Embed Size (px)
Citation preview
Do invaders always perform better? Comparing the response of native and invasive shrimps to temperature and salinity gradients in south-west Spain
Lejeusne C.a*, Latchere O.a, Petit N.a, Rico C.a, Green A. J.a
a Doñana Biological Station-CSIC, EBD-CSIC, Wetland Ecology Department, Avenida Américo Vespucio s/n, 41092 Sevilla, Spain
* Corresponding author: Christophe LejeusneDoñana Biological Station-CSIC, EBD-CSIC, Wetland Ecology Department, Avenida Américo Vespucio s/n, 41092 Sevilla, Spain [email protected].: +34 954 232 340
Abstract
Invasive species are often thought to benefit from climate change, outcompeting native species as
temperatures increase. However, the physiological tolerance has been little explored as a potential
mechanism explaining biological invasion success. In this study, we used empirical data from both
invasive and native estuarine species as a case study to address the hypotheses that (1) invasive species
show a better resistance to acute thermal stress, (2) invasive species present lower oxygen consumption
rates owing to greater resistance to environmental stressors, and (3) native species have lower survival
rates under chronic temperature and salinity stress. We conducted various comparative experiments on
three sympatric and syntopic closely related shrimp species (one invasive Palaemon macrodactylus, and
two natives Palaemon longirostris and Palaemonetes varians). We evaluated their critical temperature
maxima, their oxygen consumption rates under different salinities and temperatures, and their survival
rates under chronic salinity and temperature. We found that the invasive species was the most tolerant to
rapid increase in temperature, and consistently consumed less oxygen over a broad range of temperatures
and salinities. P. macrodactylus also had lower mortality rates at high temperatures than P. longirostris.
These results support previously reported differences in physiological tolerance between native and
invasive species, with the invasive species always performing better. The consistently higher tolerance of
1
123456789
10111213141516171819
20
21
22
23
24
25
26
27
28
29
30
31
32
33
1
the non-indigenous species to temperature variation suggests that climate change will increase the success
of invaders.
Keywords: Introduced species, Estuarine organisms, Environmental factors, Biological Stress, Palaemon
macrodactylus
Regional index terms: Europe, Spain, Andalusia, Guadalquivir River
2
1
2
3
4
5
6
1
1. Introduction
Invasive species often have tremendous ecological impacts on invaded ecosystems and native species
(Nentwig, 2007; Richardson and Pysek, 2008). They also have huge economic impacts estimated at more
than five per cent of the global economy (Burgiel and Muir, 2010). Together with climate change, they
constitute a “deadly duo” threatening worldwide biodiversity (Halpern et al., 2008; Burgiel and Muir,
2010; Barnosky et al., 2012). Both factors can act individually on species abundances, distributions and
biotic interactions, inducing local and regional extinctions (Grosholz, 2002; Parmesan, 2006; Lejeusne et
al., 2010; Durrieu de Madron et al., 2011), but they also can act synergistically (Dukes and Mooney,
1999; Stachowicz et al., 2002; Hellmann et al., 2008)
To become established then invasive, a non-indigenous species (NIS) has to successfully pass through a
series of biotic and abiotic filters acting as barriers between the different steps of the invasion process (see
Blackburn et al., 2011 for synthesis). However, the mechanisms leading to a successful invasion are
poorly understood in most cases. The numerous non-exclusive hypotheses proposed to explain invasion
mechanisms, include evolutionary hypotheses (e.g. hybridisation) and ecological hypotheses (e.g. enemy
release) (Hufbauer and Torchin, 2007; Sax et al., 2007; Catford et al., 2009). Another potential
mechanism, the physiological tolerance hypothesis, is as yet relatively unexplored (Zerebecki and Sorte,
2011). This hypothesis predicts that invasive species have a greater and/or broader physiological
tolerance than native species occupying the same habitat. Predictions of this hypothesis have been
verified in a large taxonomical panel of species and stress factors (e.g. Lenz et al., 2011). However, owing
to the importance of climate change, most of the studies dealing with this hypothesis have focused on
temperature effects and eurythermality of invasives compared to a more stenothermal tolerance of natives
(Dukes and Mooney, 1999; McMahon, 2002; Rahel et al., 2008; Zerebecki and Sorte, 2011). In the
present study, we address tolerance to two major environmental factors (salinity and temperature) as
potential contributors to the success of an invasive estuarine species.
3
12
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
1
Estuaries are very productive ecosystems providing nursery habitats to many marine and commercial
species. These marine-freshwater ecotones show strong fluctuations of physical and chemical parameters
at both spatial and temporal scales (e.g. tidal-based salinity fluctuations with a decreasing spatial gradient
from the inner mouth). Estuaries are particularly impacted by climate change but are also especially
susceptible to biological invasions (Ruiz et al., 1997; Cohen and Carlton, 1998; Wasson et al., 2001;
Grosholz, 2002). In the San Francisco estuary, one new NIS is recorded every 14 weeks, and in Europe
one fifth of estuarine species are NIS (Cohen and Carlton, 1998; Reise et al., 2006). One key question is
whether NIS have more resistance to environmental stressors than native estuarine species, being better
adapted to strong fluctuations in temperature and salinity.
The oriental shrimp (also known as migrant prawn, or grass shrimp) Palaemon macrodactylus is an
estuarine caridean shrimp native to China, Japan and Korea. It was initially introduced to San Francisco
Bay, CA in the 1960s, before spreading northward along the US coast. Since 1992, it has reached Europe,
Argentina and the north-eastern USA coast (Newman, 1963; Cuesta et al., 2004; Spivak et al., 2006;
Warkentine and Rachlin, 2010). In European estuaries, the species has spread rapidly and extensively
since its first introduction. It is now present from SW Spain to Germany and England, and in the western
Black Sea. On the Atlantic coast, the species can interact with two other commercially exploited native
species: the Atlantic ditch shrimp Palaemonetes varians (a brackish water species found mainly in non-
tidal ponds, marshes and canals with hydrological connections to estuaries) and the delta prawn Palaemon
longirostris (an estuarine species). Despite its relatively small size, P. varians is often captured for human
consumption, use as fishing bait, or use as live diet for aquaculture (Palma et al., 2008), while traditional
fishing of P. longirostris has local economic importance (Holthuis, 1980; Béguer et al., 2012). Both
native Palaemonidae can be very abundant and they occupy a central position in the estuarine trophic
network (Salgado et al., 2004), being prey of many European native and commercial fishes (e.g. the
4
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
European sea bass Dicentrarchus labrax for P. longirostris) (Salgado et al., 2004; Dauvin and Desroy,
2005).
Competitive interactions between the NIS P. macrodactylus and the native P. longirostris may be strong,
especially for space and food. Both species are estuarine with strong overlap in habitat and trophic
preferences (González-Ortegón et al., 2010; Béguer et al., 2011a). In the Guadalquivir estuary (SW
Spain), this habitat overlap is maximal in autumn during low abundance of their shared mysid prey
Mesopodopsis slabberi (González-Ortegón et al., 2006; González-Ortegón et al., 2010). Since the NIS
was first recorded, an increase in P. macrodactylus densities recorded in some European estuaries has
coincided with a decrease in density of the native P. longirostris (González-Ortegón et al., 2010; Béguer
et al., 2011a). A previous study comparing the osmoregulatory capacities of P. macrodactylus with the
two natives P. longirostris and P. varians indicates that the three species have similar osmoregulatory
capacities (González-Ortegón et al., 2006). However, oxygen consumption rates measured under different
salinities and dissolved oxygen concentrations suggested that the NIS has a more efficient metabolism
and higher tolerance to hypoxic conditions (González-Ortegón et al., 2010). However, despite field
surveys showing the salinity-related and spatial distribution patterns of these estuarine species (González-
Ortegón et al., 2006; Béguer et al., 2011a), little is known of the ecophysiology of the NIS P.
macrodactylus compared to the natives P. longirostris and P. varians, in particular regarding the
influence of temperature variations. Taking into account the climate change expected in the Euro-
Mediterranean area, the interaction between temperature and salinity might be central to the success of
NIS and to changes in status of native species (see Coccia et al., 2013 for an example from the
Guadalquivir delta).
Studying the relative performance of NIS and natives under a range of environmental conditions allows
evaluation of the likely mechanisms of a successful invasion, and testing of the physiological tolerance
5
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
hypothesis. We therefore conducted a series of three experiments to test if P. macrodactylus performs
better under extreme conditions of temperature and salinity, the two main abiotic stress factors found in
estuaries. We evaluated behavioural activity and the critical temperature maxima of different shrimp
species under an acute short-term thermal stress. We hypothesized that the NIS would show greater
resistance to acute thermal stress, reflected in a higher critical thermal maximum. We also measured
oxygen consumption under different conditions of temperature and salinity to test whether the NIS
species present lower consumption rates owing to greater resistance to environmental stressors. Finally,
we quantified survival under different chronic thermal and salinity stress to test whether the native species
had lower survival rates.
2. Material and methods
2.1. Shrimp collection and laboratory acclimation
The oriental shrimp P. macrodactylus and the delta prawn P. longirostris were collected in the
Guadalquivir estuary, SW Spain (see Figure 1) at three distinct, tidal sites S1-S3, with P. macrodactylus
was only found at site S2 (environmental parameters at each site are described in Appendix A). The
Atlantic ditch shrimp P. varians was sampled in Veta La Palma (S4 and S5), a complex of fish ponds
connected to and supplied with water from the Guadalquivir estuary (Figure 1 and Appendix A) and
protected within Doñana Natural Park, where it is abundant and harvested commercially (see Rodriguez-
Perez and Green, 2012 for details of the study site). Living individuals were collected in 2011 using
shrimp keep-nets (mesh size 4mm) placed at low tide for S1-S3 and recuperated 24h later. Size of the
shrimps was estimated by measuring the carapace length from the orbital edge of the eye to the edge of
the cephalothorax under a stereomicroscope SteREO Discovery V8 (Zeiss) using the AxioVision Rel
4.8.2 (Zeiss) software. In order to reduce catching and manipulation stress, living shrimps were
6
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
acclimated during at least 48h before any experiment in aerated aquariums with artificial saltwater at
20°C and a salinity of 5, obtained by dissolving dry sea-salt Instant Ocean (Aquarium Systems, Mentor,
Ohio) in distilled water. Salinity was measured using the Practical Salinity Scale. Aquariums were placed
in a climatic chamber (Fitoclima 10000EHHF, Aralab) on a 12h:12h dark:light photoperiod. Shrimps
were fed daily ad libitum with commercial aquarium food (gammarids) before and during all the
experiments. In order to reduce stress and injury associated with its determination, sex was characterized
after the experiments by looking for the presence or absence of the masculine appendix on the endopodite
of the second pleopod (Siegfried, 1980). A summary of size and sex ratio of the specimens used in each
experiment is given in Table 1.
2.2. Experiment 1: critical Thermal maximum (CTmax) experiment
In order to compare thermal stress resistance between the shrimp species, Critical Thermal maximum
(CTmax) experiments were conducted in May and August 2011. Carapace lengths were measured before
the experiment. The experiment was not started until at least 24h after measurements of length.
Acclimated shrimps were placed individually in a beaker filled with 200 ml of artificial water (salinity 5
and initial temperature 20 ºC) and capped with a transparent lid to allow observation throughout the
experiment. The beaker was placed in a water bath with a magnetic stirrer allowing rapid homogenisation
of surrounding water. Temperature was monitored every minute with an electronic thermometer (model
SA880SSX, Oregon Scientific) and a temperature ramp of 1°C.min-1 was applied as in Ravaux et al.
(2012).
During the experiment, behavioral activity of each individual shrimp was continuously monitored over 30
s periods until reaching the end-point when the shrimp lay on its side or its posterior face for more than
30 s. We subdivided behaviour into four categories based on previous literature (Ravaux et al., 2003;
Shillito et al., 2006; Oliphant et al., 2011): ‘Movement’: any kind of motion of the animal except for
7
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
active movement (see below): pereopods or pleopods movements, antennal lateral sweeping on the dorsal
side, cleaning of mouth parts by rubbing them together; ‘Active movement’: when shrimps moved a
distance (either by walking or swimming) exceeding their own length in less than 30 seconds; ‘Loss Of
Equilibrium’ (LOE): shrimp on the bottom of the beaker in either an ‘upside-down' or a 'sideways'
position for more than 2 seconds; ‘Spasmodic motions or spasms’: vibrations of the pleopods and/or
sudden contraction of the abdomen.
The CTmax was determined as the temperature at which coordinated movements were lost, using LOE as
the reference parameter. The CTmax was calculated for a total number of 20 individuals per species for P.
macrodactylus and P. varians, and 18 individuals for P. longirostris.
2.3. Experiment 2: oxygen consumption rate
In order to compare oxygen consumption under different temperatures and salinities, we performed two
series of treatments with varying temperatures (20°C, 25°C and 30°C at a constant salinity of 5) and
salinities (salinity of 5, 15, 25, 35 and 45, at constant 20°C) respectively in May 2011 (9-10 shrimps per
treatment for P. longirostris and P. varians, and 5 shrimps per treatment for P. macrodactylus). Each
shrimp was weighted 24h before experiment with a Voyager analytical balance (Ohaus) after removal of
excess water using blotting paper. In order to avoid any heat shock when moving shrimps from their
original aquarium (20°C at salinity 5) to aquariums with higher temperatures, they were acclimated
overnight prior to the experiments by gradually increasing temperature (2°C.h -1) or salinity (10 salinity
units.h-1) depending on the treatment. Temperature within each treatment was maintained within ± 0.2°C
using a heater (Jäger 300; Eheim) controlled by a Biotherm Pro (Hobby) temperature regulator.
To measure oxygen consumption rate (OCR), shrimps were put into cylindrical flasks (12.3 mL) and the
flow rate of water circulating in each flask was measured. The difference between oxygen concentrations
in water at the entrance and exit of the flasks was recorded using a 10-channel OXY-10 mini (PreSens)
8
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
fiber optic oxygen transmitter connected to a computer with the OXY10v3_33 software. OCR was
calculated according to the formula: OCR = F × ([O2]in – [O2]out)/BW, where OCR is oxygen consumption
rate (mg O2.gwwt-1.h-1), F is water flow rate (L.h-1) circulating in each flask, [O2]in is oxygen content of
the water inflow (mg O2.L-1), [O2]out is oxygen content of the water outflow (mg O2.L-1), and BW is wet
mass (g).
2.4. Experiment 3: comparative survival of P. longirostris and P. macrodactylus under chronic stress
Shrimps were placed individually in small, closed plastic aquaria (0.35L) with a 1mm mesh sieve at the
bottom and placed within 91L experimental aquaria.
Acclimatised shrimps were reared in different 91L aquaria at three different temperatures (20°C, 24°C
and 28°C, with a constant salinity of 5) and three different salinities (5, 25, and 45, with a constant
temperature of 20°C) during 28 days. As environmental parameters are constantly varying in an estuary,
especially salinity that has tide-based regime, submitting estuarine organisms to constant salinity or
temperature as here represents thus a chronic stress. Shrimp size and weight were measured twice a week
and survival was checked daily.
Experiments were conducted in October 2011 when both species were caught at the same time and place.
The experiment was repeated twice (15 day interval between sampling) on both species (8 individuals per
treatment for both P. longirostris and P. macrodactylus and per sampling time).
2.5. Statistical analysis
All statistical analyses were performed using R 2.15.2 (R Core Team, 2012). The CTmax data were not
normally distributed, even after transformations (Shapiro-Wilk’s test, p<0.001) and had unequal variances
(Bartlett test, p<0.001). These data were therefore analysed using the non-parametric Kruskal-Wallis
ANOVA and Wilcoxon-Mann-Whitney tests. However, for oxygen consumption data, a parametric
9
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
ANOVA was performed, after data transformation when necessary. The post-hoc Tukey HSD test was
used to compare treatments. Survival analysis were performed with the Survival package in R (Therneau
and Lumley, 2009) using Kaplan-Maier estimates and log-rank tests.
3. Results
3.1. Experiment 1: behavioral analysis and Critical Thermal maximum (CTmax) experiment
P. macrodactylus was collected at only one site (S2) in the estuary (Fig. 1). In contrast, P. longirostris
was collected at the three sampling sites in the Guadalquivir River (Fig. 1), representing a decreasing
salinity gradient from S1 to S3.
Due to density variations at each sampling site, the experiment was conducted on 9, 7 and 2 individuals of
P. longirostris. sampled the same day at sites S1, S2 and S3 respectively. We pooled the different sites
into one group for further comparative analysis as no statistical differences were found among sites
(Kruskal-Wallis test, p=0.37 and p=0.82 for the CTmax and temperature at first spasmodic motion
respectively).
In the same manner, P. varians was sampled at two sites (S4 and S5; Fig. 1) differing in salinity. The
experiment was conducted on 10 individuals from each site. No statistical differences were found for the
CTmax and for the temperature at first spasmodic motion between the two sites (Wilcoxon-Mann-Whitney
test, p=0.15 and p=0.17 respectively). Hence, we pooled the two sites for further analysis.
Despite identical pre-experimental acclimation conditions, at the start of the experiment, no P.
longirostris individual was presenting an active motion, whereas 60% and 20% of P. varians and P.
macrodactylus, respectively were presenting an active motion (Fig. 2). The temperatures at which 50% of
individuals were actively moving were reached earlier for P. varians (20.0 ºC) and P. macrodactylus
(22.0 ºC) than for P. longirostris (24.6 ºC). The maximal number of individuals presenting active
10
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
movements was reached as early as ca. 28 ºC for P. longirostris, compared to ca. 33 ºC and ca. 32.0 ºC
for P. varians and P. macrodactylus respectively. Moreover, the active moving curves closely preceded
the loss of equilibrium (LOE) curves (Fig. 2). In the case of P. varians and P. macrodactylus, the LOE
and spasms curves were closer together. As a consequence, LOE was observed at much lower
temperature for P. longirostris (mean CTmax ± SE = 27.24 ºC ± 2.16) compared to P. varians (mean CTmax
± SE = 31.71 ºC ± 2.21) and P. macrodactylus (mean CTmax ± SE = 33.0 ºC ± 1.11)(Fig. 2 and 3). The
CTmax values were significantly different between species (Kruskal-Wallis test, H=33.3276, df=2,
p<0.001), with all pairwise comparisons between the three species being significantly different
(Wilcoxon-Mann-Whitney test, p<0.001).
For individuals used in the above experiments, information about size and sex ratio of the different
samples have been gathered into Table 1. When considering each species separately, there was no effect
of size (Spearman rank correlation, p>0.15) or sex on LOE values (Kruskal-Wallis test, p>0.05).
3.2. Experiment 2: oxygen consumption rate
In the salinity experiment, OCR values were significantly different between species and salinity
treatments (four-way ANOVA, F8,109=15.58, p<0.001) without effects of sex or size (see detailed value of
these parameters in Table 1). The significant differences between species were due to lower OCRs of P.
macrodactylus compared with the two native species (post hoc Tukey HSD test, p<0.001), which did not
differ between them (post hoc Tukey HSD test, p=0.075). Whatever the salinity treatment, P. varians had
the highest OCR values and P. macrodactylus the lowest (Fig. 4).
The significant effect of salinity treatment reflected an increase in OCR with salinity (Fig. 4), for all
species (134%, 186% and 236% increase for Palaemonetes varians, P. longirostris, and P. macrodactylus
respectively, between the lowest and highest treatments). In the case of P. longirostris, which presented
intermediate OCR values, OCR was significantly lower at the lowest salinity treatment (salinity 5) than at
11
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
all others. Low salinity effects were more gradual for the other two species (Fig. 4).
In the temperature experiment, OCRs were significantly different between species and temperature
treatments (four-way ANOVA, F6,65=21.30, p<0.001) without effects of sex or size (see Table 1 for details
on values of these parameters). All pairwise species differences were significant (post hoc Tukey HSD
tests, p<0.015). As for the salinity experiment, P. macrodactylus had the lowest OCR, and P. varians the
highest. OCR increased significantly with increasing temperature for all species (Fig. 4; 183%, 257% and
200% increase for Palaemonetes varians, P. longirostris, and P. macrodactylus respectively, between the
lowest and highest treatments).
3.3. Experiment 3: comparative survival of P. longirostris and P. macrodactylus under chronic stress
We did not find any significant effect of sampling date for P. macrodactylus (log-rank test, χ2=0, df=1,
p=0.923) or P. longirostris (log-rank test, χ2=0, df=1, p=0.989) on survival rate at different salinities.
Likewise, no significant effect of the date of sampling was found in the temperature experiment (P.
macrodactylus, log-rank test, χ2=0, df=1, p=0.946; P. longirostris, log-rank test, χ2=0, df=1, p=0.993).
Thus, samples from different dates were pooled for further analyses. In the treatment 20 ºC-salinity 5 that
provided the least stressful conditions, only one individual (P. macrodactylus) showed a premature death
(two weeks before the end of the experiment). No significant size differences was found between the two
shrimp species in each of the treatment (see Table 1).
Survival curves of both species according to salinity are shown in Fig. 5. There was a significant effect of
salinity treatment on the survival of P. macrodactylus (log-rank test, χ2=54.0, df=2, p<0.001) and of P.
longirostris (log-rank test, χ2=41.3, df=2, p<0.001). No significant difference was found between the two
species when comparing their general survival trend according to salinity (log-rank test, χ 2=1, df=1,
12
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
p=0.308): the higher the salinity, the lower the survival (Fig. 5). However, when comparing survival of
both species in detail at each salinity treatment, significant interspecific differences were noted only at the
high salinity of 45 (log-rank test, χ2=8.6, df=1, p=0.00338).
In the temperature experiment (Fig. 5), no significant effect of temperature was found on survival of P.
macrodactylus (log-rank test, χ2=1.2, df=2, p=0.555), despite a slight increase of mortality with increasing
temperature (Fig. 5). However for P. longirostris, temperature had a significant effect (log-rank test,
χ2=19.4, df=2, p<0.001), the highest temperature (28 ºC) being the only one to induce mortality (50% of
individuals dead by the end of the experiment; Fig. 5). The general trend for survival with temperature
was not significantly different between the two species (log-rank test, χ2=0.3, df=1, p=0.570). However, a
marginally significant difference in survival could be noted between the two species at 28 ºC (log-rank
test, χ2=3.8, df=1, p=0.051).
4. 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 (but see González-Ortegón et al., 2006; González-Ortegón et al., 2010).
In the case of P. macrodactylus and P. longirostris, they were even syntopic and congeneric.
4.1. 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
13
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
related, native species and NIS under identical experimental conditions has rarely been adopted (but see
Coccia et al., 2013). 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 (Nielsen and Hagerman, 1998; Gelin and Souty-Grosset, 2006; González-Ortegón and
Cuesta, 2006; Ravaux et al., 2012). The delta prawn P. longirostris is strictly estuarine, present in all the
NE Atlantic (Bah et al., 2006; Béguer et al., 2010). 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 (Campbell and Jones, 1989; González-
Ortegón and Cuesta, 2006; Béguer et al., 2011b).
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 (Baldó et al., 2005; González-Ortegón et al., 2006; Navarro et al.,
2011; García-Lafuente et al., 2012). 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
14
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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 (e.g. M.
acanthurus 34.2 ºC ± 0.48; Díaz et al.). 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 (Oliphant et al. (2011). More interestingly, the CTmax of P. macrodactylus is
closer to that of its Euro-Mediterranean euryoecious temperate congener P. serratus (31-37ºC for
acclimation temperatures in the natural range 14-25ºC; details in Richard, 1978; Oliphant et al., 2011). 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
(Oliphant et al., 2011; Ravaux et al., 2012). 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 (respectively 30.9ºC ± 1.0 and 35.9ºC ± 0.6; Ravaux et al., 2012). 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, Madeira et al. (2012) 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
15
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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
(Lutterschmidt and Hutchison, 1997). 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
(Shillito et al., 2006). 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
(Hopkin et al., 2006; Ravaux et al., 2012; Somero, 2012). Adequate interspecific comparisons can
however be made through experiments that use the same behavioral parameters and similar heating rates
(Shillito et al., 2006) as in Madeira et al. (2012) or in the present study.
4.2. 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 (González-Ortegón et al.,
2010). P. macrodactylus was shown to be much more tolerant than P. longirostris under stressful hypoxic
16
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
conditions which, associated with the present eutrophication of estuaries in Europe, might help the NIS to
outcompete its native congener (González-Ortegón et al., 2010). 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 (Lenz et al., 2011;
Maazouzi et al., 2011; Morosawa, 2011). 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 (Angilletta, 2009), such increases are quite common and were previously recorded for
congeners such as Palaemonetes pugio, Palaemon peringueyi or Palaemon pacificus (Allan et al., 2006;
Oliphant et al., 2011; Purcell et al., 2013; Vilibić et al., 2013). 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 (González-
Ortegón et al., 2010). A similar pattern was also found previously for P. varians (Lofts, 1956), and is
quite common for decapod shrimps and other invertebrates (see for example Allan et al., 2006; Lenz et
al., 2011; Oliphant et al., 2011). 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.
4.3. 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.
17
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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 (Boonstra and Fox, 2013). 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 (Walther
et al., 2009). 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 (Lejeusne
et al., 2010; del Río et al., 2011; Philippart et al., 2011; Albouy et al., 2013). 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 (Stachowicz et al.,
2002; Walther et al., 2009; Burrows et al., 2011; Maclean and Wilson, 2011; Zerebecki and Sorte, 2011;
Madeira et al., 2012).
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
18
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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 (González-Ortegón et al., 2006; González-
Ortegón et al., 2010; Béguer et al., 2011a). 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 (González-Ortegón et al., 2010; Béguer et al., 2011a). 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 (González-Ortegón and Cuesta, 2006; González-Ortegón et al., 2010; Béguer et al., 2011a).
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 (Béguer et al., 2011a). 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.
.
4.4. Concluding remarks
We found that the NIS was more tolerant to rapid increase in temperature than the two native species, and
19
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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 Zerebecki and Sorte
(2011) 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 (Zerebecki
and Sorte, 2011). 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 (Roman and Darling, 2007; Simberloff,
2009). However, during pre- and post-establishment, NIS have to pass through a series of abiotic filters to
become introduced, then invasive (see Blackburn et al., 2011). Species presenting broader physiological
tolerances may thus be more able to survive and establish (Zerebecki and Sorte, 2011). 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 (Lejeusne et al., 2010; Durrieu de
Madron et al., 2011). 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 (see Lejeusne et al., 2010; Burrows et al., 2011; Zerebecki and Sorte, 2011). 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
20
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
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).
21
1
2
3
4
5
6
7
8
9
10
11
12
13
1
References
Albouy, C., Guilhaumon, F., Leprieur, F., Lasram, F.B.R., Somot, S., Aznar, R., Velez, L., Le Loc'h, F., Mouillot, D., Pearman, P., 2013. Projected climate change and the changing biogeography of coastal Mediterranean fishes. Journal of Biogeography 40, 534-547.
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. Oxford University Press, Oxford, UK, 304 pp.
Bah, F., Balde, A., Camara, M., Doumbouya, F., 2006. Bio-écologie et exploitation de Palaemon longirostris dans la zone littorale de Conakry. Bulletin du Centre Halieutique de Boussoura 1, 17-21.
Baldó, F., Cuesta, J.A., Fernández Delgado, C., Drake, P., 2005. Effect of the regulation of the freshwater inflow of the Gualdaquivir River on the physical-chemical characteristics of water and on the aquatic macrofauna in the Guadalquivir estuary. Ciencias Marinas 31, 467-476.
Barnosky, A.D., Hadly, E.A., Bascompte, J., Berlow, E.L., Brown, J.H., Fortelius, M., Getz, W.M., Harte, J., Hastings, A., Marquet, P.A., Martinez, N.D., Mooers, A., Roopnarine, P., Vermeij, G., Williams, J.W., Gillespie, R., Kitzes, J., Marshall, C., Matzke, N., Mindell, D.P., Revilla, E., Smith, A.B., 2012. Approaching a state shift in Earth's biosphere. Nature 486, 52-58.
Béguer, M., Bergé, J., Gardia-Parège, C., Beaulaton, L., Castelnaud, G., Girardin, M., Boët, P., 2012. Long-Term Changes in Population Dynamics of the Shrimp Palaemon longirostris in the Gironde Estuary. Estuaries and Coasts 35, 1082-1099.
Béguer, M., Bergé, J., Girardin, M., Boët, P., 2010. Reproductive Biology of Palaemon longirostris (Decapoda: Palaemonidae) from Gironde Estuary (France), with a Comparison with Other European Populations. Journal of Crustacean Biology 30, 175-185.
Béguer, M., Bergé, J., Martin, J., Martinet, J., Pauliac, G., Girardin, M., Boët, P., 2011a. Presence of Palaemon macrodactylus in a European estuary: evidence for a successful invasion of the Gironde (SW France). Aquatic Invasions 6, 401-418.
Béguer, M., Rochette, S., Girardin, M., Boët, P., 2011b. Growth Modeling and Spatio-Temporal Variability in the Body Condition of the Estuarine Shrimp Palaemon longirostris in the Gironde (Sw France). Journal of Crustacean Biology 31, 606-612.
Blackburn, T.M., Pysek, P., Bacher, S., Carlton, J.T., Duncan, R.P., JarosÌk, V., Wilson, J.R.U., Richardson, D.M., 2011. A proposed unified framework for biological invasions. Trends in Ecology & Evolution 26, 333-339.
Boonstra, R., Fox, C., 2013. Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Functional Ecology 27, 11-23.
Burgiel, S.W., Muir, A.A., 2010. Invasive Species, Climate Change and Ecosystem-Based Adaptation: Addressing Multiple Drivers of Global Change. Global Invasive Species Programme (GISP), Washington, DC, US, and Nairobi, Kenya, p. 56.
Burrows, M.T., Schoeman, D.S., Buckley, L.B., Moore, P., Poloczanska, E.S., Brander, K.M., Brown, C., Bruno, J.F., Duarte, C.M., Halpern, B.S., Holding, J., Kappel, C.V., Kiessling, W., O'Connor, M.I., Pandolfi, J.M., Parmesan, C., Schwing, F.B., Sydeman, W.J., Richardson, A.J., 2011. The pace of shifting climate in marine and terrestrial ecosystems. Science 334, 652-655.
Campbell, P.J., Jones, M.B., 1989. Osmoregulation of the estuarine prawn Palaemon longirostris (Caridea, Palaemonidae). Journal of the Marine Biological Association of the U. K. 69, 261-272.
Catford, J.A., Jansson, R., Nilsson, C., 2009. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Diversity and Distributions 15, 22-40.
Coccia, C., Calosi, P., Boyero, L., Green, A.J., Bilton, D.T., 2013. Does ecophysiology determine invasion success? A comparison between the invasive boatman Trichocorixa verticalis verticalis and the native Sigara lateralis (Hemiptera, Corixidae) in south-west Spain. PLoS One 8, e63105.
Cohen, A.N., Carlton, J.T., 1998. Accelerating invasion rate in a highly invaded estuary. Science 279, 555-558.
22
1
23456789
1011121314151617181920212223242526272829303132333435363738394041424344454647484950
1
Cuesta, J.A., González-Ortegón, E., Drake, P., Rodríguez, A., 2004. First record of Palaemon macrodactylus Rathbun, 1902 (Decapoda, Caridea, Palaemonidae) from European waters. Crustaceana 77 377-380.
Dauvin, J.-C., Desroy, N., 2005. The food web in the lower part of the Seine estuary: a synthesis of existing knowledge. Hydrobiologia 540, 13-27.
del Río, S., Herrero, L., Pinto-Gomes, C., Penas, A., 2011. Spatial analysis of mean temperature trends in Spain over the period 1961-2006. Global and Planetary Change 78, 65-75.
Díaz, F., Sierra, E., Re, A.D., Rodrı́guez, L., 2002. Behavioural thermoregulation and critical thermal limits of Macrobrachium acanthurus (Wiegman). Journal of Thermal Biology 27, 423-428.
Dukes, J.S., Mooney, H.A., 1999. Does global change increase the success of biological invaders? Trends in Ecology & Evolution 14, 135-139.
Durrieu de Madron, X., Guieu, C., Sempéré, R., Conan, P., Cossa, D., D’Ortenzio, F., Estournel, C., Gazeau, F., Rabouille, C., Stemmann, L., Bonnet, S., Diaz, F., Koubbi, P., Radakovitch, O., Babin, M., Baklouti, M., Bancon-Montigny, C., Belviso, S., Bensoussan, N., Bonsang, B., Bouloubassi, I., Brunet, C., Cadiou, J.F., Carlotti, F., Chami, M., Charmasson, S., Charrière, B., Dachs, J., Doxaran, D., Dutay, J.C., Elbaz-Poulichet, F., Eléaume, M., Eyrolles, F., Fernandez, C., Fowler, S., Francour, P., Gaertner, J.C., Galzin, R., Gasparini, S., Ghiglione, J.F., Gonzalez, J.L., Goyet, C., Guidi, L., Guizien, K., Heimbürger, L.E., Jacquet, S.H.M., Jeffrey, W.H., Joux, F., Le Hir, P., Leblanc, K., Lefèvre, D., Lejeusne, C., Lemé, R., Loÿe-Pilot, M.D., Mallet, M., Méjanelle, L., Mélin, F., Mellon, C., Mérigot, B., Merle, P.L., Migon, C., Miller, W.L., Mortier, L., Mostajir, B., Mousseau, L., Moutin, T., Para, J., Pérez, T., Petrenko, A., Poggiale, J.C., Prieur, L., Pujo-Pay, M., Pulido, V., Raimbault, P., Rees, A.P., Ridame, C., Rontani, J.F., Ruiz Pino, D., Sicre, M.A., Taillandier, V., Tamburini, C., Tanaka, T., Taupier-Letage, I., Tedetti, M., Testor, P., Thébault, H., Thouvenin, B., Touratier, F., Tronczynski, J., Ulses, C., Van Wambeke, F., Vantrepotte, V., Vaz, S., Verney, R., 2011. Marine ecosystems’ responses to climatic and anthropogenic forcings in the Mediterranean. Progress In Oceanography 91, 97-166.
García-Lafuente, J., Delgado, J., Navarro, G., Calero, C., Díez-Minguito, M., Ruiz, J., Sánchez-Garrido, J.C., 2012. About the tidal oscillations of temperature in a tidally driven estuary: The case of Guadalquivir estuary, southwest Spain. Estuarine, Coastal and Shelf Science 111, 60-66.
Gelin, A., Souty-Grosset, C., 2006. Species identification and ecological study of the genus Palaemonetes (Decapoda : Caridea) in the French Mediterranean. Journal of Crustacean Biology 26, 124-133.
González-Ortegón, E., Cuesta, J., Pascual, E., Drake, P., 2010. Assessment of the interaction between the white shrimp, Palaemon longirostris, and the exotic oriental shrimp, Palaemon macrodactylus, in a European estuary (SW Spain). Biological Invasions 12, 1731-1745.
González-Ortegón, E., Cuesta, J.A., 2006. An illustrated key to species of Palaemon and Palaemonetes (Crustacea : Decapoda : Caridea) from European waters, including the alien species Palaemon macrodactylus. Journal of the Marine Biological Association of the U. K. 86, 93-102.
González-Ortegón, E., Pascual, E., Cuesta, J.A., Drake, P., 2006. Field distribution and osmoregulatory capacity of shrimps in a temperate European estuary (SW Spain). Estuarine Coastal and Shelf Science 67, 293-302.
Grosholz, E., 2002. Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution 17 22-27.
Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F., D'Agrosa, C., Bruno, J.F., Casey, K.S., Ebert, C., Fox, H.E., Fujita, R., Heinemann, D., Lenihan, H.S., Madin, E.M.P., Perry, M.T., Selig, E.R., Spalding, M., Steneck, R., Watson, R., 2008. A global map of human impact on marine ecosystems. Science 319, 948-952.
Hellmann, J.J., Byers, J.E., Bierwagen, B.G., Dukes, J.S., 2008. Five potential consequences of climate change for invasive species. Conservation biology : the journal of the Society for Conservation Biology 22, 534-543.
Holthuis, L.B., 1980. FAO species Catalogue. Vol. 1. Shrimps and prawns of the world. An annoted catalogue of species of interest to fisheries., FAO Fisheries Synopsis. FAO, Roma, Italy, p. 271.
Hopkin, R.S., Qari, S., Bowler, K., Hyde, D., Cuculescu, M., 2006. Seasonal thermal tolerance in marine Crustacea. Journal of Experimental Marine Biology and Ecology 331, 74-81.
Hufbauer, R.A., Torchin, M.E., 2007. Integrating Ecological and Evolutionary Theory of Biological Invasions, in: Nentwig, W. (Ed.), Biological Invasions - Ecological Studies. Springer-Verlag, Berling Heidelberg, pp. 79-96.
Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution 25, 250-260.
23
123456789
10111213141516171819202122232425262728293031323334353637383940414243444546474849505152
1
Lenz, M., da Gama, B.A., Gerner, N.V., Gobin, J., Groner, F., Harry, A., Jenkins, S.R., Kraufvelin, P., Mummelthei, C., Sareyka, J., Xavier, E.A., Wahl, M., 2011. Non-native marine invertebrates are more tolerant towards environmental stress than taxonomically related native species: results from a globally replicated study. Environmental research 111, 943-952.
Lofts, B., 1956. The effects of salinity changes on the respiratory rates of the prawn Palaemonetes varians (Leach). Journal of Experimental Biology 33, 730-736.
Lutterschmidt, W.I., Hutchison, V.H., 1997. The critical thermal maximum: history and critique. Canadian Journal of Zoology 75, 1561-1574.
Maazouzi, C., Piscart, C., Legier, F., Hervant, F., 2011. Ecophysiological responses to temperature of the "killer shrimp" Dikerogammarus villosus: is the invader really stronger than the native Gammarus pulex? Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 159, 268-274.
Maclean, I.M.D., Wilson, R.J., 2011. Recent ecological responses to climate change support predictions of high extinction risk. Proceedings of the National Academy of Sciences 108, 12337-12342.
Madeira, D., Narciso, L., Cabral, H.N., Vinagre, C., 2012. Thermal tolerance and potential impacts of climate change on coastal and estuarine organisms. Journal of Sea Research 70, 32-41.
McMahon, R.F., 2002. Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Canadian Journal of Fisheries and Aquatic Sciences 59, 1235-1244.
Morosawa, T., 2011. Hypoxia tolerance of three native and three alien species of bitterling inhabiting Lake Kasumigaura, Japan. Environmental Biology of Fishes 91, 145-153.
Navarro, G., Gutiérrez, F.J., Díez-Minguito, M., Losada, M.A., Ruiz, J., 2011. Temporal and spatial variability in the Guadalquivir estuary: a challenge for real-time telemetry. Ocean Dynamics 61, 753-765.
Nentwig, W., 2007. Biological Invasions, Ecological Studies. Springer, Berlin, Germany, p. 446.Newman, W.A., 1963. On the introduction of an edible oriental shrimp (Caridea, Palaemonidae) to San Francisco
Bay. Crustaceana 5, 119-132.Nielsen, A., Hagerman, L., 1998. Effects of short-term hypoxia on metabolism and haemocyanin oxygen transport
in the prawns Palaemon adspersus and Palaemonetes varians. Marine Ecology Progress Series 167, 177-183.Oliphant, A., Thatje, S., Brown, A., Morini, M., Ravaux, J., Shillito, B., 2011. Pressure tolerance of the shallow-
water caridean shrimp Palaemonetes varians across its thermal tolerance window. Journal of Experimental Biology 214, 1109-1117.
Palma, J., Bureau, D.P., Andrade, J.P., 2008. Effects of binder type and binder addition on the growth of juvenile Palaemonetes varians and Palaemon elegans (Crustacea: Palaemonidae). Aquaculture International 16, 427-436.
Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37, 637-669.
Philippart, C.J.M., AnadÛn, R., Danovaro, R., Dippner, J.W., Drinkwater, K.F., Hawkins, S.J., Oguz, T., O'Sullivan, G., Reid, P.C., 2011. Impacts of climate change on European marine ecosystems: Observations, expectations and indicators. Journal of Experimental Marine Biology and Ecology 400, 52-69.
Purcell, S.W., Mercier, A., Conand, C., Hamel, J.-F., Toral-Granda, M.V., Lovatelli, A., Uthicke, S., 2013. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish and Fisheries 14, 34-59.
R Core Team, 2012. R: A language and environment for statistical computing. R Foundation for Statisical Computing, Vienna, Austria.
Rahel, F.J., Bierwagen, B., Taniguchi, Y., 2008. Managing aquatic species of conservation concern in the face of climate change and invasive species. Conservation biology : the journal of the Society for Conservation Biology 22, 551-561.
Ravaux, J., Gaill, F., Le Bris, N., Sarradin, P.M., Jollivet, D., Shillito, B., 2003. Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. Journal of Experimental Biology 206, 2345-2354.
Ravaux, J., Leger, N., Rabet, N., Morini, M., Zbinden, M., Thatje, S., Shillito, B., 2012. Adaptation to thermally variable environments: capacity for acclimation of thermal limit and heat shock response in the shrimp Palaemonetes varians. Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology 182, 899-907.
Reise, K., Olenin, S., Thieltges, D.W., 2006. Are aliens threatening European aquatic coastal ecosystems? Helgoland Marine Research 60, 77-83.
24
123456789
1011121314151617181920212223242526272829303132333435363738394041424344454647484950515253
1
Richard, P., 1978. Tolérance aux températures extrêmes de Palaemon serratus (Pennant): influence de la taille et de l'acclimatation. Journal of Experimental Marine Biology and Ecology 35, 137-146.
Richardson, D., Pysek, P., 2008. Fifty years of invasion ecology - the legacy of Charles Elton. Diversity and Distributions 14, 161-168.
Rodriguez-Perez, H., Green, A.J., 2012. Strong seasonal effects of waterbirds on benthic communities in shallow lakes. Freshwater Science 31, 1273-1288.
Roman, J., Darling, J.A., 2007. Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution 22, 454-464.
Ruiz, G.M., Carlton, J.T., Grosholz, E.D., Hines, A.H., 1997. Global invasions of marine and estuarine habitats by non-indigenous species: Mechanisms, extent, and consequences. American Zoologist 37, 621-632.
Salgado, J., Cabral, H., Costa, M., Deegan, L., 2004. Nekton use of salt marsh creeks in the upper Tejo estuary. Estuaries 27, 818-825.
Sax, D.F., Stachowicz, J.J., Brown, J.H., Bruno, J.F., Dawson, M.N., Gaines, S.D., Grosberg, R.K., HastingS, A., Holt, R.D., Mayfield, M.M., O'Connor, M.I., Rice, W.R., 2007. Ecological and evolutionary insights from species invasions. Trends in Ecology & Evolution 22, 465-471.
Shillito, B., Le Bris, N., Hourdez, S., Ravaux, J., Cottin, D., Caprais, J.C., Jollivet, D., Gaill, F., 2006. Temperature resistance studies on the deep-sea vent shrimp Mirocaris fortunata. Journal of Experimental Biology 209, 945-955.
Siegfried, C.A., 1980. Seasonal abundance and distribution of Crangon fransciscorum and Palaemon macrodactylus (Decapoda, Caridea) in the San Francisco Bay-Delta. Biological Bulletin 159, 177-192.
Simberloff, D., 2009. The Role of Propagule Pressure in Biological Invasions. Annual Review of Ecology, Evolution, and Systematics 40, 81-102.
Somero, G.N., 2012. The Physiology of Global Change: Linking Patterns to Mechanisms. Annual Review of Marine Science 4, 39-61.
Spivak, E.D., Boschi, E.E., Martorelli, S.R., 2006. Presence of Palaemon macrodactylus Rathbun 1902 (Crustacea : Decapoda : Caridea : Palaemonidae) in Mar del Plata harbor, Argentina: first record from southwestern Atlantic waters. Biological Invasions 8, 673-676.
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B., Osman, R.W., 2002. Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. Proceedings of the National Academy of Sciences 99 15497-15500.
Therneau, T., Lumley, T., 2009. A Package for Survival Analysis in R, R package version 2.36-14. ed.Vilibić, I., Šepić, J., Proust, N., 2013. Weakening thermohaline circulation in the Adriatic Sea. Climate Research 55,
217-225.Walther, G.-R., Roques, A., Hulme, P.E., Sykes, M.T., Pysek, P., Kuhn, I., Zobel, M., Bacher, S., Botta-Dukat, Z.,
Bugmann, H., Czucz, B., Dauber, J., Hickler, T., Jarosik, V., Kenis, M., Klotz, S., Minchin, D., Moora, M., Nentwig, W., Ott, J., Panov, V.E., Reineking, B., Robinet, C., Semenchenko, V., Solarz, W., Thuiller, W., Vila, M., Vohland, K., Settele, J., 2009. Alien species in a warmer world: risks and opportunities. Trends in Ecology & Evolution 24, 686-693.
Warkentine, B.E., Rachlin, J.W., 2010. The First Record of Palaemon macrodactylus (Oriental Shrimp) from the Eastern Coast of North America. NorthEastern Naturalist 17, 91-102.
Wasson, K., Zabin, C., Bedinger, L., Diaz, M., Pearse, J., 2001. Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biological Conservation 102, 143-153.
Zerebecki, R.A., Sorte, C.J.B., 2011. Temperature Tolerance and Stress Proteins as Mechanisms of Invasive Species Success. PLoS One 6, e14806.
25
123456789
101112131415161718192021222324252627282930313233343536373839404142434445
1
Table 1: Summary of treatments applied in the different experiments with initial experimental conditions and size and sex ratio of the shrimps. T: temperature; S: salinity; PL: Palaemon longirostris (native); PV: Palaemonetes varians (native); PM: Palaemon macrodactylus (non indigenous); F: female; M: male; SD: standard deviation; SE: standard error. Different uppercase letters indicate statistical significant differences (Wilcoxon-Mann-Whitney test with p<0.05), while an asterisk indicates divergence from an equal sex-ratio (Chi-squared test with p<0.05).
Experiment (number)
Initial conditions Treatments
Specimen carapace length Specimen sex ratio
(F/M)Mean Size range
CTmax (1) T = 20ºCS = 5 +1ºC.min-1 until spasms
PL 12.44a mm (± 1.37 SD)PV 5.82b mm (± 1.10, SD)PM 5.49b mm (± 1.00, SD)
8.98-14.26 mm4.50-8.22 mm4.05-8.35 mm
3.5*
1.221.86
Oxygen consumption
rate (2)
T = 20ºCS = 5
1h at T = 20, 25, or 30ºCPL 6.19c mm (± 0.12, SE)PV 5.69d mm (± 0.20, SE)PM 6.32cd mm (± 0.33, SE)
5.06-7.86 mm3.76-8.08 mm4.44-8.86 mm
3.67*
1.641.50
1h at S=5, 15, 25, 35, 45 PL 6.08e mm (± 0.09, SE)PV 6.01e mm (± 0.20, SE)PM 5.88e mm (± 0.28, SE)
4.47-7.34 mm3.76-8.87 mm3.90-8.68 mm
4.44*
3.70*
1.44
Comparative survival under chronic stress
(3)
T = 20ºCS = 5
4 weeks at 20, 24, 28ºC PL 6.76f mm (± 1.73, SD)PM 6.57f mm (±1.70, SD)
4.32-12.06 mm4.51-12.36 mm
NA
4 weeks at S=5, 25, 45 PL 6.69g mm (± 1.82, SD)PM 6.30g mm (±1.36, SD)
3.70-12.06 mm4.51-10.19 mm
26
123456789
10111213141516171819202122
1
27
1
1
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.
28
12
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
1
Figure 1
Sampling locations in the Guadalquivir estuary, south-west Spain. Sampling points are indicated by black dots.
29
1234
5
1
Fig. 2
Distribution of behavioral categories of the three palaemonid shrimps (lower figures) according to temperature increase (upper). Moving: empty circles;
active moving: black filled circles; loss of equilibrium (LOE): black filled triangles; spasms: black filled squares. Note the change of scale for the
horizontal and vertical axes.
30
12
3
4
5
6
7
8
1
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.
31
12
3
4
5
6
7
1
Figure 4
Oxygen consumption rates according to salinity (left) and temperature (right) for P. macrodactylus (circles), P. longirostris (squares) and P. varians (triangles). For each species, values with different letters are significantly different.
32
1
23
4
5
6
1
Figure 5
Kaplan–Meier survival estimates (filled lines) with 95% confidence bounds (dashed lines) for Palaemon macrodactylus (PM) and Palaemon longirostris (PL) under different conditions of temperature and salinity.
33
1
23
4
1
Appendix A: Temperature, salinity, and pH monitored at the five sampling sites (S1-S5) during one year
in 2011-2012.
34
1
2
3
4
1
