responsible for littoral zonation of the organisms living in Ospina, 2001). The results show that the CTMax of tropical intertidal that habitat, depending on how adapted they are to water loss and species was 2 to 5 °C higher than the MHT while the CTMax of heat. Species inhabiting such an environment, especially the resident ones, have evolved specific adaptations that allow them to cope with environmental stress due to exposure to terrestrial conditions (Stillman, 2002). These adaptations lead to a higher CTMax hence Table 2 CTMax (Critical Thermal Maximum) intraspecific variability given by the reason why organisms living in variable environments have the coefficient of variation (in percentage). higher tolerances (e.g. Badillo et al., 2002; Mora and Ospina, 2001; Shaefer and Ryan, 2006) than those living in more stable environ- %CV Species ments, e.g. the subtidal zone. Additionally, species that also explore 0 Pegusa lascaris the supratidal zone (e.g. Pachygrapsus marmoratus) showed an even Liza ramada 1≤%CV≤2 Liocarcinus marmoreus Crangon crangon Table 4 Gobius cobitis Differences between CTMax (Critical Thermal Maximum) and MHT (Maximum Habitat Diplodus sargus Temperature) for temperate/subtropical and tropical intertidal fish. The difference was Lipophrys trigloides calculated for each species and then a mean difference and SD was calculated for each b ≤ 2 %CV 3 Carcinus maenas latitudinal group. CTMaxs of tropical fish used in these calculations were obtained from Pachygrapsus marmoratus Mora and Ospina (2001). 3b%CV≤4 Lophozozymus incisus Palaemon elegans Temperate/subtropical Tropical Gobius niger Gobius Gobius Lipophrys Malacoctenus Bathygobius Mugil Palaemon longirostris cobitis niger trigloides zonifer ramosus curema 4b%CV≤5 Diplodus bellottii Diplodus vulgaris CTM-MHT (°C) −1.25 −0.90 −1.00 2.1 3.5 4.8 >5 Dicentrarchus labrax Mean±SD (°C) −1.05±0.18 3.46±1.35 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41 37

Intertidal Demersal 40 Subtidal M 38

36 M

34 C o

32

30

28 Temperature 26

24

22

20

Gobius niger Liza ramada Gobius cobitis Pegusa lascaris Diplodus sargus PalaemonCarcinus elegans maenas DiplodusDiplodus bellottii vulgaris Crangon crangon Lipophrys trigloides Palaemon longirostris Dicentrarchus labrax LophozozymusLiocarcinus incisus marmoreus Pachygrapsus marmoratus

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 species and 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 study area (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 are tagged with M. greater CTMax as they are exposed to terrestrial conditions most of range on a regional scale, so crabs from the North Sea would be the time. Our results, along with other studies (e.g. Davenport and expected to have lower CTMax values than their conspecifics living Davenport, 2005; Davenport and McAlister, 1996) follow the idea more to the south (e.g. Beitinger et al., 2000; Eme and Bennett, that organisms living in higher shore are more tolerant than those 2009; Freitas et al., 2010; Lutterschmidt and Hutchison, 1997a; in the lower shore. Other authors, however, did not find such a Mora and Ospina, 2001; Re et al., 2005; Shaefer and Ryan, 2006). connection (e.g. Clarke et al., 2000). However, this was not the case. Results suggest that this species Subtidal and demersal species had lower CTMax values (Fig. 3, does not adapt or acclimate locally, which is in agreement with Table 5). These species live in relatively variable or more stable Tomanek (2005) and Tomanek and Somero (1999, 2002). habitats (e.g. estuaries, coastal waters, coastal upwelling, deep Among species with a temperate/subtropical distribution, results waters) so they are exposed to lower temperatures, having physiolog- showed that species with a wide continuous distribution (e.g. ical set-points lower in the temperature gradient. The exceptions to Diplodus sargus) had higher CTMax values than species with a wide this pattern were migratory species (Palaemon longirostris and Liza but discontinuous distribution (e.g. Diplodus vulgaris). A continuous ramada). These species have to pass through several habitat types distribution means that species can also occur in tropical areas and thermal regimes to be able to reproduce and keep the population while a discontinuous distribution means that they are absent from numbers up, so higher tolerances were expected for these species. the warmer zones. Thus, if discontinuous species are absent from the warmer areas, they are not capable of withstanding very high 4.3. Interspecific differences depending on geographic distribution temperatures. Hence, they showed lower CTMax values.

Species which have a distributional range in the Northern/Eastern 4.4. Differences between taxonomic groups Atlantic or live in upwelling systems are characteristically from colder waters (e.g. Diplodus bellottii, Liocarcinus marmoreus, Lophozozymus The analysis of CTMax values over several taxonomic groups incisus, Crangon crangon). Therefore, they showed lower CTMax showed that species from different taxa living in identical habitat values when compared to species with wider and more southern types had similar upper thermal limits (Fig. 1). As they have evolved distributional ranges. A wide distributional area means that species in similar abiotic conditions, they have probably developed identical need to function over a wide range of temperatures, so their physiol- physiological and cellular adaptations. At first, we expected a greater ogy allows them to withstand very different temperatures by having discrepancy as the mean genetic distance increased but this would more extreme thermal limits. In order to address local adaptation/ only occur if ecological niches were very dissimilar. This was not the acclimation of CTMax in wide distributed species we compared our case because we analyzed fish, crabs and shrimps from every type results for Carcinus maenas with the results obtained by Ahsanullah of habitat. Thus, the observed differences are mainly due to habitat and Newell (1971) and Cuculescu et al. (1998) for the same species. type, distributional depth and geographic distribution. Nevertheless, The analysis showed that the CTMax was very similar for northern each species has its own genetic traits and set-points for physiological and southern crabs (around 35 °C). Some authors report that performance (see Dent and Lutterschmidt, 2003) which may also set organisms suffer local adaptation or acclimation to the temperature thermal limits. 38 D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41

Table 5 Main findings of the present study.

Results Rationale

4.2 Interspecific differences depending on Higher CTMax in intertidal/supratidal species Highly variable environment, extreme temperature values habitat (intertidal, subtidal, demersal) Higher CTMax in migratory species They have to pass through several thermal regimes in order to reproduce Lower CTMax in subtidal/demersal species More stable habitats with lower temperatures 4.3 Interspecific differences depending Lower CTMax in Northern/Eastern Atlantic species Colder waters on geographic distribution Lower CTMax in species from upwelling areas Colder waters Higher CTMax in species with southern distribution Warmer waters Higher CTMax in eurythermal species They have to perform across a broad range of temperature Higher CTMax in species with a wide continuous distribution They can occur in warmer stretches of the globe Lower CTMax in species with a wide discontinuous distribution They are absent from the warmer stretches of the globe 4.4 Differences between taxonomic Species from different taxa living in similar habitats have They evolved in similar abiotic conditions so they probably groups similar CTMax developed identical physiological and cellular adaptations CTMax was more variable between fish than between crabs Fish have a great locomotory capacity and colonize all kinds and shrimps of habitats 4.5 Intraspecific differences Generally low intraspecific variability Specific genetic features and the previous influence of environmental variables D. labrax, D. bellotti and D. vulgaris appear to have the highest They possibly have the highest genetic variability concerning variability the genes involved in the stress response 4.6 Climate change: temperate D. bellotii and D. vulgaris might be threatened by sea warming Their CTMaxs are really close to mean water temperature (24°) versus tropical species and they are already in stress during heat waves (28°) or will be stressed in a climate change scenario of a plus 2 °C increase in water temperature (24+2=26 °C; 28+2=30 °C) Intertidal temperate/subtropical fish have an upper thermal limit on average 9.95 °C above mean water temperature (24°) Tropical intertidal fish have an upper thermal limit on average 12 °C above mean water temperature (27 °C). Temperate/subtropical fish have CTMaxs on average 1.05 °C May rely on a strategy of escaping extreme conditions through under the maximum habitat temperature behavioral thermoregulation Tropical species have CTMaxs on average 3.46 °C above maximum habitat temperatures Higher vulnerability of intertidal/supratidal organisms towards CTMax is high but they live closer to their thermal limits. climate change Maximum Habitat Temperatures may reach or exceed their CTMax Eurythermal species may be vulnerable even though they Eurythermal species show limited acclimatory plasticity when perform in a wide range of temperatures compared to stenothermal ones

In addition, the CTMax was more variable between fish than be- state, nutritional condition, diseases and parasites, inter-population tween crabs and shrimps. This is probably because fish have a great variability, age/size (Becker and Genoway, 1979; Copeland et al., locomotory capacity and colonize all kinds of habitats. Therefore, if 1974; Cox, 1974; Hutchison, 1976; Lutterschmidt and Hutchison, the CTMax and optimal temperatures are co-adapted (Huey and 1997b) and seasonal variation (Cuculescu et al., 1998; Hopkin et al., Kingsolver, 1993), the diversity of habitats (i.e. thermal regimes) 2006). Yet, there seems to be a certain degree of controversy on the accounts for the variation in CTMax. influence of these factors as some authors found significant differences for instance between different sized individuals (e.g. Copeland et al., 4.5. Intraspecific differences 1974; Cox, 1974; Peck et al., 2004, 2007, 2009) while others did not (e.g. Ospina and Mora, 2004), nor for males versus females (Badillo Intraspecific variability was generally low, which is in concor- et al., 2002). Even though we limited the influence of some of these dance with Mora and Ospina (2001). According to Cuculescu et al. factors by, for example, restricting sampling to July and testing individ- (1998), thermal tolerance is subjected to phenotypic alteration uals of approximately the same size, this might have the disadvantage within a genetically fixed range. This phenotypic plasticity is depen- of missing important intraspecific variability patterns. Further studies dent upon several factors but thermal history of individuals and should address this issue and the CTMax should be tested at different parental effects (e.g. epigenetic changes) seem to be the most life stages, for different sexes, different seasons and different habitats important ones (Cossins and Bowler, 1987; Shaefer and Ryan, 2006). used by conspecifics. These factors induce irreversible changes to thermal tolerance (Shaefer and Ryan, 2006). Then, variability found for each species 4.6. Climate change: temperate versus tropical species relates not only to specific genetic features but also to the previous influence of environmental variables. Although genetic variability is In order to know which species might be more vulnerable to tem- low in general, this does not mean that organisms will not be able to perature and further sea warming, we calculated the difference adapt to further warming due to climate change. If thermal history in- between thermal limit and mean water temperature for each species. fluences CTMax then it is possible that in each generation phenotypes Mora and Ospina (2001) conducted a similar study on tropical reef with higher CTMax values are being produced due to sea warming. fish and concluded that the CTMax of the least tolerant species was Nevertheless, there are no certainties yet so further research is needed 8 °C above the current mean sea temperature, while in the present on the capacity to adapt. Our data shows that D. labrax, D. bellotti and D. study the CTMax of the least tolerant species, D. bellottii, is only 3 °C vulgaris appear to have the highest variability in the response to tem- above the average summer estuarine temperature (it is in summer perature and thus possibly have the highest genetic variability in the that this species' juveniles occur in estuaries). In fact, this species is genes involved in such a response. already under stress during current heat waves because the water There are various untested factors that can potentially influence the temperature can reach 28 °C, and last for more than 2 weeks. species' upper thermal limits. These factors can be sex, reproductive D. bellottii's CTMax is 27.4 °C, which is very close to 28 °C. Thus, its D. Madeira et al. / Journal of Sea Research 70 (2012) 32–41 39 presence in estuarine nursery areas (where juveniles are very 1999). Thus, intertidal/supratidal and eurythermal organisms may abundant nowadays) is possibly threatened by climate warming, as be more vulnerable to further temperature increases, and have to observed by Vinagre et al. (in press) during experimental studies. In a rely on behavioral thermoregulation to survive these extreme climate warming scenario, if we add 2 °C (Miranda et al., 2002)tothe conditions. current temperature attained by the waters during heat waves (28 °C +2 °C), it is clear that another seabream, D. vulgaris (CTMax 31.1 °C), 4.7. Conclusions may also face thermal stress. After comparing mean differences between CTMax and mean Predicting the impacts of climate change on particular species is not fi water temperature for temperate/subtropical and tropical sh, no sig- a simple task and requires in depth knowledge on several subjects from fi ni cant differences were found considering all species. When we molecular biology, physiology, ecology and evolution. Thus, realistic evaluated demersal and intertidal species separately, demersal ones predictions will essentially be the result of multidisciplinary and fi did not show signi cant differences either, but intertidal species integrative approaches. Since sea warming effects are already clear fi did. The intertidal temperate/subtropical sh had an upper thermal throughout ecosystems and base studies are urgently needed, the find- limit on average 9.95 °C above mean water temperature (24 °C) ings of the present study (summarized in Table 5) are considered a fi while tropical intertidal sh had an upper thermal limit on average necessary first step in the investigation of climate change impacts 12 °C above mean water temperature (27 °C). This suggests that upon marine biota and ecosystems. temperate/subtropical intertidal species might be more vulnerable to further increases in temperature. In addition, we calculated the difference between CTMax and Role of the funding source Maximum Habitat Temperature (MHT) for temperate/subtropical and ‘ fi tropical intertidal fish. Results showed that temperate/subtropical fish This study was entirely supported by Centro de Oceanogra a, ’ have CTMax values on average 1.05 °C under the maximum habitat Faculdade de Ciências, Universidade de Lisboa . Study design, temperature while tropical species have CTMax values on average collection, analysis and interpretation of data, report writing, and the 3.46 °C above maximum habitat temperatures. Therefore, maximum decision to submit the article for publication were carried out solely habitat temperatures in temperate/subtropical regions may exceed by the authors and not by the sponsor. the upper thermal limits of intertidal fish species, making them espe- cially vulnerable to high temperatures and climate warming. However, Acknowledgments further studies should focus on obtaining more comparable data in order to reveal patterns in temperate and tropical organisms. Authors would like to thank everyone involved in the field work, In general, results show that although organisms that occur in maintenance of the experimental tanks and in the feeding of the thermally unstable environments, e.g. intertidal/supratidal habitats, organisms. Authors would like to express their gratitude to “Aquário have higher CTMax values, they live closer to their thermal limits. Vasco da Gama” for the collaboration in the sampling and This occurs because maximum habitat temperatures may reach or maintenance of organisms, in particular to Dr Fátima Gil. Authors exceed their CTMax. Subtidal species are in less danger since they would like to thank Zara Reveley for the English revision. This study rarely encounter temperatures near their CTMax. These results are had the support of the Portuguese Fundação para a Ciência e a in accordance with Somero, 2010. 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