Inter-specific and inter-individual trait variability matter in surface sediment reworking rates of intertidal benthic foraminifera

Although benthic foraminifera are an important component of meiofauna and contribute to carbonate production and carbon/nitrogen cycles, their role in bioturbation processes remains poorly known. Five dominant intertidal benthic foraminiferal species were recently classified into functional bioturbator groups according to their sediment reworking mode and intensity. Our study aimed at identifying potential drivers (i.e. size and/or travelled distance) of species-specific surface sediment reworking rate. The travelled distance and surface sediment reworking rate of Haynesina germanica, Cribroelphidium williamsoni, Ammonia tepida, Quinqueloculina seminulum and Miliammina fusca were assessed through image analysis. Our results show that the surface sediment reworking performed by these species is not size-dependent, but dependent on their motility traits through interspecific differences in the travelled distance. Smaller species (i.e. Quinqueloculina seminulum and Haynesina germanica) contributed more to surface sediment reworking than larger ones (i.e. Ammonia tepida, Cribroelphidium williamsoni and Miliammina fusca). These observations stress the critical role of motion behaviour in surface sediment reworking processes by intertidal foraminifera. Finally, we stress that the high inter-individual variability observed in conspecific motion behaviour may be important to decipher the role of foraminifera in sediment bioturbation. Noticeably, the species characterized by a strong inter-individual variability are also the species that have the highest surface sediment reworking rates. This last observation may inform on the species-specific phenotypic plasticity and, therefore, the potential for the functional role of these species to be maintained in their natural environment. This is particularly relevant in an era of global change where ecosystem balance is increasingly threatened by various stressors such as heat-waves, ocean acidification and pollution.


Introduction
Bioturbation activities of benthic fauna contribute to the structure and functioning of most marine soft-sediment ecosystems; see Kristensen et al. (2012) for a review. Sediment particle reworking typically drives (i) substrate physical properties such as granulometry and erodibility and (ii) bacterial communities (Orvain et al. 2003(Orvain et al. , 2004. This process affects chemical gradients and increases dissolved fluxes at the sediment-water interface (Orvain et al. 2004;Kristensen et al. 2012;Schratzberger and Ingels 2018;Bonaglia et al. 2020). Overall, bioturbation contributes to the mineralisation of organic matter; thereby enhancing carbon and nutrient cycling (Aller 1994;Mermillod-Blondin and Rosenberg 2006;Meysman et al. 2006;Kristensen et al. 2012).
Meiobenthos refers to organisms that are retained in the size fraction between 63 and 1000 µm (Mare 1942;Hulings and Gray 1971;Higgins and Thiel 1988). Their role in bioturbation processes has received an increasing amount of attention over the last decade. Beyond the fact that they may be more abundant, diverse and resilient to environmental disturbances than macro-invertebrates (Gerlach 1978;Bouchet et al. 2018, their contribution to sediment reworking and bio-irrigation is non-negligible compared to those of macro-invertebrates (Rysgaard et al. 2000;Gross 2002;Näslund et al. 2010;Bonaglia et al. 2014;. Through their movement and feeding activity, meiofaunal organisms further structure and constrain microbial communities that are crucial for organic matter mineralization (De Mesel et al. 2004;Moens et al. 2005;Nascimento et al. 2012). They also affect the oxygen penetration depth, increasing solute transport (e.g. sulphides) into the sediment (Aller and Aller 1992;Rysgaard et al. 2000;Bonaglia et al. 2020). For instance, in an intertidal mudflat, nematode displacements have been shown to stimulate microphytobenthos accumulation in the surface biofilm leading to a shift in diatom community (D'Hondt et al. 2018). Taken together, these observations strongly suggest that the role of meiofauna in bioturbation processes needs to be urgently considered in studies dealing with benthic ecosystem functioning as they play an important role in soft-sediment ecosystems (Näslund et al. 2010;Nascimento et al. 2012;Bonaglia et al. 2014Bonaglia et al. , 2020. Traditionally, foraminifera have been overlooked in studies assessing total meiofaunal bioturbation, mostly because these works only considered metazoan meiofauna (Schratzberger and Ingels 2018). These abundant and diverse organisms in intertidal mudflats are able to significantly alter sediment structure through the creation of burrows and cyst building both at the interface and deeper into the sediment (Severin and Erskian 1981;Kitazato 1988Kitazato , 1994Chandler 1989;Green and Chandler 1994;Gross 2000Gross , 2002Deldicq et al. 2020), leading to sediment mixing (Gross 2002). Surface sediment reworking rates of the intertidal foraminiferal species Ammonia tepida and Quinqueloculina seminulum were recently shown as comparable to those of macrofaunal species . These observations highlighted the non-negligible importance of benthic foraminifera to contribute to sediment reworking processes. Furthermore, meiofauna (including foraminifera) can increase rates of solute transport and stimulate aerobic decomposition and nitrification processes in the oxic zone (Aller and Aller 1992;Aller 1994;Bonaglia et al. 2020). Recently, five dominant intertidal foraminifera have been classified in distinct functional groups (e.g. surficial-, epifaunal-and gallery-biodiffusors; see Deldicq et al. 2020) that underpinned their differences in the type and intensity of sediment reworking. Distinct species-specific behavioural patterns related to their displacement both within the sediment and at the sediment-water interface were, therefore, hypothesized to differently affect sediment reworking rates .
These preliminary results on the potential of benthic foraminifera to contribute to bioturbation processes emphasize the need to further estimate surface sediment reworking rates of foraminiferal species to better understand their role in benthic ecosystem functioning. In this context, the specific objectives of this study were (i) to estimate individual surface sediment reworking rate (hereafter referred as SSRR i ) of five dominant intertidal foraminifera species in temperate intertidal mudflats, (ii) to understand how morphological traits or those related to their displacements would influence SSRR i and (iii) to further link these traits and SSRR i intensity to the functional groups recently introduced for benthic foraminifera ).

Studied species
Five intertidal species were selected considering their high abundance in the foraminiferal assemblage at the study site: (i) the prolate ellipsoid-shaped Quinqueloculina seminulum and Miliammina fusca (Fig. 1a, b), (ii) the trochospiral Ammonia tepida (Fig. 1c) and (iii) the planispiral Haynesina germanica and Cribroelphidium williamsoni (Fig. 1d,e). In contrast to the other species that have a calcareous shell, Miliammina fusca is an agglutinated species.
Note that C. williamsoni, H. germanica and A. tepida may co-occur with species that are morphologically identical though they are genetically distinct (Pawlowski et al. 1995;Hayward et al. 2004;Saad and Wade 2016). Despite morphological similarities, those species may have different ecological requirements (Richirt et al. 2020), hence different behavioural traits. Molecular identification is, therefore, needed to discriminate morphospecies before the assessment of their behavioural traits. In our sampling site, we find H. germanica S16, C. williamsoni S1 and A. tepida T6 (Schweizer M., personal communication). Depending at the abundance at the time of sampling, between 8 and 33 individuals per species were used for the experiment (Table 1). Please note that conspecifics of each species were similar in size, i.e. with uniform length and width of the test. The size of prolate ellipsoid-shaped species (i.e. M. fusca and Q. seminulum) ranged between 500-700 µm and 450-650 µm in length and 250-350 and 200-300 µm in width, respectively. For the trochospiral species A. tepida, both length and width ranged between 450-650 µm. Finally, the size of planispiral species (i.e. C. williamsoni and H. germanica) ranged between 450-650 and 350-550 µm in length and 350-550 and 300-500 µm in width, respectively.

Sediment sampling and experimental set-up
Sampling was performed in the Authie Bay (50°22′20″N, 1°35′45″E) which is an intertidal mudflat located on the French coast of the English Channel. This estuary is a well-preserved area that is sparsely populated and slightly impacted by industrial and recreational activities (e.g. Henry et al. 2004). It is characterized by a semidiurnal macrotidal regime where tidal range can exceed 10 m during highest astronomical tides (McLusky and Elliott 2004). Among the intertidal zones located along the northern part of the French coast, the Authie Bay is the one displaying the highest diversity in foraminiferal species (Francescangeli et al. 2020).
Surface sediment (0-1 cm) was collected from February to June 2018 at low tide and stored in plastic containers (100-ml). Samples were then transported to the laboratory, where it was washed through a > 125-µm mesh-size sieve. During the sampling period, temperature has increased from ~ 7 °C (February) to ~ 18 °C (June), which may have induced a seasonal effect on the organism' activity as evidenced for macrofaunal species (Pascal et al. 2019). A recent study on Haynesina germanica showed, however, that the species' SSRR i has a low thermal dependence in the range 6-24 °C (Deldicq et al. 2021). In this study, we assume that the potential seasonal effect could be negligible through the use of an acclimation period carried out before running the experiment. Hence, living benthic foraminifera were subsequently individually sorted with a brush, identified and their pseudopodial activities checked under an inverted phasecontrast microscope (Olympus IX71, Tokyo, Japan). Only active individuals were subsequently imaged to measure the shell size parameter, i.e. maximum length and width of each individual (Olympus SZX16, Tokyo, Japan, TC capture software).
Behavioural observations were performed in 300-ml aquaria filled with 25 − 30-ml of thawed Authie Bay sediment (i.e. ~ 1 cm thick) (Fig. 2). We used previously frozen sediment to ensure that the sediment was free of moving macroand meio-organisms so that the only tracks observed on the sediment surface would be those from foraminifera.

Quantification of behavioural traits
After the acclimation period, foraminifera were randomly placed on the sediment surface ( Fig. 2), under 250-ml of  natural unfiltered and air saturated seawater (salinity = 33) following 10 min of vigorous air bubbling immediately before spreading foraminifera on the sediment surface. In total 15 experiments were performed. Individual displacements in and on the sediment were recorded by time-lapse photography ( Fig. 2; 1 image every 10 min for 24-h) using a digital camera (Nikon V1 with a Nikkor 10-30 mm lens). For each foraminifera, 144 images were combined in the image-analysis software Fiji to extract (x,y) coordinates using the Manual tracking plugin (Schindelin et al. 2012). A total of 230 active (i.e. moving) individuals was initially selected for the experiment. Please note that the majority of living individual initially deposited at the sediment surface moved during the experiment but the coordinates could not be extracted for all individuals. Indeed, during the experiment, it was not possible to track all individuals (i) because some burrowed into the sediment up to a depth where their paths were not visible and/or (ii) because some paths crossed and consequently individual trajectories were lost. We, therefore, only kept individuals that exhibited visible tracks throughout the whole 24-h experiment so that the information related to their behavioural traits had the same statistical weight. In total we followed the trajectories of 103 individuals. Note that at the end of each 24-h experiment, dissolved oxygen saturation was consistently ca. 56% in the overlying seawater directly above the sediment-water interface (HI9829 MULTIPARAMETER Meter, HAN-NAH INSTRUMENTS).
The distance travelled by each individual between two images (i.e. 10 min) was calculated as: where (x t ,y t ) and (x t+10 , y t+10 ) are the coordinates between two successive images taken at times t and t + 10 min, respectively. The total distance travelled within 24 h, D 24 , was subsequently calculated by summing individual D t .

Quantification of surface sediment reworking rates
To estimate the surface sediment reworking rate of intertidal foraminifera we used the calculation method previously used for macrofaunal species such as sea urchins (Hollertz and Duchêne 2001;Lohrer et al. 2005;Maire et al. 2008): where DT is the distance travelled during a time interval Δt and CS the cross section, i.e. surface reworked along the motion plane (Maire et al. 2008, see Fig. 3A, for an example). This calculation method was recently applied on two intertidal foraminiferal species, i.e. Ammonia tepida and Quinqueloculina seminulum . Nevertheless, in their calculations, the authors used the maximum test length rather than the cross section as the morphological component. However, test length may not be optimal as some foraminifera such as Q. seminulum and M. fusca, have asymmetrical shapes with test length greater than test width (Fig. 1a,b). Noticeably, the length/width ratio is close to 1 for A. tepida, 1.2 for H. germanica and C. williamsoni and to 2 for Q. seminulum and M. fusca. The use of the surface area, therefore, appears to be more accurate for the calculation. However, measurement of the cross section involves the characterisation of the organism' height ( Fig. 3). Due to their small size, foraminifera are manipulated under binocular microscope that makes very difficult to measure their cross section as it involves a vertically positioning of the individual (Fig. 3B). We, therefore, assume that the surface area corresponding to the larger part of the test, i.e. umbilical sides may be used for the estimation of the surface sediment reworking performed by foraminifera. Hence, using the measurements of maximum length and width (see Sect. 2.2), the surface area (mm 2 ) of each individual (S i ) was estimated under the assumption of an ellipse-shaped shell: Since we used conspecifics of similar size, the mean surface area S for each species was then calculated and subsequently used for the calculation of the individual surface sediment reworking rate (SSRR i(t) , mm 3 ind −1 10 min −1 ) as follow: where D t is the distance travelled (mm ind −1 d −1 ) by each individual between two images (i.e. 10 min).
In our experiments, individuals of both species can move on the surface (Fig. 4A), at the interface (Fig. 4B) or in the sediment (Fig. 4C).
When the individual was observed crawling at the sediment surface or at the interface only 1 3 and 1 2 of the mean surface area S was considered in the SSRR i calculation, respectively (Fig. 4A, B). Conversely, when the individual was observed burrowed in the sediment, the total of the mean surface area S was used (Fig. 4C). Finally, the individual surface sediment reworking rate (SSRR i , mm 3 ind −1 day −1 ) were estimated as follow: where SSRR i(t) is the individual surface sediment reworking rate between two images (i.e. within 10 min).

Data analysis
Because the surface area of individual foraminifera, their travelled distances and SSRR i were non-normally distributed (Shapiro-Wilk test, p < 0.05), a Kruskal-Wallis test was applied to infer the presence of significant differences between species, and eventually followed by a Dunn test to identify distinct groups of measurements. All statistical analyses were performed using R.3.5.2. software (R Core Team 2019).

Species-specific size
In our experiment, the mean surface area of A. tepida is almost twice as large as those of H. germanica and Q. seminulum (Table 1). Indeed, there were significant Cross secƟon A B Fig. 3 Illustration of the cross section of (A) polychaete and (B) benthic foraminifera that may be used for sediment reworking calculation

Travelled distance
Among the five studied species, Q. seminulum display the highest mean travelled distance, i.e. 130 mm d −1 with all individuals being in the range 12-145 mm.d −1 . In contrast, M. fusca and A. tepida are the species that travelled the least distances, i.e. between 12 and 32 mm d −1 and 17 and 37 mm d −1 , respectively (Fig. 5). With intermediate values, the mean travelled distance of H. germanica and C. williamsoni ranged between 16 and 112 mm d −1 and 19 and 67 mm d −1 (Fig. 5). Hence, three groups of homogeneous travelled distance were identified: Our results showed a strong intra specific variability in the distance travelled by individuals of H. germanica, C. williamsoni and Q. seminulum. For instance, the travelled distance between individuals of Q. seminulum may range from 12 to 142 mm d −1 (Fig. 5).

Surface sediment reworking rate
Individual surface sediment reworking rates ranged from 1.15 mm 3 day −1 for M. fusca up to 21.6 mm 3 day −1 for Q. seminulum, and significantly differed between species (KW test, p < 0.05; Fig. 6). Quinqueloculina seminulum showed higher SSRR i than the other species (Dunn test, p < 0.01).
Three groups of SSSR i were subsequently identified as S SRR i -A. tepida = SS RR i-M. fusca < SSR R i-C. williamsoni = SSRR i-H. germanica < SSRR i-Q. seminulum ( Fig. 6; Dunn test, p < 0.01). As a consequence, the most and the least efficient surface sediment reworkers are Q. seminulum and M. fusca, respectively. As previously evidenced for the travelled distance, SSRR i values showed a strong intraspecific variability in H. germanica, Q. seminulum and C. williamsoni species. Noticeably, the difference in the SSRR i between individual of the aforementioned species may be one order of magnitude while it is restricted between 1 and 3 mm 3 day −1 for M. fusca (Fig. 6).

A methodological note on individual surface sediment reworking calculation
In the present work, SSRR i was estimated using the surface area of the test, whereas  considered the test length in their calculation. Hence, these authors showed SSRR i values expressed as a surface unit, i.e. in cm 2 ind −1 d −1 . However, the studied foraminifera moved in and on the sediment, hence were ipso facto displacing a volume of particles rather than a surface. The use of the surface area of the test instead of the maximum test length, therefore, appears as more ecologically relevant allowing to express SSRR i as volume of sediment particles displaced. Furthermore, the prolate ellipsoid-shaped test of Q. seminulum and M. fusca are asymmetrical with the length much longer than the width. Similarly, within rotaliid species, i.e. A. tepida, H. germanica and C. williamsoni test length typically is about 1.2 times larger than test width. As a consequence, the approach followed by  most likely leads to a biased estimation of the SSRR i values by considering only the length as representative of the test size.  We further stress that the use of the larger surface area of the test is consistent with the surface involved in the burrowing behaviour of planispiral and trochospiral species. In our experiment, planispiral species, i.e. H. germanica and C. williamsoni burrowed in the sediment by successively orienting both their umbilical and apertural sides perpendicular to the direction of movement (Fig. 7A, B). Additionally, as previously observed (i.e. Langer et al. 1989), trochospiral species such as A. tepida moved with a corkscrew movement with its umbilical side oriented toward the direction of the displacement. The aforementioned species have ornamentations (e.g. pores, interlocular spaces and spikes) that have been expected to influence the displacement of foraminifera within the sediment (Langer et al. 1989). The pseudopodial network may then be extended outside the shell through ornamental features. Therefore, both shell surfaces, i.e. apertural, spiral, umbilical, are likely to be involved in the displacement of these foraminiferal species. In contrast, prolate ellipsoid-shaped species such as Q. seminulum and M. fusca burrowed in the sediment with their mouth oriented toward the direction of displacement (Fig. 7C).
These observations indicate that the apertural side (i.e. the cross section) is likely to be the surface that is essentially involved in the displacement of Q. seminulum and M. fusca, which, therefore, may lead to an overestimation of SSRR i in the present study. Such observations were, however, made during the burrowing process of these two species as they never reached the sediment surface and remained burrowed in the sediment throughout the rest of the experiment ). This may not necessarily suggest that it is the only side involved in the displacement hence the sediment reworking. In addition, all studied foraminiferal species left a track in the sediment that is greatly larger than the individual width (Fig. 8). This observation is consistent with the above-mentioned potential underestimation of the SSRR i of these two species.
In the present study, we consider the temporal evolution in the vertical position of each individual in our SSRR i calculation. This method allows a more rigorous estimation of the surface sediment reworking intensity of each species as it considers the real portion of the surface area of the test that is actively involves in the reworking of surface particles during individual displacement (Fig. 4).
Taken together, these observations suggest that considering both the surface area of the test as a proxy of foraminiferal test size and the position of each individual in the sediment may allow a reliable assessment of species-specific surface sediment reworking rate. However, behavioural observations dealing with the functional morphology of prolate ellipsoid-shaped species are needed to further identify which surfaces areas of their test are involve in the displacement of sediment particles.

SSRR i is not size-dependent but trait-dependent through interspecific differences in motion behaviour
Our results showed that the largest foraminiferal species (A. tepida) did not rework the sediment more than the smallest species such as H. germanica and Q. seminulum. In contrast, Q. seminulum can even rework up to three times more sediment than the larger A. tepida (Fig. 6) despite a test surface area nearly half that of A. tepida (Table 1). This result indicates that the species-specific SSRR i could be inversely size-dependent as evidenced in the five species. Specifically, the higher the surface area of the test, the lower the species-specific SSRR i . Here, the travelled distance is likely the parameter that drives the intensity in the surface sediment reworking performed by the five foraminiferal species. These results are consistent with previous works on macro-invertebrate species, where large bivalves may have lower sediment reworking rates than small polychaetes since the latter have more intensive displacements, i.e. different motion-behaviour traits (Mermillod-Blondin et al. 2004;Michaud et al. 2005;Gilbert et al. 2007). Furthermore, differences in SSRR i between foraminiferal species have been previously hypothesised following the assumption that species with distinct bioturbating modes would exhibit different SSRR i ; see Deldicq et al. (2020) for further details. Noticeably, the five species considered in the present study were recently classified in the following bioturbating groups: Q. seminulum and M. fusca as gallery-biodiffusors, H. germanica and A. tepida as surficial-biodiffusors and C. williamsoni as an epifaunal-biodiffusor . This classification implies that they would contribute differently to benthic-ecosystem functioning . For instance, C. williamsoni that prefers surface sediment was classified as epifaunal-biodiffusor meaning that the species would rework particles at the surface. In contrast, H. germanica and A. tepida move in and on the sediment, hence they may rework particles more deeply than C. williamsoni . Finally, Q. seminulum and M. fusca prefer to be burrowed in the sediment that may likely induce the reworking of sediment particles below the interface. As these species do not occupy the same microhabitat, they may consequently exhibit differences in their SSRR i . Therefore, to consider the functional classification of the five studied species in the estimation of their SSRR i , we include the position of their test in the sediment.
Based on this study's findings, it occurs that, although C. williamsoni is larger than H. germanica and that both species displayed similar travelled distance, the latter rework A B Fig. 8 The position of the individual at the beginning of the experiment indicated by the red circle. B Visual observation of the width of the path that is greatly larger than the individual width during the displacement of Q. seminulum after 24 h of experiment. Scaled bar = 0.5 cm the surface sediment more efficiently. This is consistent with previous studies which showed that gallery-biodiffusor (i.e. burrow-dwelling organism) macro-invertebrates are more efficient bioturbators than epifaunal-biodiffusors as they displaced a larger amount of sediment particles through their burrowing activity (Mermillod-Blondin et al. 2004;Michaud et al. 2005). However, in the present study, the most and the least efficient species in reworking surface sediment (i.e. Q. seminulum and M. fusca) both belong to the gallery-biodiffusor group. As a consequence, the potential link between the intensity of surface sediment reworking and the functional group of a species is not straightforward. We may suggest that the motion behaviour of foraminifera, i.e. travelled distance and vertical position (e.g. Deldicq et al. 2020) both matter in their ability to rework surface sediment.
In macrofauna, species-specific sediment reworking rate is intrinsically linked to abiotic and biotic factors such as food concentration, temperature and chemical properties of the sediment (Przeslawski et al. 2009, Maire et al. 2007aMestre et al. 2013;Verdelhos et al. 2015;Bernard et al. 2016;Pascal et al. 2019). In the present study, the experimental set-up do not provide all the food sources such as live prey that some species, e.g. A. tepida may feed (Dupuy et al. 2010;Jauffrais et al. 2016) as we used thawed sediment to eliminate macro-and meiobenthic bioturbation effects. Foraging activity is, however, intrinsically linked to organism displacement (e.g. Pyke 1984;Bell 1991;Seuront 2010Seuront , 2015. This stresses the need to further investigate the effect of food concentration and diversity on the SSRR i of intertidal foraminifera. In addition, the effect of progressive oxygen depletion on foraminiferal activity hence sediment reworking intensity should be further investigated although we did not observed temporal changes in the activity of our five species during our experiments.

Inter-individual variability matters in the contribution of benthic foraminifera to SSRR i
Beyond the interspecific variability discussed above (Sect. 4.2), SSRR i of the five studied species were consistently characterised by inter-individual variability (i.e. up to one order of magnitude for Q. seminulum; see Fig. 5,6). Note that the differences identified here cannot be related to environmental factors or size, since our experiments were performed on similar-sized individuals under controlled conditions in the absence of any cues. The above mentioned inter-individual variability is then more likely to be an intrinsic property of the species considered here.
Behavioural plasticity has previously been reported in foraminifera (Hallock and Hansen 1979;Seuront and Bouchet 2015;Prazeres et al. 2017), but also in pelagic copepods (e.g. Seuront et al. 2004) and intertidal gastropods (e.g. Chapperon and Seuront 2011) with individuals from the same species showing both a large repertoire of behavioural traits (e.g. feeding activity, trajectory complexity, intensity of displacement) and a large variability in the values of each trait. Noticeably, in our experiments, conspecific individuals of Q. seminulum, C. williamsoni and H. germanica displayed a high variability in their travelled distance but also in their motion behaviour, e.g. tortuosity, vertical position (see Deldicq et al. 2020 for further details). Please note that the lowest inter-individual variability was observed for M. fusca and may result from the analysis of only 8 individuals.
Having a wide diversity in the behavioural repertoire between conspecific individuals may be a selective advantage for species facing long-term environmental fluctuations as previously suggested for intertidal gastropods (Chapperon and Seuront 2011). Such evolutionary adaptation to increase survival in a changing environment can, in turn, also affect individual contribution to ecosystem processes (Maltagliati et al. 2006;Bolnick et al. 2011). Noticeably, the species characterized by the highest inter-individual variability (i.e. Q. seminulum, C. williamsoni and H. germanica) are also the species that contribute most to SSRR i (see Fig. 6). This last observation is particularly relevant as it may inform on the species-specific phenotypic plasticity and, therefore, the sustainability of the functional role of these species that live in a highly variable environment such as intertidal sedimentary ecosystems.
Taken together our observations may suggest that individual trait variations matter in the SSRR i of the five studied foraminiferal species. This is consistent with previous studies showing that inter-individual variations can have large ecological consequences on ecosystem processes such as primary production, nutrient cycling than interspecific variability (Crutsinger 2006;Lecerf and Chauvet 2008;Bolnick et al. 2011).

Conclusion
Our study revealed that bioturbation by benthic foraminifera is the result of the complex interplay between species-specific features such as motion behaviour, phenotypic plasticity and functional classification, i.e. bioturbation mode. Note that the individuals smaller than 125 µm were not considered in the present study. It would be interesting to consider smaller-sized fractions as their surface sediment reworking rate might be different from those of adult specimen. Indeed, previous experiments have shown that juveniles can contribute more or equally than adults to the functioning of benthic ecosystem (Wukovits et al. 2018). Furthermore, they represent a large part of the foraminiferal community and have high energetical needs for growth (Caralp 1989;Murray 1983;Nomaki et al. 2006;Wukovits et al. 2018). Hence, their displacements would also matter in the reworking of surface sediment particles. Despite their relatively small size, these five benthic foraminiferal species showed nonnegligible sediment mixing rates at the sediment water interface through their active displacements. Additional studies are nevertheless needed to further estimate the role of intertidal foraminifera to bioturbation processes because the species-specific traits that control their activity in and on the sediment may depend on both allogenic (e.g. temperature, food availability) and autogenic (e.g. size, age) factors.