Journal of Sea Research 78 (2013) 1–7

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Journal of Sea Research

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Feeding habits of amphipods (Crustacea: ) from shallow soft bottom communities: Comparison between marine caves and open habitats

Carlos Navarro-Barranco a,c,⁎, José Manuel Tierno-de-Figueroa b,c, José Manuel Guerra-García a,c, Luis Sánchez-Tocino b, José Carlos García-Gómez a a Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain b Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Campus Fuentenueva s/n, 18071 Granada, Spain c Jun Zoological Research Center, C/Los Jazmines n° 15, 18213 Jun, Granada, Spain article info abstract

Article history: Marine caves are environments of great interest since the organisms that inhabit them are forced to develop Received 20 August 2012 specific adaptations to high constraint conditions. Because of some of these particular conditions, such as Received in revised form 22 December 2012 light absence or oligotrophy, it can be expected that feeding strategies into caves differ from that present out- Accepted 30 December 2012 side them. Nevertheless, no studies have been done to compare the trophic structure of marine caves and Available online 17 January 2013 open habitats, at least for amphipod communities, considering their importance both inside and outside of

Keywords: the caves. In this study, the diet of the dominant amphipod living on shallow sediments, both inside Feeding Habits and outside of six marine caves in western Mediterranean, was characterized. Thereby, the gut content of 17 Marine Caves amphipod species was studied, being this study the first attempt to establish the feeding habit of most of Soft-bottom these species. Analysis of digestive contents of the species showed that amphipod diet is less diverse in sed- Amphipods iments than in other environments, such as algae and seagrasses. No herbivorous species were found in the Gut Contents sediment and carnivorous amphipods showed a little variety of prey, feeding mainly on . Differ- Trophic Dynamics ences in the trophic structure were also found between marine caves and open habitats sediments: while outside the caves detritivorous was the dominant group (both in number of species and number of individ- uals), amphipods mainly play the role of carnivorous inside the caves. No detritivorous species were found into the caves, where carnivorous represents almost 60% of amphipods species and more than 80% of amphi- pod individuals. This pattern obtained in amphipods differ from the general trend observed in marine cave organisms, for which a generalist diet, such as omnivory, usually is an advantage in these oligotrophic condi- tions. The possible causes of this pattern are discussed. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved.

1. Introduction freshwater and terrestrial caves) avoids the presence of primary pro- ducers (except in some cases chemosynthetic bacteria) (e.g. Airoldi and Submarine caves constitute interesting ecosystems characterized Cinelli, 1996; Pohlman et al., 1997). Parravicini et al. (2010) pointed out by distinctive biological and ecological peculiarities (Gili et al., 1986). that, because of the differences in water confinement and trophic deple- Despite the increased interest of the last decades in the study of these tion among different sectors inside marine caves, consistent variations habitats (Benedetti-Cechi et al., 1996), many aspects remain almost in the trophic guild of sessile species can be found. Additionally for soft unknown. Marine caves can be inhabited by specialized taxa, many of bottom communities, the existence of a lower hydrodynamism influences them restricted to live in caves (sometimes exhibiting extreme adapta- their habitat structure, usually offering a finer sediment substrate than the tions), or by more generalist taxa than can find temporal or permanent surrounding seabed (Bamber et al., 2008). Iliffe and Bishop (2007) note, at refuge there (e.g. Bussotti and Guidetti, 2009; Harmelin et al., 1985; community levels, that the scarcity of food in anchialine caves drives Vacelet et al., 1994). In any case, from the feeding point of view, caves organisms toward a generalist diet, being expected that detritus feeders, are usually poor environments that greatly condition their trophic together with omnivorous, dominate in these environments. Neverthe- webs, at a global scale, and the particular diet of the species present, at a less, the role of a particular taxon needs to be evaluated to really catego- low scale. Thus, the absence of light in marine caves (common fact to rize it inside the trophic web. In fact, it is amazing how little is known about the ecology of caves in general, particularly when it comes to their trophic structure (Romero, 2009). ⁎ Corresponding author at: Laboratorio de Biología Marina, Departamento de Zoología, In soft-bottom marine substrates, amphipod crustaceans are one of Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain. Tel.: +34 954556229. the most important and diverse components of the fauna (Dauvin et al., E-mail address: [email protected] (C. Navarro-Barranco). 1994; Fincham, 1974; Lourido et al., 2008; Prato and Biandolino, 2005)

1385-1101/$ – see front matter. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.seares.2012.12.011 2 C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7 structuring benthic assemblages (Duffy and Hay, 2000). Amphipods are Table 1 frequent both inside and outside caves (Bamber et al., 2008; Iliffe, 2005; Cave localities where amphipods were collected. Amb: Ampelisca brevicornis (Costa, 1853); Bag: Bathyporeia guilliamsoniana (Bate, 1857); Gaf: Gammarella fucicola (Leach, 1814); Navarro-Barranco et al., 2012). In relation with all the previously noted, Haa: Harpinia antennaria Meinert, 1890; Hac: Harpinia crenulata (Boeck, 1871); Hap: the study of the feeding habits of amphipods can constitute an interesting Harpinia pectinata Sars, 1891; Him: Hippomedon massiliensis Bellan-Santini, 1965; Leh: tool to understand the trophic webs in the benthos of marine caves and Leptocheirus hirsutimanus (Bate, 1862); Mem: Megaluropus monasteriensis Ledoyer, their surroundings. 1976; Mef: Metaphoxus fultoni (Scott, 1890); Mog: Monoculodes griseus Della Valle, Thus, the aim of the present study is to describe the feeding habits 1893; Pat: typicus (Krøyer, 1884); Pel: Perioculodes longimanus (Bate & Westwood, 1868); Phl: Photis longipes (Della Valle, 1893); Phm: Phtisica marina Slabber, of the most abundant species of amphipods inhabiting inside and outside 1769; Sis: Siphonoecetes sabatieri De Rouville, 1894; Ure: elegans (Bate, 1857). of some marine caves in western Mediterranean, to compare the obtained results and to test the hypothesis that species and/or populations living Caves Coordinates Depth Amphipod species (m) inside the caves are more detritivorous or omnivorous than those living Outside Inside outside of the caves. Gorgonias (GR) 36° 44′ 17″ N, 3° 46′ 42″ W 6 Bag, Mem Hap, Pel Cantarriján (CN) 36° 44′ 16″ N, 3° 46′ 41″ W 8 Sis, Ure Hap, Pel 2. Material and methods Treinta Metros 36° 43′ 12″ N, 3° 44′ 9″ W 30 Hac Haa, Hac (TM) Raja de la Mona 36° 43′ 10″ N, 3° 44′ 6″ W 30 Leh, Phl Gaf, Phm Six karstic marine caves were selected for this study (Fig. 1 and (RM) Table 1). All the caves presented similar length (10–25 m) and Punta del Vapor 36° 43′ 22″ N, 3° 42′ 35″ W 12 Amb, Him, Hac morphology, with a single submerged entrance followed by a rectilinear (PV) Mem, Pat, blind-ending tunnel without air chambers. The sampling was conducted Pel, Phl, Sis Calahonda (CL) 36° 42′ 46″ N, 3° 22′ 18″ W19 Hap,Him, Hac, Hap, during July and August of 2011. Two sampling stations were selected in Mem, Mef, Mog each cave: one in the exterior area (outside the cave) and another inside Phl, Pat, the cave (each one approximately 10 m from the cave mouth). Samples Sis, Ure were collected in each station using a hand-held rectangular core of 0.025 m2 to a depth of 10 cm by SCUBA diving. Samples were washed using a 0.5 mm mesh sieve, fixed with ethanol (70%) stained with rose groups and other , both aquatic and terrestrial forms Bengal. Amphipods were sorted under binocular microscope. Additional and both ethanol and formalin preserved samples, revealing that it is a samples were collected at each station for physicochemical analyses of very appropriate method for gut content analysis (e.g. Bo et al., 2012; the sediment. All samples were immediately stored frozen until the lab- Fenoglio et al., 2008; Tierno de Figueroa et al., 2006). Particularly, this oratory analyses. Granulometry was determined following the method method has been used previously in (Alarcón-Ortega et proposed by Guitián and Carballas (1976). Organic matter was analyzed al., 2012; Guerra-García and Tierno de Figueroa, 2009; Vázquez-Luis by dichromate oxidation and titration with ferrous ammonium sulfate et al., 2012). Each individual was introduced in a vial with Hertwig's (Walkley and Black, 1934). liquid (consisting of 270 g of chloral hydrate, 19 ml of chloridric acid To characterize the feeding habits of the amphipod community, 1 N, 150 ml of distillated water and 60 ml of glycerin) and heated in we selected the species which contributed with at least 1% to the an oven at 65 °C for approximately 3 h. After this, they were mounted total abundance. In total, we studied 137 specimens of 7 species of on slides for its study under the microscope. The percentage of the ab- amphipods living inside caves and 351 specimens of 13 species living solute gut content (at 100×), as the total area occupied by the content outside caves. The whole list of analyzed material and details of prove- in the whole digestive tract, and the relative gut content (at 400×), as nance is included in Table 1, and the mean abundance of the amphipod the area occupied for each component within the total gut content, species inside and outside the caves is included in Fig. 2. were estimated using the microscope equipped with an ocular microme- For the diet study, individuals were analyzed following the method- ter. Mean and standard error of the mean were calculated. Amphipod spe- ology proposed by Bello and Cabrera (1999) with slight variations. This cies were assigned to their feeding group (detritivorous, carnivorous, and method has been successfully used to study the gut contents of different omnivorous) according to the diet. When the gut content included more

N

Salobreña Motril La Herradura Almuñecar Castell de Ferro GR PV CN TM RM 5 km CL MEDITERRANEAN SEA

Fig. 1. Map of the study showing the location of marine caves where amphipods were collected. GR: Gorgonians, CN: Cantarriján, TM: Treinta Metros, RM: Raja Mona, PV: Punta Vapor, CL: Calahonda. C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7 3

Siphonoecetes sabatieri Metaphoxus fultoni Photis longipes Leptocheirus hirsutimanus Perioculodes longimanus Hippomedon massiliensis Harpinia pectinata Harpinia crenulata Bathyporeia guilliamsoniana Megaluropus monasteriensis Ampelisca brevicornis A

0 100 200 300 400 500 600 700 800 900 5000 6000 7000 8000

Harpinia pectinata

Harpinia crenulata

Perioculodes longimanus

Harpinia antennaria

Gammarella fucicola

Monoculodes griseus

Phtisica marina B

0 100 200 300 400 500 600 700 800 900 100 1000 1500 2000 Abundance (individuals/m2)

Fig. 2. Abundance (ind/m2) of the dominant amphipod species (>1%) both outside (A) and inside (B) of the studied caves.

than 50% of prey, we cataloged the species as a carnivorous, considering caves (67.8%) and 82 of the 137 specimens inside the caves (59.9%) that other materials can appear as the prey gut content or accidentally (Table 2). The average of the total area occupied by the content in ingested when preying. the whole digestive tract ranged from 11.1 to 73.3% outside the The affinities among species according to the dietary analysis were caves and from 9.4 to 58.2% inside the caves. Gut contents of the explored by cluster analysis using UPGMA (unweighted pair group studied amphipod species included mainly detritus and crustaceans, method using arithmetic averages) and Bray Curtis similarity index. and secondly microalgae and polychaetes. According to the diet, species This multivariate analysis was carried out using the PRIMER package were included in three different feeding groups: detritivorous (6 species), (Clarke and Gorley, 2001). For the three species inhabiting both inside carnivorous (5 species) and omnivorous (6 species) (Table 2). This classi- and outside of the caves (Harpinia crenulata, Harpinia pectinata and fication was supported when the cluster analysis was conducted (Fig. 3). Perioculodes longimanus), we used an analysis of variance (ANOVA) with Carnivorous and detritivorous constituted well defined groups, while the following factors: ‘Position’,afixed factor with two levels: outside omnivorous species were in an intermediate position, with most of and inside the caves; ‘Species’ a fixed factor and orthogonal, with three species closer to detritivorous, and one species, Hippomedon massiliensis, levels (the three species). The number of specimens with detected diges- closer to carnivorous. tive contents was different among species. Consequently, to properly con- We found species belonging to the three feeding groups outside the ductabalancedANOVAdesign,wechosethespecieswiththelowest caves, while inside the caves the detritivorous were absent. Carnivorous values (n=8 for P. longimanus) and we selected randomly 8 specimens dominated the caves, both in number of species and abundances, while of the remaining species. Additional ANOVA was used to test whether detritivorous were dominant outside the caves (Fig. 4). The three stud- the organic matter and silt and clay percentage in the sediment changes ied species which were found inside and outside the caves, H. crenulata, between positions. Prior to ANOVA, heterogeneity of variance was tested H. pectinata,andP. longimanus, were carnivorous. There were no signif- with Cochran's C-test. Univariate analyses were conducted with GMAV5 icant differences in digestive contents (measured as percentage of (Underwood et al., 2002). detritus) among the three species. Furthermore, each species showed the same feeding pattern inside and outside the caves (Table 3, Fig. 5). 3. Results In connection with physicochemical parameters, organic matter was higher inside the caves, although values were always low (b1%) both In total, we studied 488 specimens of 17 species of amphipods. inside and outside the caves (Fig. 6). The studied caves showed a dom- Digestive contents were found in 238 of the 351 specimens outside the inance of very fine and fine sands and this pattern was obtained inside 4 C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7

Table 2 Gut contents of the studied amphipod species inside and outside of the caves. N: number of specimens of each species examined; n: number of specimens with detected gut content. %abs: total area occupied by the content in the whole digestive tract. Values: mean values±standard errors of the mean and, in parenthesis, minimum–maximum. FG (feeding group): D: detritivorous; O: omnivorous; C: carnivorous.

N/n % abs Components (100%) FG

%detritus %microalgae %crustacea %polychaeta

Outside Ampelisca brevicornis 12/12 60.8±8.5 (10–90) 92.5±4.5 (50–100) – 4.2±4.2 (0–50) 3.3±2.3 (0–20) O Bathyporeia gilliamsoniana 14/13 46.5±8.7 (5–90) 100±0 (0–100) –– –D Harpinia crenulata 12/9 11.1±2.9 (5–30) 41.1±7.7 (0–70) – 58.9±7.7 (30–100) – C Harpinia pectinata 17/14 28.6±5.5 (5–70) 35.4±7.6 (0–100) 0.5±0.4 (0–5) 60.6±8.8 (0–100) 3.6±3.6 (0–50) C Hippomedon massiliensis 30/17 69.4±6.0 (20–100) 58.2±9.9 (0–100) 0.3±0.3 (0–5) 41.5±9.9 (0–100) – O Leptocheirus hirsutimanus 25/17 43.5±8.3 (5–100) 100±0 (100–100) –– –D Megaluropus monasteriensis 6/6 73.3±11.1 (20–90) 100±0 (100–100) –– –D Metaphoxus fultoni 49/5 28.0±3.7 (20–40) 14.0±7.5 (0–40) – 86.0±7.5 (60–100) – C Pariambus typicus 24/18 44.4±7.1 (5–100) 100±0 (100–100) –– –D Perioculodes longimanus 25/16 16.9±3.1 (5–50) 29.4±7.3 (0–80) – 70.6±7.3 (20–100) – C Photis longipes 41/30 29.2±5.2 (5–100) 100±0 (100–100) –– –D Siphonoecetes sabatieri 70/60 41.7±4.0 (5–100) 100±0 (100–100) –– –D Urothoe elegans 26/21 21.0±2.5 (10–50) 73.3±5.4 (0–10) 1.4±1.0 (0–20) 25.2±5.6 (0–100) – O

Inside Gammarella fucicola 8/7 40.0±10.5 (10–80) 85.7±7.2 (60–100) – 14.3±7.2 (0–40) – O Harpinia antennaria 8/6 14.2±2.7 (5–20) 80.0±16.3 (0–100) – 20.0±16.3 (0–100) – O Harpinia crenulata 20/12 15.4±3.2 (5–40) 42.5±9.1 (0–90) – 57.5±9.1 (10–100) – C Harpinia pectinata 66/34 13.8±1.5 (5–40) 39.1±5.6 (0–100) – 60.1±5.6 (0–100) – C Monoculodes griseus 7/4 12.5±2.5 (10–20) 32.5±11.8 (0–50) – 67.5±11.8 (50–100) – C Perioculodes longimanus 17/8 9.4±1.8 (5–20) 26.3±9.6 (0–70) – 73.8±9.6 (30–100) – C Phtisica marina 11/11 58.2±8.2 (20–90) 91.8±7.2 (20–100) 0.5±0.5 (0–5) 7.7±7.3 (0–80) – O and outside. However, the percentage of silt and clay was significantly there are not always clear relationships among these characters and the higher inside the caves (Fig. 6). digestive contents. Only the diet of 2 of the 17 species considered had previously been 4. Discussion studied based in the gut contents. The data obtained in the present study for these two species, Pariambus typicus and Phtisica marina, The present work is the first comprehensive study on the feeding agree with those obtained by Guerra-García and Tierno de Figueroa habits of amphipod species inhabiting soft bottom communities. There (2009). On the other hand, the knowledge about feeding habits in are very few studies dealing with the diet of amphipod species and this amphipods is limited, in some cases, to family level. In this sense, our re- biological aspect is unknown for many of them (Scipione, 1989). More- sults usually agree with the previous literature. According to our data, over, the knowledge about the feeding of many species was based on as- Siphonocetes sabatieri is a strictly detritivorous species, which agree sumptions from fecal pellet composition or morphological characters, but with the previously recorded for the Corophidae family (Bellan-Santini these assumptions must be taken carefully since they are not always ful- and Ruffo, 1998). Studying the crop contents of some phoxocephalid filled. For example, the feeding habit of caprellids has been traditionally species, Oliver et al. (1982) concluded that this group acts as a key inferred from mouthparts or antennae morphology (Caine 1974, 1977); taxon in soft bottom communities, playing an important functional role however, Guerra-García and Tierno de Figueroa (2009) showed that as carnivorous. Other studies using stable isotope analyses also showed

Harpinia crenulata IN Harpinia crenulata OUT Harpinia pectinata IN Harpinia pectinata OUT Perioculodes longimanus OUT Monoculodes griseus IN

Perioculodes longimanus IN CARNIVOROUS Metaphoxus fultoni OUT Hippomedon massiliensis OUT Harpinia antennaria IN Gammarella fucicola IN Urothoe elegans OUT Phtisica marina IN

Ampelisca brevicornis OUT OMNIVOROUS Pariambus typicus OUT Megaluropus monasteriensis OUT Leptocheirus hirsutimanus OUT Bathyporeia guilliamsoniana OUT Siphonoecetes sabatieri OUT Photis longipes OUT DETRITIVOROUS

40 60 80 100 Bray Curtis Similarity (%)

Fig. 3. Dendrogram based on the digestive contents of the studied amphipod species inside and outside the caves. C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7 5

100% OUT INOUT IN OUT IN 100%

80% 80%

60% 60%

40% 40%

20% 20%

0% 0% Outside Inside Outside Inside Harpinia Harpinia Perioculodes NUMBER OF SPECIES ABUNDANCE crenulata pectinata longimanus

Omnivorous Carnivorous Detritivorous Microalgae Prey Detritus

Fig. 4. Contribution in percentage of each feeding group to the total number of species Fig. 5. Contribution of each feeding component for the three species inhabiting both in- and abundance. side and outside of the caves. See also Table 3. the carnivorous behavior of Harpinia species (Fanelli et al., 2009). Our P. longimanus (all of them carnivorous) between habitats could be data support this assertion, since almost all the phoxocephalid species due to the availability of this food source inside and outside the caves. studied (H. pectinata, H. crenulata and Metaphoxus fultoni)hadadiet Strong differences between habitats can also been found when all mainly composed by crustaceans. Nevertheless, in some cases, species amphipod assemblages are considered. Our data reflects that amphi- belonging to the same family or even showed different feeding pod diet in sediments is less diverse than in other environments such habits. For example, Harpinia antennaria had an omnivorous diet in as algae and seagrasses (Guerra-García and Tierno de Figueroa, 2009; the present study. Urothoe elegans was omnivorous while Bathyporeia Vázquez-Luis et al., 2012). The percentage of algae in the gut contents guilliamsoniana (both of them belonging to Haustoridae family) fed was zero or very low in all cases. Obviously, that pattern was expected in- exclusively on detritus. These results show that the feeding habits of side the caves, where no primary producer is present, but it is remarkable an unstudied species cannot be inferred from studies of congeners, as it that no herbivorous species could be found in the external sediments. The has been noted for other aquatic invertebrates (e. g. Stewart and Stark, variety of prey in carnivorous species was also lower, composed mainly 2002), and consequently gut content analyses are needed to correctly (and often exclusively) by crustaceans. assign each taxon to each feeding group. Diet diversity in soft bottom amphipod assemblage was even less Within the same species, variations in the trophic preferences can diverse inside the caves. No detritivorous species was present inside also be found when studying different environments. In a comparative the caves and, while this feeding group was the dominant group work carried out in the Mediterranean to study the variations in the (both number of species and number of individuals) in the external gut contents of some amphipod species living in native and invasive sediments, cave community was dominated by carnivorous species. seaweeds, Vázquez-Luis et al. (2012) found that some species (such This pattern in amphipod species is highly unexpected since the general as Ampithoe ramondi or Dexamine spiniventris) had different feeding pattern in cave communities drives organisms toward a generalist diet modes depending on the habitat they live on. In the same way, (with a dominance of omnivorous and detritivorous species). However, Alarcón-Ortega et al. (2012) reported variations in the feeding behav- as in such case, some particular groups can follow a different trend. ior of the caprellids Aciconula acanthosoma and Caprella equilibra when Bianchi (1985) found a high percentage of carnivorous species in poly- they live in algae, hydroids or gorgonians. In our study, the three species chaete assemblages of marine cave. According to Romero (2009),cave found both inside and outside the caves did not show significant amphipods feed mostly on detritus but our data show that they occupy changes in their gut components between both habitats. The absence mainly the role of carnivorous. The reason of the absence of detritivorous of differences in the feeding modes for H. crenulata, H. pectinata,and amphipods into these caves remains still uncertain. A potential factor could be the limited food supply, since marine caves are usually consid- Table 3 ered as oligotrophic habitats. Experimental studies on vegetated habitats Results of the two-factor ANOVA for percentage of detritus in the amphipod species reveal that species richness and abundance of amphipods were highly inhabiting outside and inside of the caves: Harpinia crenulata, H. pectinata and Perioculodes and positively related with the detritus content (Vázquez-Luis et al., longimanus. MS=mean square; df=degrees of freedom. 2009). However, our chemical data showed significant higher concentra- Source of variation %detritus tions of organic matter inside the caves, although it has been suggested df MS FPthat the quality of organic matter in marine caves may decrease toward the inner parts (Fichez, 1991). The feeding behavior, not only the feeding Position (Po) 1 75.00 0.08 0.78 Species (Sp) 2 506.25 0.55 0.58 group, should be also an important factor to consider. Because of the low Po×Sp 2 1406.25 1.53 0.23 hidrodinamism inside caves, strong differences between habitats can be Residual 42 921.43 expected in the way in which such organic matter is available to organ- Cochran's C-test C=0.22 isms. Thereby, while inside the caves the organic matter percentage in Transformation None the sediment is higher, the suspended detritus is much less abundant. 6 C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7

ORGANIC MATTER colonize such habitats, among others, which can act like a limiting factor 1,5 for the presence of detritivorous. Further studies about the ecological conditions in marine caves and the feeding habit and behavior of all the soft-bottom community are necessary to understand the trophic dynamic of such environments.

Acknowledgments 1 Financial support of this work was provided by the Ministerio de Educación y Ciencia (Project CGL 2011-22474/BOS). This work forms part of C.N-B's Ph.D. Thesis, supported by the Universidad de Sevilla % (PIF Grant).

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