# Thermal tolerance and vulnerability to climate warming in the freshwater shrimp Atyaephyra desmarestii and Caridina multidentata

Juliette Ravaux, Olivia Bosc, Charles-Edouard Fusari, Sara-Mae Gricourt, Maria Itin, Michel Lestin, Valentin de Mazancourt

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Juliette Ravaux, Olivia Bosc, Charles-Edouard Fusari, Sara-Mae Gricourt, Maria Itin, et al. Thermal tolerance and vulnerability to climate warming in the freshwater shrimp Atyaephyra desmarestii and Caridina multidentata. Journal of Thermal Biology, 2025, 129, pp.104121. 10.1016/j.jtherbio.2025.104121. hal-05072935

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# Thermal tolerance and vulnerability to climate warming in the freshwater shrimp *Atyaephyra desmarestii* and *Caridina multidentata*

Juliette Ravaux<sup>a,*</sup>,<sup>†</sup> Oliva Bosc<sup>a</sup>, Charles-Edouard Fusari<sup>b,1</sup>, Sara-Mae Gricourt<sup>b,1</sup>,
Maria Itin<sup>a</sup>, Michel Lestin<sup>b,1</sup>, Valentin de Mazancourt<sup>a</sup>

## ARTICLE INFO

Keywords:
Crustacea
Caridea
Thermal limit
Ecophysiology
Amphidromy

## ABSTRACT

Freshwater shrimp play crucial roles in aquatic ecosystems, yet their vulnerability to climate change remains poorly understood. This study investigates the thermal tolerance and vulnerability to climate warming of two important freshwater shrimp species with contrasting ecological preferences, *Atyaephyra desmarestii* and *Caridina multidentata*. Critical thermal maximum (CTMax) was assessed for different acclimation temperatures that cover the current summer range for both species, as well as for populations from different geographical origins for *A. desmarestii*. Both species demonstrated an excess of thermal tolerance in all conditions, as calculated with the thermal safety margins (TSM). However, the decrease of TSM with increasing acclimation temperatures suggested potential limitations in their ability to cope with future warming, particularly for the southern populations of *A. desmarestii*. Furthermore, while *C. multidentata* showed a high tolerance to extreme temperature fluctuations, it may face challenges in maintaining viable populations under projected climate change scenarios.

The present study also provides a survey of the thermal limits of Caridea, thereby highlighting the necessity for further research on the thermal tolerance of shrimp to inform effective conservation strategies and mitigate the impacts of climate change.

## 1. Introduction

Freshwater ecosystems, which include rivers, lakes, streams, and wetlands, are diverse and ecologically important systems, which provide vital services to humans, such as drinking water source, and habitat for a wide range of species (Brink et al., 2013; Singh et al., 2021). These ecosystems are currently facing a number of threats related to a variety of human activities including pollution, flow modification, invasive species, overexploitation, and sand mining (WWF, 2024). As a consequence of these large-scale threats, freshwater populations have declined by an average of 85 % since 1970 (according to the Living Planet Index, which measures the abundance of vertebrate species by the total number of individuals; WWF, 2024), making freshwater habitats one of the most endangered across the globe (Strayer and Dudgeon, 2010; Vörösmarty et al., 2010). Caridean shrimp are of significant importance in freshwater ecosystems, as they can be a dominant component of the community, numerous species are harvested or

farmed for food, and they exhibit remarkable diversity in terms of species, life-histories with many migrating species, and ecological niches (De Grave et al., 2015; Bauer, 2023). Yet, some species of freshwater shrimp are already extinct, and almost one third of the others are threatened (De Grave et al., 2015). The major family of freshwater shrimp, the Atyidae, has a quite high extinction risk of 37 % (De Grave et al., 2015).

The thermal landscapes of streams and rivers also evolve as a result of anthropogenic activities such as discharge of heated effluents from industry, water abstraction, removal of riparian shade, and on a larger scale global warming (e.g. Floury et al., 2013; Benateau et al., 2019). Since temperature is one of the major structuring factors in the distribution of populations at both geographical and local levels, temperature-related modifications have already been observed in freshwater communities. As for example, Floury et al. (2013) demonstrated that temperature is one of the major predictors of invertebrate community composition in the river Loire (France), and that Atyidae

<footnote><sup>a</sup> Laboratoire de Biologie des Organismes et Écosystèmes Aquatiques (BOREA), MNHN, CNRS-8067, IRD-207, Sorbonne Université, UCN, UA, Équipe Biodiversité, Plasticité, Adaptation et Conservation, 43 rue Cuvier, 75005, Paris, France</footnote>

<footnote><sup>b</sup> Établissement public du Palais de la Porte Dorée, Aquarium tropical, 293 avenue Daumesnil, 75012, Paris, France</footnote>

<footnote>* Corresponding author.
E-mail address: juliette.ravaux@sorbonne-universite.fr (J. Ravaux).</footnote>

<footnote n="1">¹ www.palais-portedoree.fr.</footnote>
populations abundance was significantly correlated to water tempera-
ture. Yet, thermal tolerance knowledge on atyid shrimp is very limited
(Table 1) and without sufficient data, it is difficult to predict their re-
sponses to environmental changes and to further implement conserva-
tion strategies.

Our study investigates the thermal tolerance of two freshwater atyid
shrimp, which are important for different reasons. The first species,
*Atyaephrya desmarestii* (Millet, 1831), has been used as a bioindicator to
evaluate the health status of river ecosystems (e.g. Janssens de Bist-
hoven et al., 2006; Pestana et al., 2007; González-Ortegón et al., 2012)
and as a model in ecotoxicology studies to assess the impact of pollutants
(Bethke et al., 2023). The second species, *Caridina multidentata* Stim-
pson, 1860, also known as the Amano shrimp, is widely used in aquar-
ium trade due to its ability to consume and therefore control algal
growth in aquariums. However, despite their importance, both species
lack comprehensive data on their thermal tolerance.

A. desmarestii is an atyid shrimp widely distributed in freshwater
habitats, spanning from North Africa to West-central Europe
(Christodoulou et al., 2012), therefore occupying a large part of Europe
and some Mediterranean islands (Noël, 2017). The edges of its distri-
bution range have recently extended to northeastern Europe in areas
across the Rhine (Schoolmann et al., 2015) reaching the Elbe up to the
Czech Republic (Straka and Špaček, 2009) and the Oder in Poland
(Gruszka, 2001), which sometimes leads to refer to this species rather
excessively as invasive (Noël, 2017). This species is considered to have
high ecological valence and is therefore commonly described as eur-
yecic, thermotolerant and sometimes even thermophilic, although there
is limited data to support these statements. The thermotolerance pro-
posed for the species is based on two in situ population monitoring
studies, which reported the presence of shrimp in waters at temperatures
from 3 to 22 °C in the Netherlands (Van den Brink and Van Den Velde,
1986), and from 13 to 28 °C in Morocco (Mabrouki et al., 2018). The
only study currently providing experimental data on the thermal toler-
ance of this species reports a normal respiratory activity between 15 °C
and 30 °C in specimens from southern Spain, indicating that the popu-
lation in this region has a good capacity to tolerate high temperatures
(González-Ortegón et al., 2012). The species' thermal tolerance may
however very according to the geographical origin of the population.
Thermal tolerance is indeed expected to vary with latitude, a phenom-
enon that has been demonstrated in a large number of terrestrial, marine
and freshwater organisms (Gaston et al., 2009; Sunday et al., 2011,
2019; Cereja, 2020). The magnitude of variation expected for CTMax in
freshwater species is of the order of –0.17 °C per degree of latitude
increase (upper thermal limit data for 99 freshwater species; Sunday
et al., 2019). For freshwater crustaceans, there are currently few studies
on the variation of thermal limits as a function of latitude for pop-
ulations of the same species (Cereja, 2020), and only one study on
shrimps, even when considering not only the Caridea but even more
broadly the Penaeidae. This study showed a variation in CTMax of
0.16 °C per degree of latitude in populations of the shrimp *Betaeus
emarginatus* separated by 20° of latitude (Barria et al., 2018; values
included in the dataset used by Sunday et al., 2019). This raises the
question of whether the northward expansion of *A. desmarestii* has been
accompanied by an adjustment in its thermal tolerance in order to
acclimate to the more moderate thermal conditions of these regions.

C. multidentata also belongs to the atyid family but has a narrower
geographic range that is limited to Taiwan, the main islands of Japan,
the Ogasawara Islands and the Ryukyu Archipelago (Nagai et al., 2022).
This shrimp is an amphidromous species, which means that it migrates
between freshwater and marine environments during its life cycle (see
de Mazancourt and Ravaux, 2024 for review). It inhabits freshwater as
an adult, then returns to the ocean as a larva to complete its develop-
ment before returning to rivers. While this species is harvested for
aquarium trade from natural populations without any regulation, our
current knowledge of this species is still very limited (de Mazancourt
and Ravaux, 2024). The biotic and abiotic factors responsible for

determining its geographical distribution remain unknown, as well as its
resilience to natural and anthropogenic environmental variations. A
single recent study addressed the thermal tolerance of this species, and
reported a decrease in the survival rates for temperature exceeding 36 °C
(Kobayashi et al., 2024).

The thermal tolerance is here assessed in two populations of
*A. desmarestii* (Spain and France), and for commercially purchased
specimens of *C. multidentata* (Japan), for different temperatures of
acclimation that cover the range of summer temperatures encountered
by these species in their natural habitat. Their response and their po-
tential vulnerability to water warming is evaluated by estimating the
plasticity of their critical thermal limit (CTMax) and the thermal safety
margin (TSM is the excess of thermal tolerance measured by the dif-
ference between a species CTMax and the environmental/body tem-
perature; see for example Vinagre et al., 2019; Gunderson and Stillman,
2015). Finally, the thermal limit data provided for these two species of
Atyidae shrimp are contextualized within the global dataset available
for all Caridea shrimp.

## 2. Material and methods

2.1. Specimen collection and acclimation conditions

Specimens of *Atyaephrya desmarestii* were collected in July 2023
from Ter River (Flaça, Sobránigues low-water crossing, Spain;
42°3.577'N 2°57.589'E; approximately 100 individuals), and from the
Seine (Vitry-sur-Seine, France; 48°48.257'N 2°24.568'E; approximately
30 individuals). The average water temperature at the time of capture
was 28 °C (Spain) and 24 °C (France). The shrimp were collected with a
sampling net, they were transported to the laboratory at the MNHN
(Paris) in aerated bottles, and transferred to 50-L (Spain) or 30-L
(France) aquarium tanks filled with tap water maintained at 23 °C,
and submitted to a 12h:12h light:dark cycle. The shrimp primarily
consumed algae and biofilm accumulated on the aquarium walls, dec-
orations and plants, and they were provided with pellets (JBL Novo
Prawn that contain vegetable by-products, fish and fish by-products,
molluscs and crustaceans) once a week to complement their diet. They
were allowed to acclimate for 3 months prior to the CTMax experiments
(long-term acclimation protocol according to Ravaux et al., 2012). At
the end of the acclimation period at 23 °C, two batches from the Spanish
population were placed in 50 L aquariums and acclimated respectively
to a temperature of 18 °C and 28 °C. The temperature was increased or
decreased by 2 °C every 3 days, starting at 23 °C, until the desired final
temperature was reached. A. desmarestii populations were maintained in
ornamental tanks that were extensively decorated, thereby hindering
the ability to accurately record mortality rates during the acclimation
periods. The individuals were maintained at their temperature of
acclimation for 3 months before the CTMax experiments.

Specimens of *Caridina multidentata* were purchased from “Comptoir
du poisson exotique” (Héric, France, https://www.poisson-exotique.fr/)
and batches of 25 individuals were placed in seven 70-L aquarium tanks
at the Aquarium tropical de la Porte dorée (Paris). Each tank was filled
with tap water (dechlorinated by oxygenation for 24h before use)
maintained at 23 °C using an Aquavi chiller (model Ice 400) powered by
a Sicce pump (Micraplus 600; capacity 600 l/h), aerated using large air
stones, and submitted to a 12h:12h light:dark cycle. The water in the
aquaria is continuously filtered by an exhauster sponge filter supplied
with compressed air. All tanks were closed with transparent plastic lids,
and all pipe passages were secured with wire mesh, to prevent the escape
of shrimps, which are capable of climbing up the walls and pipes. Shrimp
were kept at 23 °C for 2 months before the temperature was increased or
decreased to reach the final temperature of acclimation: 14, 17, 20, 23,
26, 29, or 32 °C (Fig. 1A). Specimens were fed throughout the accli-
mation period with pellets (Pro JBL Novo Crabs that contain shrimps,
vegetable by-products, fish and fish by-products, soya flour) every other
day. Temperature and survival were monitored throughout the
<table><caption>**Table 1**

Thermal tolerance in Atyidae shrimp. SW: seawater; FW: freshwater; A: amphidromy; Climatic zones have been indicated according to the sampling site. CTM: critical thermal maximum or minimum,UILT: upper incipient lethal temperature, LILT: lower incipient lethal temperature, LT50: median lethal temperature (temperature required to kill 50 % of the population). N.B.UILT and LT50 are equivalent techniques.</caption><thead><tr><th>Species</th><th>Habitat</th><th>Climate zone</th><th>Stage</th><th>Sampling site</th><th>Sampling site T°</th><th>Acclimation / Experimental T°</th><th>Thermal tolerance index</th><th>Optimum T°</th><th>Maximal thermal limit</th><th>Minimal thermal limit</th><th>Reproduction T°</th><th>Reference</th></tr></thead><tbody><tr><td>Atyaephrya desmarestii</td><td>FW</td><td>Temperate</td><td>Adult</td><td>Flaça, Spain</td><td>10 - 29</td><td>18 - 28</td><td>CTM</td><td></td><td>33.3-37.3</td><td></td><td></td><td>This study</td></tr><tr><td>Caridina dali</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Vitry-sur-Seine, France</td><td>5 - 24</td><td>23</td><td>CTM</td><td></td><td>34.6</td><td></td><td></td><td>Annawaty et al., 2016</td></tr><tr><td>Caridina fernandoi</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Lake Lindu, Sulawesi, Indonesia</td><td>18 - 32</td><td></td><td>distribution in situ</td><td></td><td>22</td><td></td><td></td><td>De Silva, 1989</td></tr><tr><td>Caridina kaili</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Lake Lindu, Sulawesi, Indonesia</td><td>18 - 32</td><td></td><td>ILT/LILT</td><td></td><td>29</td><td>15</td><td></td><td></td></tr><tr><td>Caridina leucosticta</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20-32</td><td>distribution in situ</td><td></td><td>34</td><td></td><td></td><td></td></tr><tr><td>Caridina linduensis</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Lake Lindu, Sulawesi, Indonesia</td><td>5-25</td><td></td><td>distribution in situ</td><td></td><td>23</td><td></td><td></td><td>Annawaty et al., 2016</td></tr><tr><td>Caridina multidentata (Caridina japonica)</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20-28</td><td>survival %</td><td>23 - 26</td><td></td><td></td><td>Kondo et al., 2021</td></tr><tr><td>Caridina multidentata (Caridina japonica)</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20 - 32</td><td>distribution in situ</td><td></td><td>>15</td><td>&lt;10</td><td>18-25</td><td>Yamada et al., 2024</td></tr><tr><td>Caridina linduensis</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Lake Lindu, Sulawesi, Indonesia</td><td>18 - 32</td><td></td><td>distribution in situ</td><td></td><td>29</td><td></td><td></td><td>Kobayashi et al., 2024</td></tr><tr><td>Caridina multidentata (Caridina japonica)</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20-28</td><td>survival %</td><td>20</td><td></td><td></td><td>Lee, 2009</td><td>Kondo et al., 2021</td></tr><tr><td>Caridina multidentata (Caridina japonica)</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20 - 32</td><td>survival %</td><td>23 - 29</td><td></td><td></td><td>Yamada et al., 2024</td></tr><tr><td>Caridina nilotica</td><td>FW</td><td>Subtropical</td><td>Adult</td><td>Lake Sibaya, South Africa</td><td></td><td>23</td><td>distribution in situ</td><td></td><td>>15</td><td>&lt;5</td><td>17-25</td><td>Kobayashi et al., 2024</td></tr><tr><td>Caridina pristis</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Peradeniya University campus, Sri Lanka</td><td></td><td>18-30</td><td>ILT</td><td></td><td>37.2-37.4</td><td></td><td></td><td>This study</td></tr><tr><td>Caridina serratirostris</td><td>FW(A)</td><td>Temperate</td><td>Adult / juvenile</td><td>Banda River, Japan</td><td>5-25</td><td></td><td>ILT</td><td></td><td>31.5-40.1</td><td></td><td></td><td>Hart, 1983</td></tr><tr><td>Caridina serratirostris</td><td>FW(A)</td><td>Temperate</td><td>Adult / juvenile</td><td>Banda River, Japan</td><td>5-25</td><td></td><td>ILT/LILT</td><td></td><td>31.5-40.1</td><td></td><td></td><td>De Silva, 1989</td></tr><tr><td>Caridina simoni</td><td>FW / BW</td><td>Tropical</td><td>Adult</td><td>Lac Kandy, Galagedera, Sri Lanka</td><td></td><td>23</td><td>distribution in situ</td><td></td><td>27</td><td>13</td><td></td><td></td></tr><tr><td>Caridina typus</td><td>FW(A)</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td>20-32</td><td>distribution in situ</td><td></td><td>27</td><td>15</td><td></td><td></td></tr><tr><td>Paratya australiensis and P. spinosa</td><td>FW / BW</td><td>Subtropical</td><td>Adult</td><td>Leycester Creek, Barkers Vale, Australia</td><td></td><td>23</td><td>ILT/LILT</td><td></td><td>33</td><td></td><td></td><td></td></tr><tr><td>Paratya australiensis and P. spinosa</td><td>FW / BW</td><td>Subtropical</td><td>Adult</td><td>Leycester Creek, Barkers Vale, Australia</td><td></td><td>23</td><td>distribution in situ</td><td></td><td>>15</td><td>&lt;11</td><td>19-25</td><td>Kondo et al., 2021</td></tr><tr><td>Paratya australiensis and P. spinosa</td><td>FW / BW</td><td>Subtropical</td><td>Adult</td><td>Leycester Creek, Barkers Vale, Australia</td><td></td><td>23</td><td>ILT</td><td></td><td>36.6</td><td></td><td></td><td>Yamada et al., 2024</td></tr><tr><td>Paratya australiensis and P. spinosa</td><td>FW / BW</td><td>Subtropical</td><td>Adult</td><td>Leycester Creek, Barkers Vale, Australia</td><td></td><td>15-28</td><td>ILT(LT50)</td><td></td><td>34.6-36.1 (CTMax ~ 37)</td><td></td><td></td><td>Kobayashi et al., 2024</td></tr></tbody></table>

(continued on next page)
<table><caption>Table 1 (continued)</caption><thead><tr><th>Species</th><th>Habitat</th><th>Climate zone</th><th>Stage</th><th>Sampling site</th><th>Sampling site T°</th><th>Acclimation / Experimental T°</th><th>Thermal tolerance index</th><th>Optimum T°</th><th>Maximal thermal limit</th><th>Minimum thermal limit</th><th>Reproduction T°</th><th>Reference</th></tr></thead><tbody><tr><td rowspan="2">Paratya compressa</td><td rowspan="2">FW(A)</td><td rowspan="2">Temperate</td><td>Adult / juvenile</td><td>Banda River, Japan</td><td>5-25</td><td></td><td>distribution in situ</td><td>&gt;15</td><td></td><td>&lt;1</td><td>15-25</td><td>Yamada et al., 2024</td></tr><tr><td>Adult</td><td>Boso Peninsula, Japan</td><td>23</td><td>23-38</td><td>UILT</td><td></td><td>34.2-34.6</td><td></td><td></td><td>Kobayashi et al., 2024</td></tr><tr><td rowspan="2">Paratya curvirostris</td><td rowspan="2">FW(A)</td><td rowspan="2">Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td>20-33</td><td></td><td>survival %</td><td>20</td><td></td><td>33.3</td><td></td><td>Hamasaki et al., 2021</td></tr><tr><td>Adult</td><td>Waihou river, New-Zealand</td><td>12-15</td><td>15-35</td><td>LT50</td><td></td><td></td><td>25.7-27.4</td><td></td><td>Quinn et al., 1994</td></tr><tr><td>Paratya improvisa</td><td>FW</td><td>Temperate</td><td>Larvae</td><td>Laboratory rearing</td><td></td><td></td><td>survival %</td><td>20</td><td></td><td></td><td></td><td>Hamasaki et al., 2021</td></tr><tr><td rowspan="2">Typhlataya dzilamensis</td><td rowspan="2">SW</td><td rowspan="2">Tropical</td><td>Adult</td><td>Boso Peninsula, Japan</td><td>23</td><td>23-38</td><td>UILT</td><td></td><td>32.7-34.9</td><td></td><td></td><td>Kobayashi et al., 2024</td></tr><tr><td>Adult</td><td>Cenote Tza Itza, Nohmozón, Ponderosa, Mexico</td><td>26-27.3</td><td>-</td><td>CTM</td><td></td><td>36.5</td><td>14.3</td><td></td><td>Chávez-Solis et al., 2022</td></tr><tr><td rowspan="2">Typhlataya mitchelli</td><td rowspan="2">FW</td><td rowspan="2">Tropical</td><td>Adult</td><td>Cenote Tza Itza, Nohmozón, Ponderosa, Mexico</td><td>26-27.3</td><td>-</td><td>CTM</td><td></td><td>34.9</td><td>13.8</td><td></td><td>Chávez-Solis et al., 2022</td></tr><tr><td>Adult</td><td>Cenote Tza Itza, Nohmozón, Ponderosa, Mexico</td><td>26-27.3</td><td>-</td><td>CTM</td><td></td><td>34.7</td><td>13.9</td><td></td><td>Chávez-Solis et al., 2022</td></tr><tr><td>Typhlataya pearsei</td><td>FW</td><td>Tropical</td><td>Adult</td><td>Cenote Tza Itza, Nohmozón, Ponderosa, Mexico</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

acclimation and maintenance period in the 7 tanks. Dead individuals were removed from the tanks. Water was changed in the tanks 1–2 times a month (1/2 of the volume replaced), and water parameters (pH, KH, NO2 and NO3 concentration) were tested before and after each water change. The shrimp were maintained at their final acclimation temperatures for at least a month before the CTMax experiments.

## 2.2. Thermal tolerance of *A. desmarestii* and *C. multidentata*

After the acclimation period, the shrimp were transferred to the experimental system used to determine their thermal tolerance. The dynamic method (Mora and Ospina, 2001) was used to evaluate the critical thermal maximum (CTMax), which is defined as the arithmetic mean of the collective thermal points at which the end-point is reached (see Madeira et al., 2012), by using the equation: $CTMax = \Sigma (T_{end-pointn})/n$; where $T_{end-point}$ is the temperature at which the end-point was reached for any given individual, and n stands for the total number of individuals. The temperature was increased at a constant rate until they reach the end-point, which was the first occurrence of the loss of equilibrium (LOE), i.e. when the shrimp loses its balance, resulting in abnormal positions such as swimming on its side, or falling to the bottom of the tank in either an « upside-down » or a « sideways » position.

Specimens of similar size (total length approximately 1.5 cm for *A. desmarestii* and 2.6 cm for *C. multidentata*) were placed individually in a beaker filled with 80 ml of water from the acclimation tank and capped with a transparent lid to allow observation throughout the experiment. The beaker was placed in a water bath (Polystat 22, Bioblock Scientific, Illkirch, France), which regulated the temperature of the surrounding water. The water temperature was monitored in the beaker using an electronic thermometer (VWR® Traceable® Digital Thermometer, Rosny-sous-bois, France). The temperature was increased at a mean rate of $1.6 \,^{\circ}C \,\text{min}^{-1}$ (heating rate in the $0.2-2 \,^{\circ}C \,\text{min}^{-1}$ range to enable the shrimp body to match the environmental temperature without acclimation effect, and to allow interspecies comparison with similar heating rates; Lutterschmidt and Hutchinson, 1997; Vinagre et al., 2015; Gunderson and Stillman, 2015), and the temperature at which each animal reached its end-point was recorded. The experiment ended when the shrimp experienced LOE for about 30 s. The trial was repeated 9 to 12 times, which corresponds to a total of 10 individual shrimp per condition (n = 10) for *C. multidentata* and 9 to 12 individual shrimp per condition (n = 9 to 12) for *A. desmarestii*. Following the CTMax experiment, the shrimp were rapidly returned to their acclimation temperature. The survival of *C. multidentata* was then monitored the following day and throughout the maintenance period.

The thermal safety margin was calculated for both species, as the difference between the CTMax and the mean body temperature (Gunderson and Stillman, 2015), the latter being here approximated by the acclimation temperature. The Acclimation Response Ratio (ARR = $\Delta$CTM/$\Delta$T<sub>acclimation</sub>; Claussen, 1977) was calculated for both species (see Supplementary Table 1 for interspecies comparison).

## 2.3. Data analysis

All analyses were performed with the RStudio program, version 2023.12.1 + 402 (R Core Team, 2024). We checked the homogeneity of variances and the goodness of fit using Levene's test and also the normality using Shapiro test. To test the thermal tolerance of *C. multidentata* according to the acclimation temperatures of individuals, we used a non-parametric Kruskal-Wallis test based on the sum of the ranks because the normality preconditions were not respected. We used the *coin()* package and the *kruskal_test()* function. When the test gives significant differences in maximum critical temperature according to the acclimation temperatures of the individuals, post-hoc analysis was carried out using the Dunn test with the *dunn_test()* function. No sequential Bonferroni correction for alpha was performed if there was a significant effect of the interaction between the two predictor variables (CTMax and
<figure><img src="image_4.png" /><figcaption>**Fig. 1.** Temperature data and survival rates of *Caridina multidentata* in the aquaria. **A)** temperature was set at 23 °C in all aquaria on shrimp arrival and left constant for 2 months (dotted line). The dotted arrows indicate the days when the temperature was increased or decreased by 3 °C to reach the final temperatures: on day 61 (aquarium 14, 17, 20, 26, 29, 32), on day 67 (aquarium 14, 17, 29, 32) and on day 70 (aquarium 14 and 32). **B)** Survival rates under the different acclimation temperatures. Black arrows indicate the days on which CTMax experiments were conducted (n = 10 individuals for each tank).</figcaption></figure>

acclimation temperature).

## 2.4. Literature search

A comprehensive literature search was conducted using Google Scholar during March-May 2024 and September 2024. In order to identify data concerning the thermal tolerance of atyid shrimp, the following search terms were used: 'thermal tolerance atyid'. This yielded 179 references, which were subsequently evaluated in order to identify only studies reporting original data on the thermal biology of atyid shrimp species. For identifying studies on the critical thermal limits in caribbean shrimp, the following search terms were employed: 'CTMax shrimp' (812 references), 'critical thermal maximum Caridea' (902 references), 'CTMin shrimp' (328 references), 'critical thermal minimum Caridea' (593). Each reference was manually evaluated by a single observer (JR) for suitability: only studies reporting original data of critical thermal limits (CTMax or CTMin) on caribbean shrimp species were selected (no citing article or review). The methodologies of the selected references were further examined in order to register the information about the protocol and results: acclimation temperature, duration of acclimation, number of specimen per experiment, temperature ramp, CTMax/Min endpoint, CTMax values, CTMin values, scope for thermal tolerance (CTMax - CTMin), CTMax acclimation response ratio (ΔCTMax)/(ΔTemperature of acclimation). In cases where CTMax or CTMin data were only presented in graphics, the values were estimated by measuring corresponding points on the graph. The information about the shrimp were also collected: environment (seawater,

freshwater, amphidromy), climate zone, stage, sampling site, average size/weight, temperature at sampling site.

## 3. Results

### 3.1. Thermal tolerance and acclimation capacity assessment of two populations of *Atyaephyra desmarestii*

The CTMax values for *A. desmarestii* originating from Spain were 33.2 °C (acclimation at 18 °C), 35.0 °C (acclimation at 23 °C), and 37.3 °C (acclimation at 28 °C), corresponding to a 2 °C increase in CTMax for each 5 °C increase in acclimation temperature (Fig. 2). The calculated thermal safety margin is 15 °C (acclimation at 18 °C), 12 °C (acclimation at 23 °C), and 9 °C (acclimation at 28 °C).

The CTMax value for *A. desmarestii* originating from France was 34.7 °C (acclimation at 23 °C), giving a summer thermal safety margin of 12 °C (Fig. 2).

### 3.2. Thermal tolerance and acclimation capacity assessment of *Caridina multidentata*

The CTMax values for *C. multidentata* acclimated at temperatures ranging from 14 °C to 32 °C gradually increased from 31.5 °C to 40.1 °C, corresponding to an increase of around 2.4 °C in CTMax for each 5 °C increase in acclimation temperature (Fig. 3). The calculated thermal safety margin ranges from 17 °C (14°C-acclimated specimens) to 8 °C (32°C-acclimated specimens).
<figure><img src="image_5.png" /></figure>

**Fig. 2.** Critical thermal maximum of two populations of *Atyaephyra desmarestii* acclimated to different temperatures. Left panel: photograph of an *A. desmarestii* specimen (photo credits: V. de Mazancourt), and map showing the location of the sampling sites in France (Vitry-sur-Seine) and Spain (Flaça). Right panel: CTMax data are represented as box plots, with whiskers indicating the minimum and maximum, the box delimiting the first quartile and third quartile, and the median and mean identified by an horizontal line (the value for median and mean is equivalent and is shown next to the line). The experiments were conducted on a sample size of n = 9 (Spain, 28 °C), n = 10 (Spain, 18 °C), and n = 12 (Spain, 23 °C and France 23 °C) individuals. Values sharing a common letter are not significantly different (p > 0.05). The summer thermal safety margin (dotted lines) is calculated as the difference between the CTMax (mean) and the maximum water temperature (31 °C for Spain: Arbat-Bofill, 2015; 27 °C for France: Rivière et al., 2021).

<figure><img src="image_6.png" /></figure>

**Fig. 3.** Critical thermal maximum of *Caridina multidentata* acclimated to different temperatures. Data are represented as box plots, with whiskers indicating the minimum and maximum, the box delimiting the first quartile and third quartile, and the median and mean identified by an horizontal line (the value is shown next to the line). Each experiment was conducted on a sample size of n = 10 individuals. Values sharing a common letter are not significantly different (p > 0.05). The summer thermal safety margin (dotted lines) is calculated as the difference between the CTMax (for acclimation at 17 °C-26 °C since summer water temperatures are between 18 °C and 25°C; Yamada et al., 2024) and the habitat maximum water temperature (25°C; Yamada et al., 2024). Photo credit: Jacky Yu.

### 3.3. Survival of *Caridina multidentata* at different acclimation temperatures

Survival of *C. multidentata* was 96–100 % after 1 month of acclimation at temperatures ranging from 14 °C to 32 °C (Fig. 1B). After this one-month period, the CTMax experiments were carried out. Among the specimens subjected to CTM experiments, 3 out of 10 died the day after testing for the acclimation temperatures of 29 °C and 32 °C (this

mortality is included in the monitoring of survival shown in Fig. 1B). Survival subsequently decreased in the following weeks to 74 % for the batch acclimated at 32 °C, and 83 % for the batches acclimated at 14 °C and 29 °C. Survival rates for the other batches (17 °C-26 °C) remained between 92 % and 100 % during the 3 months of monitoring at the final acclimation temperature.
### 3.4. Thermal limits in caridea shrimp

Very little data is currently available on the thermal tolerance of Atyidae (Table 1). Of the 542 species of Atyidae currently identified (de Mazancourt and Ravaux, 2024), only 20 have been the subject of heat tolerance studies to date. Among these studies, a single recent publication reports the maximum thermal limits of 3 species of *Typhlatya* (Chávez-Solís et al., 2022). Here we provide data on maximum thermal limits for two other species that complement the limited dataset for Atyidae shrimps (upper thermal limit known for only 11 species representing 2 % of Atyidae species), but also more generally for Caridea shrimps. Indeed, the state-of-the-art on thermal limits for all Caridea presented in Fig. 5 reveals that there is relatively little data available globally for this group (see Supplementary Table 1 for the complete list of data). Only 29 species have been documented out of about 3500 Caridea species (Caridea species census: De Grave and Fransen, 2011), including 12 freshwater species out of the 925 currently described (count of freshwater shrimp species: de Mazancourt and Ravaux, 2024), a mere 0.8 % of total shrimp species and 1.3 % of freshwater shrimp.

## 4. Discussion

### 4.1. Thermal limits and acclimation capacity of atyid shrimp *Atyaephrya desmarestii* and *Caridina multidentata*

Until now, there was no data on the thermal tolerance of *A. desmarestii*, aside from the demonstration of a respiratory activity up to temperature of 30 °C for specimens acclimated at 20 °C (González-Ortegón et al., 2012), which is quite close to the upper thermal limits we obtained for this species (CTMax in the range of 33.2 °C–35 °C for 18°C to 23°C-acclimated specimens). Only one study was available on upper thermal tolerance of *C. multidentata* adults which, based on survival rates upon a temperature increase of 1 °C per day, proposed an upper thermal limit of 37.2–37.4 °C (commercially purchased specimens placed at 23°C; Kobayashi et al., 2024, Table 1). This upper thermal limit value corresponds to that obtained for

specimens acclimated at 26 °C. However, the comparison with our results is limited by several factors, not only by the difference in indicator (UILT versus CTMax), but above all by the difference in acclimation (no acclimation versus long-term acclimation). A comparison of the CTMax data obtained for *A. desmarestii* and *C. multidentata* with those from other Atyidae shows that they are rather high (Table 1). The values obtained, at equivalent acclimatization or acclimation temperature, for our two species from temperate zones are equal to or higher than those obtained for *Typhlatya* species from tropical zones: 34.7 °C–36.5 °C (temperature at sampling site 26–27°C; Chávez-Solís et al., 2022) versus 37.3 °C for *A. desmarestii* (acclimation at 28 °C, i.e. an estimated CTMax for acclimation at 26 °C of around 36.5 °C assuming an ARR of 0.4; Supplementary Table 1), and 37.5 °C for *C. multidentata* (acclimation at 26 °C). But if these data are placed in the broader dataset of Caridean shrimp, the CTMax obtained for our two temperate Atyidae species do not stand out from the dataset obtained, which includes both temperate, tropical and subtropical species, as they are neither very low nor very high (Fig. 4, Supplementary Table 1). It should be noted, however, that few temperate species have been tested at high acclimation temperatures above 25 °C. The fact that *C. multidentata* survives a long-term exposure at an acclimation temperature of 32 °C, which has never been tested for a temperate species, and that it shows a capacity to acclimate its CTMax for environmental temperatures ranging from 14 °C to 32 °C, demonstrates a high level of thermal tolerance in this species.

One of the criteria for estimating a species vulnerability in the context of global change is the estimation of its acclimation capacity. We therefore tested the capacity for CTMax acclimation of our two Atyidae species under summer conditions. For *A. desmarestii*, temperature monitoring carried out in 2011 in the Ter River upstream of our sampling site in Spain reported a temperature range in summer between 19 and 31 °C (Arbat-Bofill, 2015). The temperature at our sampling site in July was 28 °C, hence the acclimation temperature range of 18–28 °C chosen for *A. desmarestii* covers the range of summer temperatures encountered in its habitat, although temperatures can exceed these values in some years. *Caridina multidentata* specimens were collected in Japan, north of the species' range, which is centered on Taiwan (Nagai

<figure><img src="image_7.png" /><figcaption>**Fig. 4.** Thermal limits of shrimp of different climate zone according to acclimation temperatures. Solid circles: critical thermal maximum (CTMax); open circles: critical thermal minimum (CTMin); $ARR = \Delta CTM/\Delta T_{acclimation}$; Claussen (1977). The complete list of species with values and references is given in Supplementary Table 1. The graph depicts only values for adult stages and when temperature acclimation data were available. The Loss of Equilibrium (LOE), Loss of Righting Response (LRR) or Spasms behavioural responses were here chosen for inter-species comparison since they are well established as indicators of temperature-induced loss of function. The heating rate varied from 0.02 to 1.6 °C min$^{-1}$, but was proved to have very small effects on CTmax ARR (Gunderson and Stillman, 2015). Temperate species (blue): *Cragon cragon*, *Palaemon adspersus*, *Palaemon elegans*, *Palaemon kadiakensis*, *Palaemon serratus*, *Palaemon macrodactylus*, *Palaemon varians*, *Pandalus montagui*; Subtropical species (yellow): *Macrobrachium americanum*; Tropical species (red): *Palaemon northropi*, *Hippolyte obliquimanus*, *Lysmata lipkei*, *Macrobrachium caementarius*, *Macrobrachium acanthurus*, *Macrobrachium rosenbergii*, *Macrobrachium tenellum*. Our data on *Atyaephrya desmarestii* and *Caridina multidentata* are indicated in black.</figcaption></figure>
<table><thead><tr><th rowspan="2"></th><th colspan="2">Thermal limits</th><th rowspan="2">Species</th><th rowspan="2">References</th></tr><tr><th>CTMax</th><th>CTMin</th></tr></thead><tbody><tr><td rowspan="12">Caridea</td><td rowspan="3">Atyidae</td><td>●</td><td></td><td>Atyaephrya desmarestii<br>Caridina multidentata</td><td>This study</td></tr><tr><td>●</td><td>●</td><td>Typhlatya dzilamensis</td><td>3</td></tr><tr><td>●</td><td>●</td><td>T. mitchelli</td><td>3</td></tr><tr><td>●</td><td>●</td><td>T. pearsei</td><td>3</td></tr><tr><td>Alvinocarididae</td><td>●</td><td></td><td>Mirocaris fortunata</td><td>28</td></tr><tr><td>Pandalidae</td><td>●</td><td></td><td>Rimicaris exoculata</td><td>21</td></tr><tr><td>Crangonidae</td><td>●</td><td>●</td><td>Pandalus montagui</td><td>15</td></tr><tr><td>Lysmatidae</td><td>●</td><td></td><td>Crangon crangon</td><td>6; 12; 15; 24; 32</td></tr><tr><td rowspan="3">Hippolytidae</td><td>●</td><td></td><td>Lysmata ambooinensis</td><td>26</td></tr><tr><td>●</td><td></td><td>Lysmata lipkei</td><td>14; 33</td></tr><tr><td>●</td><td></td><td>Lysmata seticaudata</td><td>26</td></tr><tr><td>Alpheidae</td><td>●</td><td></td><td>Hippolyte obliquimanus</td><td>31; 32; 33</td></tr><tr><td rowspan="12">Palaemonidae</td><td>●</td><td>●</td><td>Betaeus emarginatus</td><td>2</td></tr><tr><td>●</td><td>●</td><td>Cryphiops caementarius</td><td>25; 7</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium acanthurus</td><td>5</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium americanum</td><td>8</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium malcomsonii</td><td>27</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium occidentale</td><td>10</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium rosenbergii</td><td>4; 16</td></tr><tr><td>●</td><td>●</td><td>Macrobrachium tenellum</td><td>9; 11; 29</td></tr><tr><td>●</td><td>●</td><td>Palaemon adpersus</td><td>6</td></tr><tr><td>●</td><td>●</td><td>Palaemon elegans</td><td>1; 12; 13; 15; 23; 30; 31</td></tr><tr><td>●</td><td>●</td><td>Palaemonetes kadiakensis</td><td>18</td></tr><tr><td>●</td><td>●</td><td>Palaemon longirostris</td><td>12</td></tr><tr><td>●</td><td>●</td><td>Palaemon macrodactylus</td><td>15</td></tr><tr><td>●</td><td>●</td><td>Palaemon nothropi</td><td>31; 32</td></tr><tr><td>●</td><td>●</td><td>Palaemon serratus</td><td>13; 15; 30</td></tr><tr><td>●</td><td>●</td><td>Palaemon varians</td><td>15; 17; 19; 20; 22</td></tr></tbody></table>

**Fig. 5.** Thermal limit data currently available for Caridae. Phylogeny adapted from Davis et al., (2018). References for each species are listed hereafter in alphabetical order with their corresponding number. 1: Amsalem and Rilov (2021); 2: Barria et al. (2018); 3: Chávez-Solís et al. (2022); 4: Diaz et al. (1998); 5: Díaz et al., 2002; 6: Ern et al. (2020); 7: Ferrer-Chujutalli et al. (2024); 8: García-Guerrero et al. (2022); 9: Hernandez et al. (1996); 10: Hernández-Sandoval et al. (2018a); 11: Hernández-Sandoval et al. (2018b); 12: Madeira et al. (2012); 13: Madeira et al. (2015); 14: Madeira et al. (2019); 15: Magozzi and Calosi (2014); 16: Manush et al. (2004); 17: Missionário et al. (2022); 18: Nelson and Hooper (1982); 19: Oliphant et al. (2011); 20: Peruzza et al. (2021); 21: Ravaux et al. (2003); 22: Ravaux et al. (2012); 23: Ravaux et al. (2016); 24: Reiser et al. (2014); 25: Reyes-Avalos et al. (2023); 26: Rosa et al. (2014); 27: Selvakumar and Geraldine (2005); 28: Shillito et al. (2006); 29: Tremblay et al. (2022); 30: Vinagre et al. (2013); 31: Vinagre et al. (2015); 32: Vinagre et al. (2016); 33: Vinagre et al. (2019).

et al., 2022). Temperature data from a temperate *C. multidentata* habitat in Japan report summer values of between 18 °C and 25 °C (Banda River, 34°58′N, 139°46′E; Yamada et al., 2024). The acclimation temperatures tested for *C. multidentata* therefore cover the whole range of summer temperatures, and even go further than the current summer maximums, allowing a projection towards warmer summers. Both species showed an ability to acclimate over the summer temperature range, and even beyond the entire range tested for *C. multidentata*, with an Acclimation Response Ratio (ARR) of 0.40 for *A. desmarestii* (population from Spain) and 0.47 for *C. multidentata* (Figs. 2 and 3). *C. multidentata* therefore has a better ability to acclimate its upper thermal limit than *A. desmarestii*, suggesting that it would be less vulnerable to an increase in environmental temperature. The CTMax ARR values available for all Caridea shrimps show a great interspecific variability, and they range from a minimum value of 0.12 for *Macrobrachium rosenbergii* to a maximum value of 0.9 for *Lysmata lipkei* (19 species, Fig. 4; Supplementary Table 1). The CTMax ARR for the two atyid species are similar to the mean ARR values obtained for all other shrimp species: 0.40 for subtropical shrimp, 0.44 for tropical shrimp, and 0.46 for temperate shrimp (Fig. 4). Differences in acclimation ability are minor between shrimp species from tropical, subtropical and temperate zones. Overall, the mean increase of CTMax in shrimp compensates for the 1 °C rise in environmental temperature by a mere 0.5 °C or less. This relatively modest compensation is similarly evident at the crustacean level, where a 0.3 °C variation in CTMax is observed in response to a 1 °C change in body temperature (Gunderson and Stillman, 2015). Furthermore, this phenomenon is not exclusive to crustaceans, but is also observed across the broader range of ectothermic organisms, whose CTMax ARR rarely

exceeds 0.5 (Gunderson and Stillman, 2015). Therefore, the plasticity of the upper thermal limit alone would not be sufficient to adapt the thermal tolerance of ectotherms to environmental thermal variation.

## 4.2. Thermal limit variation with latitude: the case of Atyaephrya desmarestii

Here we compare the CTMax of two populations of *A. desmarestii* more than 900 km apart, corresponding to 6° on a latitudinal axis: the southern population of Spain and the northern population of the Paris region (Fig. 2). The expected variation in CTMax should be around 1 °C for these populations (about 0.17 °C per degree of latitude; Sunday et al., 2019), yet the CTMax values obtained were equivalent, all other things being equal: acclimation at the same temperature, identical maintenance and experimental conditions. These data suggest that this species' upper thermal limit would not shift as a function of the geographic zone, meaning that the thermal tolerance would not adjust to the thermal conditions of its habitat at the scale of its geographical distribution. And yet, the populations from Spain and from France are subject to clearly different thermal conditions in their environment, particularly with regard to extreme summer temperatures. A broad correspondence has been shown between thermal limits and extreme environmental temperatures, suggesting that latitudinal patterns of thermal tolerance can be largely explained by the extreme temperatures encountered in each environment (Sunday et al., 2019). Temperature recorded in summer ranged from 19 to 31 °C on the Spanish site (Arbat-Bofill, 2015), and from 19 to 23 °C on the French site (measurement in the Seine over 26 years for the 20th century; Rivière et al., 2021). The data of the Seine do,
however, show a warming of the water temperature, which sometimes reaches 27 °C and more rarely exceeds 27 °C. High summer temperatures for the French population therefore remain several degrees below those of the Spanish population. Moreover, the French population has settled in the Seine since at least 1843 (Noël, 2017), so it's a long-established colonization that has given this population ample time to adapt to the climatic conditions of this habitat.

These preliminary results pave the way for further study of this species to determine the seasonal thermal limits of populations over its geographical range, in order to test the relationship between geographical distribution and thermal tolerance. This would involve comparing populations at the north-south limits of the species' range, where differences in habitat temperature are most marked, to confirm whether the latitudinal migration leads to a shift in the thermal tolerance. Experimental translocations of shrimp populations could also provide information on the kinetics and range of species' acclimation and ultimately adaptation to a new thermal environment.

### 4.3. Thermal safety margins (TSM) in the context of global warming

Predicting the vulnerability of a species to climate change often relies on estimating the thermal safety margin (TSM), which measures the difference between a species' maximum tolerance to heat (CTMax) and the environmental or body temperature (Cereja, 2020; Sunday et al., 2014; Gunderson and Stillman, 2015). Positive values for TSM mean that the species has an excess of warm tolerance and would therefore be more readily able to cope with increasing environmental temperatures. For *A. desmarestii*, the TSM for Spain population under current summer temperatures of 19 °C-31 °C (Arbat-Bofill, 2015) range from 15 °C to 9 °C, and is about 12 °C for French population for a mean summer temperature of 23 °C (Rivière et al., 2021). For *C. multidentata* the TSM range from 16 °C to 11 °C for current summer temperatures (18 °C-25°C; Yamada et al., 2024). The TSM obtained for these two atyid species is comparable to values previously calculated by Bates et al. (2010) for 77 aquatic species from marine and freshwater environments (with the exception of hydrothermal species), which was approximately 12 °C. They are also comparable to TSM obtained for 6 crustaceans from shallow temperate coastal waters, which ranged from 13 °C to 9 °C (Vinagre et al., 2019), as well as to the dataset compiled for 52 freshwater Malacostraca, which gives an average TSM value of about 15 °C (Cereja, 2020). The atyid TSM values showed an excess of thermal tolerance that may allow both species to cope with an increase of the water temperature in summer.

For both atyid species the TSM decreased with increasing water temperature, due to the partial compensation by the CTMax acclimation (Fig. 2; Fig. 3). For *C. multidentata* the TSM is 11 °C for the current maximum summer temperature of 25 °C, and is still 8 °C for a water temperature of 32 °C, giving this species a significant margin to cope with future warming. For *A. desmarestii* southern population (Spain), the TSM decreased by 6 °C when the water temperature changed from 18 to 28 °C, and since current maximum summer temperatures reach 31 °C, further warming may lead to insufficient TSM. For *A. desmarestii* northern population (France), a TSM of 12 °C was estimated based on the mean maximum temperature measured during summer in the Seine (23°C; Rivière et al., 2021). However, the evolution of the thermal regime of the Seine River envisaged according to different global warming scenarios predicts an increase in average annual temperatures of over 2.5 °C by 2100, which would mean an average maximum temperature of over 25.5 °C in summer, and more frequent temperature exceeding 27 °C. The TSM might then prove insufficient to cope with heatwave episodes, and further experiments on this population are needed to determine if the TSM increase at higher acclimation temperatures. The comparison of TSM across latitude for the two populations of *A. desmarestii* showed no difference (TSM of 12 °C for 23°C-acclimated specimens; Fig. 2). These findings are not aligned with the relationship observed by Cereja (2020) in ectothermic organisms, which

demonstrates an increase in TSM from the equator towards the poles. Cereja (2020) also showed the existence of a peak for freshwater species where TSM is maximum in temperate regions at 35° North. Our results are not consistent with this latter statement. For *A. desmarestii*, the 35°N latitude would correspond to the southern part of its range, located in North Africa, and it is therefore unlikely that TSM would be higher there than in the northern parts of its range.

The *A. desmarestii* population is already known to be declining in the south of France, as a result of hot, dry summers and irrigation leading to the temporary drying up of small streams (Noël, 2017). With global warming, it may be difficult for this species to maintain itself in the southern regions of its current distribution range, and it may likely continue to extend to northern regions. This is in accordance with the conclusions of Gunderson and Stillman (2015) that the plasticity of CTMax will not compensate for environmental temperature increases and consequently not ensure sufficient thermal safety margins, and that behavioral thermoregulation (e.g. migration) will be a more effective response for mobile ectotherms. A comparison of the southern and northern *A. desmarestii* populations revealed no significant difference in their CTMax or TSM (acclimation at 23 °C). However, the northern population has a reduced risk of exposure to temperatures approaching its thermal limit. By extending to the northern regions, *A. desmarestii* might therefore respond to global warming by settling in habitats with lower environmental temperatures.

The acclimation experiments conducted on *C. multidentata* allowed to further test this species thermal tolerance. Long-term monitoring over a 4-month period of shrimps acclimated to temperatures ranging from 14 °C to 32 °C revealed a decrease in survival for extreme temperatures above 26 °C (Fig. 1B). A significant decrease in survival was observed after individuals were exposed to an experimental heat peak over a 10 min period at a temperature reaching the CTMax. This indicates that specimens that have been acclimated to temperatures between 17 °C and 26 °C, which correspond to the current summer temperatures in their natural habitat (Yamada et al., 2024), are capable of withstanding exposure to extreme temperature spikes. In contrast, specimens that have been acclimated to higher temperatures are adversely affected by such temperature fluctuations. Thus, while the TSM of *C. multidentata* would enable this species to cope with heat waves or heat peaks under current temperature conditions, this does not necessarily mean that it can withstand warmer environmental temperatures over the long term. The terms “thermal safety margin” and “warming tolerance” (used for example by Vinagre et al., 2016; Sandoval-Castillo et al., 2020; Amsalem and Rilov, 2021) are thus not synonymous. And our preliminary results on *C. multidentata* suggest that for estimating the ability of species to withstand a long-term increase in the average temperature of their habitat, with more frequent heat waves, the TSM alone is not sufficient.

### 4.4. Thermal tolerance of shrimp – present status and future research

A literature search was conducted on the thermal limits of shrimp in order to obtain a quantitative assessment of available publications (Supplementary Table 1 for Caridea and Table 1 for the family Atyidae). The literature reveals a paucity of data available globally for shrimp, with less than 1 % of total species that have been documented (Fig. 5, Supplementary Table 1). Expanding the thermal tolerance dataset for shrimp is of interest for understanding the species current distribution and anticipate changes in response to environmental variations or changes associated with species introductions, and more broadly for refining models for predicting the effects of climate change on crustaceans. At a specific level, the combination of experimental thermal tolerance data and in situ temperature measurements provides a valuable predictive tool for monitoring and anticipating changes in the distribution of natural populations. Studies on *Caridina* and trout species have already established a link between experimentally determined thermal tolerance and geographical distribution, validating such an experimental approach as a tool for explaining a species' range (Hart,
1983; de Silva, 1989; Wehrly et al., 2007). For species of commercial interest, such as *C. multidentata*, which have been captured for the aquarium trade since the 1990s, information on the thermal tolerance, the acclimation and resilience capacities of adults but also of all other stages, will be useful for conservation purposes for wild populations (e.g. reintroduction, translocation plans), and ultimately for laboratory rearing and large-scale aquaculture initiatives that should ultimately reduce the harvesting of natural populations. A single recent study has provided data on thermotolerance in the early life stages of *C. multidentata* (Kondo et al., 2021), and the field remains unexplored for the majority of shrimp species. To date, only eight studies have examined CTMax during development in shrimp, covering post-larval and juvenile stages, with only one study involving larval stages (see detailed information and references in Supplementary Table 1). On a broader scale, the dataset for crustaceans, particularly freshwater crustaceans, needs to be expanded as current predictive models of the effects of climate change and possible changes in geographic distribution are based on very limited data for these groups, and in particular for Caridea shrimp. For example, the broad CTMax analyses by Cereja (2020) collected 457 data points of aquatic ectotherms divided into 292 points for marine species and 165 for freshwater species, the majority of the latter concerning fish and covering only 52 species of Malacostraca, including 13 species of Caridea. Adding more data on Caridean shrimp to these datasets may provide more accurate projections for these species.

## 5. Conclusions

Our study provides the first experimental data on the thermal tolerance of two atyid shrimp species, *Atyaephyra desmarestii* and *Caridina multidentata*. Both species demonstrate a high capacity for thermal acclimation, with critical thermal maxima (CTMax) increasing with acclimation temperature. This nevertheless only partially compensates for the increase in environmental temperature, and the thermal safety margin (TSM) may therefore end up being insufficient for these species to cope with temperature fluctuations such as heat waves. Furthermore, we addressed the limitations of the current indices (CTMax and TSM) for estimating warming tolerance. Long-term exposure to elevated temperatures, even if below the CTMax, impaired shrimp survival and may also have sublethal effects on reproduction and growth, impacting populations over time. Therefore, a multi-parameter approach (thermal limits, acclimation capacity, thermal safety margin, long-term survival, etc) is crucial for accurately predicting the impact of climate change on shrimp populations. Moreover, while temperature is a major stressor, other environmental factors like salinity and pollution may also interact with thermal tolerance. The development of a multifactorial approach that includes additional environmental factors present in the natural habitat of the shrimp will facilitate the elaboration of more accurate scenarios for the evolution of atyid shrimp populations.

Thermal tolerance data for Atyidae shrimp is scarce, with only a small fraction of species studied. This limits our ability to generalize about the vulnerability of the entire family. Future research should focus on expanding the thermal tolerance data for this group and investigating the combined effects of temperature with other environmental stressors. This will improve our understanding of atyid shrimp vulnerability and will ultimately inform conservation strategies.

### CRediT authorship contribution statement

**Juliette Ravaux:** Writing – review & editing, Writing – original draft, Visualization, Supervision, Methodology, Funding acquisition, Formal analysis, Conceptualization. **Olivia Bosc:** Writing – review & editing, Investigation. **Charles-Edouard Fusari:** Writing – review & editing, Supervision. **Sara-Mae Gricourt:** Investigation. **Maria Itin:** Investigation. **Michel Lestin:** Investigation. **Valentin de Mazancourt:** Writing – review & editing, Supervision, Methodology, Investigation,

Funding acquisition, Conceptualization.

### Data accessibility statement

The data generated in this study are provided as supplementary material: Data acclimation.xls, Data_CTM_Atyaephyra.xls, Data_CTM_Caridina.xls.

### Funding

Olivia Bosc's work was funded by a grant from the Institut de l'Océan, Alliance Sorbonne Université (Paris, France).

### Declaration of competing interest

The authors declare no competing or financial interests.

### Acknowledgements

The authors would like to thank the entire aquariology team at the Palais de la Porte dorée in Paris, and Jacky Yu (National Sun Yat-sen University, Kaohsiung, Taiwan) for kindly providing the picture of *Caridina multidentata*.

## Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.jtherbio.2025.104121.

### Data availability

No

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