Latchere O. a, Petit N
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Discussion The primary objective of this work was to compare the resistance to two major environmental stressors (temperature and salinity) between native and NIS palaemonid shrimps, through the comprehensive study of their critical temperature maximal, oxygen consumption and long-term survival. Such a series of experiments has rarely been conducted at the same time on NIS and native species using both sympatric and phylogenetically close taxa . In the case of P. macrodactylus and P. longirostris, they were even syntopic and congeneric. CTmax We evaluated simultaneously the upper thermal tolerance of the two native shrimps P. varians and P. longirostris, and of the NIS P. macrodactylus. Such an approach comparing CTmax of both sympatric and related, native species and NIS under identical experimental conditions has rarely been adopted . There were clear significant differences in the CTmax values found between the three species (Fig. 3). The species P. longirostris presents by far the lowest CTmax value (27.24 ºC ± 2.16), while P. varians and P. macrodactylus present closer though significantly different CTmax values (31.71 ºC ± 2.21 and 33.0 ºC ± 1.11 respectively). The high interspecific difference found in CTmax values between the two European native species is likely to be associated with their habitat preferences. The Atlantic ditch shrimp P. varians is a ubiquitous shrimp inhabiting shallow waters (mainly ponds and canals) in and around NE Atlantic estuaries. It typically tolerates salinity ranges from 1-2 to >45 (though it has a preference for brackish waters), associated with seasonal fluctuations of water temperature ranging from 0 to 33 °C, and summer daily variations >10 °C . The delta prawn P. longirostris is strictly estuarine, present in all the NE Atlantic . The species is known to be euryhaline though being more abundant in brackish waters at the outer estuarine zone and in intermediate salinities, with spatial sexual segregation and within-estuary reproductive migrations . Temperature ranges experienced by this species are therefore those of the estuary itself. In the Guadalquivir river where P. longirostris and P. macrodactylus were sampled, temperature is quite homogenous along the estuary and presents a consistent seasonal pattern oscillating in the 10-30ºC range, with summer daily variations of <5ºC . Major differences in habitat preferences between the two native species thus imply differences in water depth and temperatures: maximum water temperatures in ponds and canals frequented by P. varians are much higher with strong daily and seasonal temperature fluctuations (especially in summer), while in the core of the river estuary used by P. longirostris such variations are highly buffered. Adaptation of each species to its environment is reflected in their different CTmax values and ecophysiology may partly explain the niche partitioning observed between these two sympatric species. As for the NIS P. macrodactylus, we report in this study the first CTmax value (33.0 ºC ± 1.11) for this worldwide invader, which is much higher than for the two European natives (27.24 ºC ± 2.16 and 31.71 ºC ± 2.21 for Palaemonetes varians and P. longirostris respectively). Compared to values found in the literature for other Palaemonid adults, these values are low. The Mississippi grass shrimp Palaemonetes kadakiensis or shrimps of the widespread genus Macrobrachium present much higher values . However, those species are tropical freshwater species living in waters that never cool down to 20ºC, and as such their acclimation was conducted at higher temperatures than in the present study (. More interestingly, the CTmax of P. macrodactylus is closer to that of its Euro-Mediterranean euryoecious temperate congener P. serratus . In any case, the present study clearly demonstrates that the NIS P. macrodactylus presents a higher upper thermal tolerance than the native P. varians and P. longirostris when submitted to an acute thermal stress. Intraspecific comparisons for our specimens of P. varians sampled in SW Spain can be made with French specimens stressed with a similar temperature ramp (0.9 ºC.min-1) but acclimated at 10 ºC and 20 ºC . The CTmax value we observed for P. varians (31.71 ºC ± 2.21) is more similar to the previous CTmax value reported for the 10 ºC-acclimated P. varians than for the 20 ºC-acclimated shrimps . Such a discrepancy might be explained by either the differences in acclimation duration (4 months vs. 48h in our study) or salinity of water used (salinity 35 vs. 5 in our study), or both. In the case of P. longirostris, obtained a much higher CTmax value of 34.4 ºC (Portuguese shrimps acclimated for 2 weeks at 24 ºC and salinity 35 and stressed with a temperature ramp of 1 ºC.h-1) than in the present study (27.24 ºC ± 2.16). Unlike for P. varians, the very different heating rates used in the two studies are the most likely explanation for this difference. Indeed, an exhaustive literature review demonstrated that commonly-used temperature ramps (in the 0.5–1.5°C.min–1 range, as in the present study) allow avoidance of either thermal acclimation (so called heat-hardening) or mismatching of body and environmental temperatures, due to slow or excessive heating rates respectively . Moreover, non-significant differences have been shown between environmental and body temperatures for animals of <150g submitted to a heating rate of 1 ºC.min-1 . As a consequence, a match between experimental and shrimp body temperatures without heat-hardening can be assumed in the present study. In any case, the examples of P. varians and P. longirostris illustrate that caution must be taken when comparing CTmax values between studies, even within a single species, as they clearly depend on both acclimation temperature and experimental procedures and can also differ markedly between seasons . Adequate interspecific comparisons can however be made through experiments that use the same behavioral parameters and similar heating rates as in or in the present study.
Oxygen consumption In the present study, under the different stressful conditions of temperature and salinity tested, the NIS consistently showed better respiratory performances, with lower OCRs than its native counterparts (Fig. 4). Such a pattern of better NIS performance had previously been observed between the NIS P. macrodactylus and the native P. longirostris, for various combinations of salinity and dissolved oxygen concentrations (but not of temperature), although such interspecific differences were not always statistically significant and acclimation conditions were much less drastic . P. macrodactylus was shown to be much more tolerant than P. longirostris under stressful hypoxic conditions which, associated with the present eutrophication of estuaries in Europe, might help the NIS to outcompete its native congener . Our results for both salinity and temperature agree with and support this scenario, and are in accordance with other studies dealing with NIS from a wide range of phyla such as tunicates, other crustaceans, and fishes . Overall, our results reinforce previous findings that a successful NIS is often associated with a much better respiratory performance and more efficient metabolism compared to native congeners. We recorded a similar trend for increase in OCRs with salinity and temperature for all species (Fig. 4). Because of the major role of these two major abiotic variables in physiological responses of most invertebrates , such increases are quite common and were previously recorded for congeners such as Palaemonetes pugio, Palaemon peringueyi or Palaemon pacificus ). However, direct comparisons of values from the literature are difficult, due to differences in methodology and study aims. However, trends can be compared, and a similar increase of OCR with dissolved oxygen concentration and salinity (but not for temperature) was previously found for the two Palaemon species from the Guadalquivir river . A similar pattern was also found previously for P. varians , and is quite common for decapod shrimps and other invertebrates . However, unlike the present study, OCRs have rarely been compared between sympatric NIS and native species reared under identical conditions of both temperature and salinity. Comparative survival of P. longirostris and P. macrodactylus under chronic stress In the present study, we deliberately used normal to acute parameters of chronic stress compared to those found in the wild in order to evaluate the comparative survival abilities of the native species and the NIS. Chronic exposure to a stress factor increases physiological stress, sometimes compromising fitness and even survival, while in other cases it might induce a better resistance of the organism to future, more acute stress through an increase of the tolerance threshold . Furthermore, the duration, frequency and intensity of stress factors are fundamental in conditioning the organismal response to chronic stress. The chronic exposure to temperature gave contrasting results between the two syntopic, congeneric species as the survival of the NIS P. macrodactylus was not affected by temperature, while the native species P. longirostris was negatively affected by high temperature (28ºC). Differences between the two species at this high temperature were significant. These results are of particular interest in the present context of climate change, which often results in an increase of both air and water temperatures . The chronic exposure at a temperature of 28ºC is quite realistic in estuarine waters in southern Europe. Such a temperature is presently often reached during summer periods (e.g. in the Guadalquivir river) and might be more frequently encountered in the wild with the observed and predicted increasing temperature in the Euro-Mediterranean zone, and especially in SW Spain . This double stress of climate change and competition with NIS is becoming a very common pattern of threats for native species in general. Indeed, many of them are presently close to their upper thermal tolerance, with dispersal abilities being much lower than NIS and insufficient to cope with the pace of climate change . Chronic exposure to high salinity had a significant effect on the survival of both P. longirostris and P. macrodactylus. As long as salinity remained in a range similar to that found in the estuary (5-25), no difference in survival could be noted between the native and NIS. However, at higher salinity (45), survival of both species was severely affected, with the NIS presenting a significantly higher mortality than the native species (Fig. 5). Such a discrepancy in the survival under acute chronic salinity stress mirrors the different habitat preferences found between the two species. Indeed, despite similar osmoregulatory capacities in the 3-35 salinity range, P. longirostris and P. macrodactylus present different, though largely overlapping, salinity preferences . Those differences seem to have been accentuated since the introduction of P. macrodactylus that displaced the midpoint of distribution of the native P. longirostris in invaded estuaries . Presently the midpoint of P. macrodactylus is more commonly found in the inner part of European estuaries with greater abundance at lower salinities, while P. longirostris is more common in the outer estuarine zone and at intermediate salinities . The NIS preference for lower salinity in the Guadalquivir River associated with different survival at experimental long-term high salinity might thus reflect a higher sensitivity of the NIS to salinity. However this result should be treated with caution, as the experimental salinity at which differences between species was found is much higher than the natural salinities both species experience in the wild. Moreover, P. macrodactylus can be found in polyhaline to mixoeuhaline waters in other invaded areas (e.g. Argentina or the United Kingdom), and in the Gironde estuary, France, the species prefers mesohaline to polyhaline waters while the native species is found in lower salinity waters, unlike in SW Spain . In any case, as expected for estuarine species, there were no significant differences between species in survival when exposed to chronic salinity stress within the range of natural estuarine fluctuations. .
Concluding remarks We found that the NIS was more tolerant to rapid increase in temperature than the two native species, and consistently consumed less oxygen than native species, over a broad range of temperatures and salinities. P. macrodactylus also had lower mortality rates at high temperatures than P. longirostris. Overall, using a rare combination of comparative experiments on sympatric and congeneric species, this work further substantiates the broader physiological tolerance hypothesis of NIS as evoked by through the greater eurythermality of invasive species. Indeed, it is often assumed that NIS tend to inhabit locations with broader ranges of stress factors (e.g. temperature) and higher maxima than native species. Range width has often been evoked as a general trait of invasive success, with propagule pressure and broad physiological tolerance as main explicative variables acting jointly or separately . Propagule pressure can play a fundamental, but not exclusive, role providing new individuals and genotypes due to the close proximity of the primary sites of introduction (e.g. ballast water release from shipping traffic) with the surrounding habitats . However, during pre- and post-establishment, NIS have to pass through a series of abiotic filters to become introduced, then invasive . Species presenting broader physiological tolerances may thus be more able to survive and establish . Without excluding the role of propagule pressure in the success of P. macrodactylus, this work provides empirical evidence that the NIS P. macrodactylus has a broader tolerance to abiotic stress (especially temperature) and better physiological performance than closely related native species, particularly the European syntopic P. longirostris. This is especially true in the present context of climate change where increased temperatures associated with more frequent and severe thermal events are expected . Tolerance to abiotic factors and especially to temperature may play a fundamental role and might help NIS to spread faster than expected (e.g. in the Mediterranean Sea) and out-compete natives . Future research should take more into account the physiological tolerance hypothesis and explore whether the effect of eurytolerance (not only eurythermality) might be a general pattern in invasion success, and occur during the pre- or post-establishment of NIS. For the shrimps under study here, it would be useful to compare experimentally the physiological tolerance at the egg and larval stages for each species, as well as to use an ecogenomic approach to compare gene expression under stress, and genetic adaptation to environmental extremes. Acknowledgements We are indebted to Raquel López-Luque, Cristina Pérez-González, Cristina Coccia, Carmen Diaz, Alice Saunier, J. Miguel Medialdea and to Pesquerías Isla Mayor, S.A. for their assistance during fieldwork. Technical assistance was kindly provided by Francisco M. Miranda-Castro and by the staff of the Laboratory of Ecophysiology and of the Laboratory of Aquatic Ecology at the Doñana Biological Station-CSIC. We are also grateful to Doñana Natural Space for sampling authorization. We thank the three anonymous reviewers for the useful comments. This work was funded by the Spanish Ministry of Economy and Competitiveness (program CGL2010-16028). References Allan, E.L., Froneman, P.W., Hodgson, A.N., 2006. Effects of temperature and salinity on the standard metabolic rate (SMR) of the caridean shrimp Palaemon peringueyi. Journal of Experimental Marine Biology and Ecology 337, 103-108. Angilletta, M.J.J., 2009. Thermal Adapatation - A Theoretical and Empirical Synthesis. 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S = 5
PV 5.82b mm (± 1.10, SD) PM 5.49b mm (± 1.00, SD)
4.50-8.22 mm 4.05-8.35 mm
1.22
S = 5
PV 5.69d mm (± 0.20, SE) PM 6.32cd mm (± 0.33, SE)
3.76-8.08 mm 4.44-8.86 mm
1.64
PV 6.01e mm (± 0.20, SE) PM 5.88e mm (± 0.28, SE)
3.76-8.87 mm 3.90-8.68 mm
3.70* 1.44
S = 5
PM 6.57f mm (±1.70, SD) 4.51-12.36 mm PM 6.30g mm (±1.36, SD) 4.51-10.19 mm Figure 1: Sampling locations in the Guadalquivir estuary, south-west Spain. Sampling points are indicated by black dots. Fig. 2: Distribution of behavioral categories (lower figures) of the three palaemonid shrimps Palaemon longirostris, Palaemonetes varians and Palaemon macrodactylus according to temperature increase (upper). Moving: empty circles; active moving: solid black circles; loss of equilibrium (LOE): solid black triangles; spasms: solid black squares. Note the change of scale for the horizontal and vertical axes. Figure 3: Boxplot of the critical thermal maximum (CTmax) values for the three palaemonid shrimps Palaemon longirostris, Palaemonetes varians and Palaemon macrodactylus. For each box, the first and third quartiles delimitate the box, the bold line represents the median value, the dashed line the mean of the CTmax, the whiskers represent the minimum and maximum values, and the empty circle represents an outlier. Values of mean CTmax with different letters are significantly different. Figure 4: Oxygen consumption rates according to salinity (left) and temperature (right) for Palaemon macrodactylus (circles), Palaemon longirostris (squares) and Palaemonetes varians (triangles). For each species, values with different letters are significantly different. Figure 5: Kaplan–Meier survival estimates (filled lines) with 95% confidence bounds (dashed lines) for Palaemon longirostris (PL) and Palaemon macrodactylus (PM) under different conditions of temperature and salinity. re gene expression under stress, and genetic adaptation to environmental extremes. Figure 1
Fig. 2
Figure 3
Boxplot of the critical thermal maximum (CTmax) values for the three palaemonid shrimps. For each box, the first and third quartiles delimitate the box, the bold line represents the median value, the dashed line the mean of the CTmax, the whiskers represent the minimum and maximum values, and the empty circle represents an outlier. Values of mean CTmax with different letters are significantly different. 
Figure 4
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