Introduction

Marine ecosystems are amongst the most heavily invaded globally (Geburzi and McCarthy 2018) and marine bioinvasions are often associated with disturbance of native communities (e.g. Silva et al. 2021) such as disease and parasite introduction (Thieltges et al. 2008; Anouk Goedknegt et al. 2017), new predation and competition pressures (van den Brink et al. 2012), and new types of ecosystem engineering (Crespo et al. 2018). These disturbances may result in significant economic losses (Cuthbert et al. 2021). For a species to become invasive, it must pass through several stages in the invasion process (sensu Blackburn et al. 2011): after the initial introduction, survival and reproduction in the new environment need to lead to the establishment of self-sustaining populations, and further spread in the new environment must eventually expand its range. However, invasions can fail at all these stages if the environmental conditions in the new range are unfavourable. Temperature is known to be particularly important in this respect as it strongly influences physiology, ecology, and evolution of marine ectotherms (Nguyen et al. 2011a; Pinsky et al. 2019). Its importance as an environmental barrier in invasion processes is highlighted by the fact that warming is known to influence the range expansion of already established invasive species and affects general bioinvasion potential (Stachowicz et al. 2002; Raitsos et al. 2010; Elliott et al. 2015).

Among the invasive taxa that may be limited by temperature barriers are crustaceans, which are particularly conspicuous invaders in marine ecosystems (Brockerhoff and Mclay 2011). Recently, Swart et al. (2018) identified 56 species of predatory brachyuran crabs spreading outside their native range, and life-history traits such as reproductive strategies, plasticity, and behaviour have been proposed as drivers for the invasion success of brachyurans (Rato et al. 2021). In Europe, the vanurid Hemigrapsus takanoi was first identified as H. penicillatus in France in 1994, and its current distribution (Fig. 1) ranges from north–eastern Spain to the Swedish west coast, south–eastern England, western and eastern Scotland, and Germany (Karlsson et al. 2019). This invasive crab exhibits a short life cycle through fast growth, early sexual maturity, high adult mortality and high fecundity [recruits of Hemigrapsus spp. can be found mostly year-round (Forsström et al. 2018; Geburzi et al. 2018)]. These traits indicate a r-selected strategy, which may explain its invasion success (Gothland et al. 2014). Potential detrimental impacts such as interspecific and inter-cohort competition of growing populations of Hemigrapsus spp. on native shore crabs Carcinus maenas have been discussed in Europe (van den Brink et al. 2012; van den Brink and Hutting 2017), highlighting the importance of assessing the potential for further spread of H. Takanoi and for studies on the interspecific processes and dynamics that determine the outcome of competition between invasive and native crabs sharing an ecological niche (Rato et al. 2021). H. takanoi reaches high densities in the Wadden Sea in Germany and the Netherlands (Landschoff et al. 2013), where average water temperature ranges from ca. 15 °C in late spring to 20 °C in summer (van Aken 2008; Jacobs et al. 2020). Although identified in northwest Spain (Makino et al. 2017; Karlsson et al. 2019), the species has yet to be found in southern European waters which raises the question of whether warmer water temperatures may provide an environmental barrier to a further southward range expansion. Under warming, it is not known how the thermal performance of the invader – compares with the one of native shore crabs inhabiting southern Europe – close to upper thermal limit – and whether it would prompt competitive advantages should the invasive colonize the region or become eventually introduced.

Fig. 1
figure 1

Carcinus maenas (native) and Hemigrapsus takanoi (invader) distribution in Europe (above) and sampling locations of C. maenas (Óbidos Lagoon, Portugal) and H. takanoi (Mokbaai, The Netherlands). Species distribution model generated through presence-only data from GBIF (2024a, b) and Sea Surface Temperature (SST) through the MARSPEC dataset. Map lines delineate study areas and do not necessarily depict accepted national boundaries. Sampling map generated by QGIS 3.36, final composition on Inkscape 1.2

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In addition to survival and moulting events, feed intake and growth were also assessed under this 30-day exposure. It was a goal of this study to evaluate such parameters over a chronic exposure since they are often related to overall fitness, and competitive and reproductive advantages – providing a glimpse of species performance under stress scenarios. Therefore, the present study compared the thermal performance of young adults of H. takanoi sourced from its current distribution centre in Europe (The Netherlands), with young adults of the native C. maenas from a southern European population (Portugal) with the aim to determine the potential of H. takanoi to acclimate to a realistic southern thermal regime.

Materials and methods

Sampling and acclimation

This study uses crab populations with different latitudinal distribution and ecological status to test an introduction scenario. Both males (M) and non-ovigerous females (F) of the native C. maenas were collected in Óbidos Lagoon, Leiria, Portugal (39.419439, − 9.222647, Fig. 1), using a hand-held net during two diurnal low tides of the same week, and crabs were transported in dry containers to laboratory facilities (MARE Polytechnic of Leiria, Peniche, Portugal) for further acclimation and experimental procedures. Only organisms with a green carapace were collected due to potential physiological differences between green and red phenotypes (Wolf 1998).

Potentially invasive crabs H. takanoi were sourced from an invasive population in Mokbaai, Texel, The Netherlands (53.0064993, 4.766677, Fig. 1) in nearshore oyster beds. Males and non-ovigerous females were hand-caught during three consecutive diurnal low tides and transported in dry containers to laboratory facilities (CETEMARES, Peniche, Portugal). They were kept in a climate chamber, in natural seawater with additional aeration, shelter (macroalgae and terracotta pots), and small feed mussels to ensure animal welfare. After three days, crabs were packed and transported within a day by a professional aquarium trade company to the final experimental facilities in Portugal.

In Portugal, each crab species had its own life support system (LSS), a Recirculating Aquaculture System (RAS) equipped with mechanical (50 µm glass fibre bags, TMC, UK); Protein Skimmer QQ2 Nano, Bubble Magnus) and biological filtration (matured bioballs with nitrifying bacteria), in addition to UV sterilization (V2 Vecton 300, TMC, UK). For both species, males and females were always physically separated, and acclimated to natural seawater at 17 °C, salinity 34, pH ~8, dissolved oxygen (DO) from 6 to 8 mg. L−1 (YSI multiparameter probe – Professional Plus), 16:8 h light:dark photoperiod, and fed daily ad libitum with cockle meat (Cerastoderma edule). The organisms were acclimated to these laboratory conditions for two months, well above the 14 days proposed by guidelines for macroinvertebrates acclimation (E729 ASTM 2002). While a part of the individuals remained at 17 °C, two sets of male and female crabs of both species were divided and subjected to an acclimation ramp of 2 °C.day−1. Until reaching the desired thermal scenario of 21 °C or 25 °C (Supplementary material, S1). The experiment started the following day with crabs whose appendages were intact.

Experimental design and setup

A local thermal range of 17 °C, 21 °C, and 25 °C-resembling late spring minimum, mean, and maximum thermal records-was set based on in situ measurements, and recent thermal records and data modelling in Óbidos Lagoon, Portugal (Machado et al. 2018; Mendes et al. 2021). This thermal range is also realistic to other Southern European inlets and shallow water bodies inhabited by native Carcinus spp such as Ria Formosa (Portugal), Doñana wetlands (Spain), or Venice Lagoon in Italy (Newton and Mudge 2003; Morris et al. 2013; Amos et al. 2017; Rodrigues et al. 2021).

Both males (N = 9) and females (N = 9) of the two crab species were exposed to one of three temperatures (N = 18 per treatment-species combination, in a total of 108 crabs) (Supplementary material, S2): in the custom-built experimental setup, seawater temperature was manipulated in each header tank to 17 °C, 21 °C, or 25 °C (60L; V2PowerPump 2200, TMC, UK; Heater ThermoControl 400 W, EHEIM, Germany), and flowed to three trays (20 L, water bath) per header tank. Since room temperature was set to 19 °C, the 17 °C header tank was also equipped with a chiller (Chiller 300 A, HAILEA, China; Pump CompactON600, EHEIM, Germany). Due to their cannibalistic behaviour and to avoid competition stress, the organisms were exposed in separate glass containers, each with constant aeration and placed in the tray water bath. Each of the 9 trays contained 12 containers, 3 for each of species-sex’ combinations. The placement of trays and containers within trays was fully randomized.

Salinity was kept at 34 PSU, and a 16:8 h light:dark photoperiod was used. The experiment lasted for 30 days to enable the assessment of acclimation potential and performance. Aiming to assess responses in young adults of both species (Miyajima and Wada 2017; Young and Elliott 2020), the selected Carcinus maenas had 35.7 ± 2.7 mm carapace width (CW) and Hemigrapsus takanoi 10.4 ± 0,9 mm CW. Since C. maenas is a larger species, to maintain similar densities, they were individually exposed to the triple water volume (750 mL) compared to H. takanoi (250 mL) and water conditions similarly maintained (Table 1). An 80% daily water renewal was performed with filtered, UV-sterilized (V2 Vecton 300, TMC, UK) natural seawater, previously equilibrated to target temperatures. Prior to partial water change, the organisms were fed daily ad libitum with Cerastoderma edule meat for 4 h. In addition to thermal control in the header tanks, during this semi-static, long-term exposure, temperature was measured every 30 min through data loggers (EBI-20-TE1, EBRO, Germany) placed inside the glass containers of both species and all treatments. Other abiotic parameters were assessed and controlled daily, as presented in Table 1 (multiparameter probe-Professional Plus, YSI, USA; handheld pH meter, VWR, USA).

Table 1 Summary of abiotic parameter measurements (Mean ± SD) on the three thermal scenarios, for both species – Carcinus maenas (CM) and Hemigrapsus takanoi (HT) – during the 30 days exposure
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Data collection

Survival was assessed daily and expressed as the mean survival per tray, per treatment (%). Moulting events, if any, were also recorded and presented as the cumulative sum along the exposure.

On days 0, 14, and 29 of thermal exposure, each crab was placed on blotting paper to remove excess water, weighed on an analytical scale (nearest 0.0001 g) and the carapace width was measured with a vernier calliper to the nearest 0.5 mm. Similarly to Yuan et al. (2017), Moult Increment (MI,%) was calculated as the percentage of carapace increase at day 14 and day 29 of exposure, in the organisms that moulted: \(MI\left( \% \right) = \left( {CW_{x} - CW_{i} } \right)*100,\) where CWx is the carapace width after exposure to 14 or 29 days, and CWi means the carapace width in the first day of exposure. Weight gain (WG, %), was calculated as the percentage of wet weight increase in all organisms at day 29 of exposure: \(WG \left( \% \right) = \left( {Ww_{f} - Ww_{i} } \right)*100\), where Wwf is the wet weight in day 29, and Wwi the wet weight in day 0. Morphometric measurements were performed during partial water change to minimize handling stress.

After morphometrics, both C. maenas and H. takanoi were fed ad libitum for 4 h. Specifically for day 14 and day 29, voluntary feed intake (Nguyen et al. 2014) was inferred through standardization by the respective organism wet weight (mg. g Ww−1), to avoid bias due to differences in species’ sizes and therefore expressed as (A – B) *100/C, where A was the initial feed weight (mg), B the amount of feed remaining (mg) after 4 h, and C the wet weight of each crab (g). Excess feed moist was removed over blotting paper in both sampling moments.

Statistical analysis

Response variables were survival, feed intake, and weight gain variability and were modelled using Generalized Linear Models (GLM) in relation to the predictor variables temperature, species, sex, tray, and molting (the latter not applied to survival)-individual crab holding containers are the unit of replication in this study (Supplementary material, S3). Survival and feed intake were fitted with a linear distribution and weight gain fitted a gamma distribution with log-link. The models included the three-way interactions of temperature*species*sex/tray/moulting and all the possible two-way interaction combinations. A backward stepwise model selection procedure was employed. According to this procedure, non-significant interactions were sequentially removed from the model and the best fitting model selected based on Akaike Information Criteria (AIC) and visual comparisons of residuals plots. Moulting events’ data was modelled using logistic regression, fitting a binomial distribution (GLM). It ascertains and retrieves thermal influence on crab moulting likelihood. Negelkenke test, % of identified cases, and p values were used for data interpretation. Moulting Increment (MI) was analysed through a linear mixed model (LMM). Temperature and crab species were considered fixed factors and, sex, and tray nested as random factors. Pairwise post-hoc comparisons (Bonferroni) were run to test for individual differences between factor levels. Multicollinearity among variables was also taken into consideration (variation inflation factor-VIF) but not detected. Data plotting and analysis were performed on SPSS 27 (IBM), and aforementioned models’ criteria and validation followed standard recommendations (Zuur et al. 2007; Ho 2008). Where applicable, results are presented as mean ± standard deviation. For all statistical tests, the significance level was set to an alpha of 5%.

Results

Temperature variance was below ± 0.5 °C in all treatments (Table 1). Although temperature was the main target factor in this study, other abiotic parameters such as salinity, dissolved oxygen, and pH were also successfully controlled and maintained at target levels during the exposure (Table 1).

Survival

The potentially invasive Hemigrapsus takanoi showed 100% survival in all treatments when exposed to southern European thermal range scenarios (Fig. 2A). In contrast, the native Carcinus maenas showed a tendency of decreasing survival along the thermal range leading to differences between species (Waldspecies, df = 1, χ2 = 48.167, p < 0.001). C. maenas survived less than H. takanoi when exposed to 21 °C (Bonferroni, p = 0.006) and 25 °C (Bonferroni, p < 0.001) for one month. Since C. maenas males exposed to 25 °C survived significantly less (Bonferroni, p = 0.004) than females (33, 3% and 77, 8% respectively, Fig. 2B), there was a significant interaction with temperature (Waldtemperature*species*sex, df = 5, χ2 = 16.833, p = 0.005) and different sexes (Waldsex, df = 1, χ2 = 4.167, p = 0.041). A summary of the results is presented in Table 2.

Fig. 2
figure 2

A Survival (%) of Carcinus maenas and Hemigrapsus takanoi after exposure to a Southern Europe thermal range (17 °C, 21 °C, or 25 °C) for 30 days; B survival of Carcinus maenas females and males upon exposure to 25 °C.“*” Indicates differences between species (A) and C. maenas sex (B) in the 25 °C scenario (p < 0.05)

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Table 2 Summary of individual Carcinus maenas (native) and Hemigrapsus takanoi (potentially invasive) responses (mean) when exposed to a realistic local thermal scenario for 30 days: Survival, Moulting Events (ME), Moulting Increment (MI), wet Weight Gain (WG) and Feed intake at day 14 (FI14) and 29 (FI29)
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Moulting Events

In C. maenas a total of 4 individuals (out of 18) moulted in the treatments 17–25 °C (Fig. 3A), while in H. takanoi 66, 6% individuals moulted at 17 °C (12 of 18 organisms) and 94, 4% at 25 °C (17 of 18 organisms). It was observed that two H. takanoi moulted twice at 21 °C, with an intermoult period (IP) of 21 and 22 days. There was no influence of temperature on moulting likelihood for both species in the applied logistic regression model (p > 0.05). However, for H. takanoi, a tendency to increasing moulting events along the thermal range was observed, although barely significant (χ2 (2) = 4.891, p = 0.061). The model explained 14% of the variance in moulting events (Nagelkerke R2) and correctly classified 81.5% of the cases. Also, HT exposed to 25 °C seemed to moult earlier, with 14 out of 18 organisms moulting in the first half of the exposure (Fig. 3B).

Fig. 3
figure 3

Moulting events (cumulative sum) in Carcinus maenas (A) and Hemigrapsus takanoi (B) when exposed to a Southern Europe thermal range (17 °C, 21 °C, or 25 °C) for 30 days

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Growth: moulting and weight gain

Moulting Increment (MI) was c.a. 25% for C. maenas and not different among temperatures or sexes. However, it was generally higher than H. takanoi MI (GLM, F = 2.076, df = 1, p = 0.001). For the invasive H. takanoi, there was a tendency of an increase of MI along the thermal range (Fig. 4A) but there was no statistical difference between temperatures nor between sexes. H. takanoi showed higher relative weight gain than C. maenas (Waldspecies, df = 1, χ2 = 13.763, p < 0.001) (Fig. 4B), and H. takanoi exposed to 25 °C weighted significantly more than the ones exposed to 17 °C (Bonferroni, p = 0.002).

Fig. 4
figure 4

A Moulting increment (MI, %), and B Weight gain (WG) of Carcinus maenas and Hemigrapsus takanoi when exposed to a southern European thermal range (17 °C, 21 °C, or 25 °C) for 30 days.*Indicates overall differences between species, letters indicate differences between thermal scenarios for a given species

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Feed intake

H. takanoi showed higher relative feed intake than C. maenas (mg wet weight. g−1 crab) after both 14 (Waldspecies, df = 1, χ2 = 47.579, p < 0.001) and 29 days of exposure (Waldspecies, df = 1, χ2 = 50.100, p < 0.001). No differences were found between temperatures (Fig. 5A, B), sex, or moulting/non-moulting for the species C. maenas. On the other hand, in day 14, H. takanoi feed intake significantly increased with higher temperatures (Bonferroni, p < 0.001; Fig. 5A). At the end of the thermal exposure, no differences were found between temperatures, moulted/non-moulted organisms, or sex (Fig. 5B).

Fig. 5
figure 5

Feed intake of Carcinus maenas and Hemigrapsus takanoi in day 14, (A) day 29, (B) when exposed to a southern European thermal range (17 °C, 21 °C, or 25 °C) for 30 days.* Indicates overall differences between species, letters indicate differences between thermal scenarios for a given species

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Discussion

When exposed to realistic local thermal scenarios from southern Europe (21 and 25 °C), the native Carcinus maenas showed lower survival than the potentially invasive Hemigrapsus takanoi. The chosen thermal range, being close to the upper tolerance limit described for C.  maenas (Truchot 1973), coupled with the long-term duration of the experiment, and the absence of daily thermal stochasticity may explain these results. In natura, upon exposure to environmental forcing in the field, crabs exhibit thermoregulatory mechanisms such as burrowing and hiding behaviour, or migrating to deeper waters (Darnell et al. 2015; Vianna et al. 2020). In this experimental setup, such mechanisms were precluded and both species relied solely on their ecophysiology and acclimation capacity to the imposed temperature conditions. Despite being locally adapted to their environment (Tepolt and Somero 2014), native ectotherm populations may face detrimental effects upon thermally stressful conditions, especially in warm-adapted organisms living closer to their upper thermal limits. This supports the observations for C. maenas in this study and suggest that the species may be more susceptible to local extinctions (Nguyen et al. 2011b) or could be outperformed by invasive crabs that display wider thermal tolerance. In contrast, the observed 100% survival of H. takanoi to all thermal scenarios indicates a strong acclimation potential of young adult crabs to southern warmer regimes: these crabs were collected at ca. 15 °C in The Netherlands, acclimated, and exposed to an additional maximum of 10 °C (25 °C treatment), resembling the latitudinal thermal differences between both sampling sites in late Spring (IST and IPIMAR 2004; van Aken 2008; Machado et al. 2018; Jacobs et al. 2020; Mendes et al. 2021). Notably, at 25 °C, C. maenas males survived less than females, possibly suggesting dimorphic thermal tolerance, as previously described for C. maenas by Coile at (2019), and in other brachyuran species such as Pachygrapsus marmoratus (Madeira et al. 2012), Uca panacea (Darnell et al. 2015), or Minuca pugnax (Hews et al. 2021).

Carcinus maenas adult stages only moult 1 to 2 times per year (Klassen and Locke 2007) which may explain why moulting events were not affected by the exposure temperatures for the duration of the experiment – effects of longer chronic exposures to thermal scenarios fitting C. maenas upper thermal window have yet to be assessed and possibly pinpoint changes in moulting and development. In early adulthood, H. takanoi moults several times a year, concentrated in the warmer months, and associated to higher metabolic activity (Nour et al. 2020). In this study, H. takanoi showed a tendency to moult more and faster in the first 15 days of exposure, at higher temperatures. According to Gothland et al 2014, the field collected H. takanoi could in fact be from the same cohort due to their similar carapace length (± 0.9 mm SD). If so, possible effects on moulting response upon exposure to 25 °C should not be disregarded-although uncertain. C. maenas showed a mean Moulting Increment (MI) of 24.5%, which corresponds with records of 22% for a C. maenas population in Portugal of similar carapace length (36 mm) in the field (Yamada et al. 2005, Gomes et al. 1991), and values of 30% described for near-optimum laboratorial rearing conditions (Adelung 1971). In general, the MI was higher in C. maenas than in H. takanoi. However, this is typical of larger crab species (Fukui 1964) and not specifically correlated with thermal treatments since no differences were found among the tested temperature range. However, H. takanoi showed a tendency of an increasing MI along the thermal range. The combination of quality feed and higher temperatures may increase crab metabolism (Gaitán-Espitia et al. 2017), and decrease intermoult period with variable effects on MI (Yuan et al. 2017).

The present study assessed feed intake through de-shelled prey (cockle meat) and standardization by individual crab weight. By eliminating interference of prey shell size or hardness, claw size and strength difference between males and females or individual crabs, this methodology can be considered a sensitive proxy for measuring specific feed intake through direct biomass consumption. Overall, H. takanoi showed higher feed intake than C. maenas in both assessments (day 14 and day 29), with invasive crabs being consistently more voracious than the native species. Advantages on foraging behaviour were described for H. sanguineus, another invasive vanurid in Europe (and North America), where non-starved crabs exhibited an exogenous day-night rhythm and starved crabs lacked photophobic behaviour, which could allow them to spend more time foraging than species characterised by true endogenous rhythms such as C. maenas (Spilmont et al. 2015), potentially increasing these invaders’ competition for food and overall fitness. Competition for food with C. maenas was described for invasive populations in the USA (Jensen et al. 2002; BD et al. 2008). In addition, prey size selection, and possible effects of Hemigrapsus spp. on native prey were also assessed by several other authors (Brousseau and Baglivo 2005a; Doi et al. 2009; Brousseau et al. 2014; Waser et al. 2015; Bouwmeester et al. 2020; Cornelius et al. 2021). As responses may vary between populations, such functional studies are of paramount importance to assess invasive or newly arrived species effects on ecosystems or food webs (Nour et al. 2020), namely when environmental conditions differ or change. In the midterm of the exposure (day 14), C. maenas showed a non-significant but higher feed intake in the highest thermal scenario (25 °C). The invasive H. takanoi showed significant higher feed intake along the thermal range. In fact, increased metabolism due to pre-moult/post moult or warmer temperatures may increase feed intake in crustaceans (Yuan et al. 2017): since no significant contribution of moulting was found for feed intake, the data suggests higher metabolic demand upon exposure to higher temperatures. When physiological thresholds are reached, namely due to thermal stress, metabolic rate depression (MRD) may occur, as well as supressed mitochondrial capacity/activity and further damage in crustaceans (Sokolova 2018, 2021; Oellermann et al. 2020), which may explain C. maenas response to thermal scenarios in the present study, associated to lower survival. On day 29, close to the end of exposure, H. takanoi showed no differences in feed intake among thermal regimes, suggesting a decrease in metabolic demand for the species and possibly acclimation to such conditions. Hemigrapsus spp. feed upon mussels, oysters, and soft-shell clams (Bourdeau and O’Connor 2003; Brousseau and Baglivo 2005b; Brousseau et al. 2014), especially juvenile and smaller prey sizes. High population density of over 200 individuals m2 (Cornelius et al. 2021) and species-specific voracity – supported by the present study – may pose detrimental effects on bivalve spat recruitment and mariculture, and potentially reduce natural stocks or industry revenue.

Overall weight gain (day 29) was higher in H. takanoi than in C. maenas, especially in H. takanoi exposed to 25 °C. These findings may be correlated with moulting events to some extent since organisms’ uptake water for ecdysis, and wet weight was assessed (instead of dry weight). However, Nguyen et al (2014) meticulous assessment of the moulting cycle of the mud crabs Scylla serrata, also fed daily ad libitum, suggests that crabs gain ca. 16.5% more tissue two days after ecdysis and lose around 25% water content between the maximum water content 24 h after ecdysis (c.a 85%) and the baseline reached further on until the next moulting event (c.a 60%), reducing significantly the role of water uptake on weight gain few days after moulting-in this experiment, most of the organisms moulted in the first half of the experiment. Therefore, instead of the contribution of moulting events and water uptake to weight gain, the increase in H. takanoi weight, namely at 25 °C, may be explained by the higher feed intake and metabolism, and supported by the tendency to higher MI – that increases under optimum rearing conditions.

Invasive populations, namely of smaller species, may have higher feeding and metabolic rates than natives (Howard et al. 2018) upon introduction (Lagos et al. 2017) and outperform natives under warmer scenarios (Nguyen et al. 2011a; Crespo et al. 2018), which is supported by the results found in this study. If that translates into increased moulting frequency and growth, often coupled to reproduction success, then warmer regimes may be expected to extend Hemigrapsus takanoi reproductive season (as mentioned in McDermott 1998; Van Den Brink et al. 2013) and latitudinal distribution, raising concerns on increasing propagule and ecosystem pressure in non-invaded areas or additional pressure in the ones already invaded but expected to endure projected global warming scenarios (IPCC 2021).

When colonizing a new geographical area, the organisms adjust their physiological state to the newly encountered conditions, often surpassing a series of biotic and abiotic filters, and mechanisms to reach invasiveness (Blackburn et al. 2011; Rato et al. 2021). In the invaded range, Hemigrapsus spp. thrive in natural and artificial structures such as mussel and oyster beds, and harbours (Klassen 2012; Gothland et al. 2014; Geburzi et al. 2018)-also found in the non-invaded southern European waters. Therefore, their non-identification may be just a matter of time or correlated to other biotic or abiotic filters, yet to be addressed. In addition, despite the lower salinity regimes in Northern European countries reporting high H. takanoi densities, the local pH, DO, and higher salinities (34) were tolerated in this life stage (euryhaline)-as also found by Nour et al (2021). The same authors described a salinity threshold for H. takanoi larval development and settlement (≥ 20, stenohaline stages) in the Baltic Sea, suggesting ontogeny-related vulnerability to environmental conditions and local limitations to propagule pressure that would not be found in southern areas. In fact, it was demonstrated that Carcinus maenas juveniles were more tolerant to emersion and warmer temperatures than the adult stages – who preferably seek shelter and immersion, especially during thermal stress. While the physiology of C. maenas is relatively well studied, to the point of the species being proposed as an ecotoxicological model (Rodrigues and Pardal 2014), the same does not apply to Hemigrapsus spp. invading populations in Europe-emphasizing the need to assess species’ ontogeny-related plasticity and performance under changing environments.

The results shown in this study support the conceptualization that young adults of H. takanoi would not only survive but tolerate southern European thermal ranges (and salinities) by surviving, growing, and showing higher overall fitness whereas the native C. maenas underperforms under the same imposed conditions. These thriving remarks on southern European thermal ranges may also pinpoint the need to further investigate the dynamics among invaders and other native species (e.g. with C. aestuarii in the Mediterranean) under rapidly changing environments and highlight the usefulness of such experimental approaches to assess native versus invasive life-history and functional responses to realistic thermal scenarios but also denote predictive ability involving biota and ecosystem effects.

Concluding remarks

Biological pollution, bioinvasions, and warming are set to increase in marine and coastal systems in the forthcoming decades, mainly due to anthropogenic activity and mediation. The results here presented suggest that warmer regimes may not deter both Hemigrapsus takanoi males and females’ establishment and spread upon introduction to newly encountered areas. Additionally, concerns may be greater given the underperforming native species, that showed a narrower plastic response under the imposed experimental conditions. In fact, voracious invasive crab species may decrease native species biodiversity and negatively impact socioeconomic revenue due to food web disruption through competition for a pre-established ecological niche and promote communities’ composition disturbance.

The competitiveness of H. takanoi over native species has been validated in situ to some extent, as aforementioned, and further mechanisms of invasive success addressed. Hemigrapsus takanoi feed upon small crustaceans and bivalves – some of them key marine resources to fisheries and mariculture such as mussels and clams. In addition to its ecological relevancy, in Portugal, Carcinus maenas has economic interest as bait for fisheries, and human consumption. Still of least interest in Europe, H. takanoi situation is much different from the one mentioned to the native C. maenas, or the invasive blue crab Callinectes sapidus which is now a fisheries’ resource in Italy (Mancinelli et al. 2017). In the USA, biotic resistance was demonstrated by C. sapidus preying upon C. maenas invasive populations, significantly limiting its abundance and distribution (DeRivera, 2005). Therefore, in situ deleterious impacts of invasive species may be naturally mitigated, but also mitigated through management plans and incentives (Pasko and Goldberg 2014). Mitigation measures targeting H. takanoi will be less spontaneous unless specific directives are proposed and implemented due to their small size and apparent low gastronomic value, and usage as bait.

Bioinvasions are a complex topic and integrative of a myriad of factors that should be addressed to better understand this phenomenon which poses biodiversity and socioeconomical impacts. Thus, in addition to life history traits and function, future studies should evaluate their ecophysiology and privilege integrative approaches (Rato et al. 2021) at several levels of biological organisation (Lemos 2021) to assess the marginal gains and underlying mechanisms leading to invasive success. Current findings suggest that further addressing invasive populations’ ecophysiology would be timely and relevant, namely regarding thermal windows or energy metabolism-related endpoints-translating ecophysiological data outputs into valuable knowledge which enables policymakers to advance informed management and/or mitigation policies regarding invaders.

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

Although not mandatory for invertebrates in Portugal, ethical procedures under experimental bioassays were taken into consideration (113/2013; 2010/63/EU; Diggles 2019), as well as crustacean welfare through the implementation of an euthanasia protocol preceding both sacrifice and dissection. Tests were performed under controlled laboratorial conditions and biosecure facilities.