Deep–Sea Research I 196 (2023) 104020 Contents lists available at ScienceDirect Deep-Sea Research Part I journal homepage: www.elsevier.com/locate/dsri Description of a first-settled stage of Aristeus antennatus (Risso, 1816) and new insights into distribution and life history of early juveniles in the NW Mediterranean sea Sara Dallarés a, *, Aina Carbonell b, Joan E. Cartes c a Departament de Biologia Animal, Biologia Vegetal i Ecologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, 08193, Barcelona, Spain b Instituto Español de Ocenografía (IEO-CSIC), Centro Oceanográfico de Baleares, Muelle de Poniente s/n, 07015, Palma de Mallorca, Spain c Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain A R T I C L E I N F O A B S T R A C T Keywords: Knowledge on settlement stages of marine fauna is scarce, especially for mobile organisms such as crustaceans. Red shrimp This is most probably explained by the difficulty of capturing them at great depths in addition to their short Decapoda lifespan and preference for special habitats. In the case of the red shrimp Aristeus antennatus (Risso, 18,16), a Deep-sea species of outstanding importance in many Mediterranean fisheries, there is an important lack of knowledge Settlement Morphological description regarding development between pelagic larval to benthic juvenile-adult phases. As a contribution to fill this gap, in the present study a first-settled stage of the red shrimp is described based on a specimen collected off For­ mentera (Algerian Basin, western Mediterranean) during October of 1996 at 1594 m depth with a Macer-GIROQ suprabenthic sledge. As a complement to this description, the seasonal distribution and density of small juveniles of A. antennatus (caparace length <16 mm) captured in the Balearic Basin during OTSB-14 bottom trawls per­ formed between the years 2007–2020 at more than 1000 m depth is mapped and discussed. From these distri­ bution maps, an increase in captures of juveniles from autumn to summer can be appreciated, as well as a phenomenon of migration of these small individuals from inner to outer regions of the Balearic Basin. Finally, a theoretical reconstruction of the early life history of these small juveniles, starting at hatching in July, which consistently fits with the size of the first-settled stage described here, is provided. 1. Introduction for mobile animals such as fish or crustaceans, being difficult to find detailed morphological descriptions of specimens at this stage. This lack Settlement, the time at which a given organism switches from a of information may be related to: i) a short lifespan coupled to a fast swimming planktonic to a benthic lifestyle, is a crucial step in the life development of these phases, and ii) the difficulty to capture them at history of many marine organisms. Indeed, recruitment occurs after great depths in the water-sediment interphase (the Benthic Boundary successful settlement on or immediately above the seafloor (Mullienaux, Layer, BBL), largely derived from the impossibility to perform 1988; Anger, 2001). Some experiments carried out with sessile epifauna specifically-designed surveys for their capture due to the generalized settled on hard substrata proved that settlement patterns depend on the lack of knowledge on their ecology. We could add a third reason related feeding modality of the organism under study and on the supply in­ to a certain preference by these first-settled stages for inaccessible and/ tensity of particulate organic matter (POM) (Mullineaux, 1988). POM or special habitats where they could find refuge, as has been reported for arrival to the seafloor experiences seasonal peaks that condition its fish recruits in coral reefs (Montgomery et al., 2001). Hence the gaps of availability for deep-sea species and can thus determine intra-annual knowledge on these phases, since settlement must be done in a specific changes in its abundance (Durden et al., 2020). Due to their feeding and short period of time and potentially in suitable areas out of reach of habits, predators like fish and shrimps may face additional uncertainty the conventional sampling methods designed for studies on adults and in finding food (i.e. prey) hotspots that foster settlement. larvae. Understandably, most existing studies on settlement of mobile In general, knowledge on settlement life phases is scarce, especially animals, such as fish and crustaceans, have focused on shallow depths (e. * Corresponding author. E-mail address: Sara.Dallares@uab.cat (S. Dallarés). https://doi.org/10.1016/j.dsr.2023.104020 Received 10 August 2022; Received in revised form 22 February 2023; Accepted 2 March 2023 Available online 4 March 2023 0967-0637/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 g. Bastrikin et al., 2014; Faillettaz et al., 2020; Eélix-Hackradt et al., described for this species, as also are depths where first-settlement takes 2013; Vinuesa et al., 2010; Tamaki et al., 2020) while the deep-sea re­ place. It is well known, however, that the ca. 1st year-old specimens (the mains almost unexplored for these kind of studies. This lack of infor­ smallest juveniles known, with a caparace length of 6–7 mm) have only mation on basic features of early stages is generalized in the marine been collected from very deep areas, at > 1000 m depth (Sardà and environment and extends far beyond free-living organisms to, for Cartes 1997; Cartes et al., 2017). The main difficulty for gaining an example, many parasites with indirect development and more or less adequate knowledge of early stages of this species lies in the fact that, complex life cycles that belong to a diversity of taxonomic groups contrary to adults and large juveniles, and as explained above, captures (Rohde, 2005). of larval stages and small juveniles are extremely rare. The high simi­ The red shrimp Aristeus antennatus (Risso, 1816) is an important larity of the larval series of A. antennatus to that of other shrimps, such as target species for fisheries of the Mediterranean Sea, where it is captured Aristaeomorpha foliacea or Gennadas elegans (Carreton et al., 2019) is an by bottom trawlers at the upper and middle slopes down to ca. 800 m added difficulty. Furthermore, and contrary to other shrimps (e.g. Per­ depth. In the Mediterranean Spanish coast, this crustacean is among the iclimenes aegylos, see Di Muzio et al., 2018), larval rearing in laboratory ten most important species captured in terms of biomass, and is the first conditions, which allows the observation and description of the com­ in terms of economic value (DGPAM, 2022). Furthermore, this species plete life cycle of the species under study, is not possible in the case of also bears a high ecological importance in benthic deep-sea ecosystems, A. antennatus and other Dendrobranchiata since eggs are released to the being a dominant species in the crustacean community of the lower water column instead of being carried by females. slope in the north-western Mediterranean area (Abelló et al., 1988; The present study describes, for the first time, a first-settled stage of Cartes et al., 1994a). The species distribution extends to 2300 m depth the red shrimp. Due to its rarity, this stage has not been previously re­ and recruitment (and thus probably settlement) occurs beyond the ported and the present description is based on a single specimen. depths where it is usually exploited (Sardà and Cartes, 1997; Cartes Furthermore, spatial and temporal distribution of small specimens of et al., 2017). Therefore, there is an important part of its population, A. antennatus (caparace length <16 mm) collected in deep waters of the represented by 1st year cohort, living at depths free of fisheries impact. Balearic Basin from 2007 to 2020 and their theoretical growth, starting An adequate and sustainable management of commercially exploited from the theoretical hatching time and setting settlement at the size of natural stocks requires a deep knowledge and understanding of the the described individual, are explored. Therefore, this is an important development, spatial and temporal distribution and basic biology and contribution to the body of knowledge of this species, shedding light into ecology of target species. While this is obvious for juveniles and adults, it the development and ecology of its early stages. is equally valid for the small larval stages. Indeed, crustacean larvae, as those of many other animal groups, play an essential role in recruitment, 2. Materials and methods population trends at different scales, populations connectivity and biogeography, among many others (Anger, 2001). This is the reason why 2.1. Data sampling and specimen collection stock management and conservation efforts for decapod crustaceans with commercial interest would benefit of a better knowledge of the A considerable number of research campaigns have been conducted dispersion patterns, settlement and ecology of their larval and juvenile off the continental margin of the Balearic basin since 1985. During these stages. surveys, a semi-balloon otter trawl (OTSB-14; Merrett and Marshall, In the specific case of the red shrimp, there are still tremendous gaps 1981) was used for capturing benthopelagic megafauna and a of knowledge regarding life phases that are switching from a pelagic to a Macer-GIROQ suprabenthic sledge to collect suprabenthic macrofauna demersal lifestyle (larvae vs. juveniles, respectively). These stages are at the sediment-water interphase (0–1 m above the seafloor) (see sometimes defined as “post larvae” or “first-settlement stages”. While detailed information below). Overall, surveys performed with both some aspects of the biology and ecology of this species being well-known sampling gears covered all seasons and all slope depth ranges between (Carbonell et al., 2006; 2008; Cartes, 1994; Cartes et al., 2017), a special the shelf-slope break at ca. 200 m to the maximum depths of the Balearic interest exists in completing the lack of information regarding its life Basin (i.e. 2300 m). Details for OTSB-14 samplings can be found in cycle and basic biology, justified by the species’ enormous commercial Cartes et al. (2017) and as supplementary material in Table S1 of the and ecological significance. This would allow a better evaluation of the present study, while the Macer-GIROQ suprabenthic hauls were mapped state of its commercial populations, which face great pressure from the in Cartes and Figueroa (2020, Fig. 1). Immediately after collection, all fishing industry, better fishery management and a more adequate pro­ samples were preserved in ~4% borax-buffered formaldehyde. Once in tection of the species. the laboratory, samples were sorted and decapod crustacean larvae were The larval development of A. antennatus starts with the nauplius classified according to species and developmental stage, when possible, larval type, common to most crustaceans. In the case of the Dendro­ using identification keys (dos Santos and Lindley, 2001; dos Santos and branchiata, it is a nonfeeding free-living pelagic phase that undergoes González-Gordillo, 2004) and species descriptions monographs (Heldt, from five to eight moults before the next stage (Anger, 2001). The next 1955; Torres et al., 2013 for A. antennatus). stage is the zoea, which comprises a variable number of the so called During Macer-GIROQ suprabenthic hauls only two juvenile speci­ protozoea (early zoea) and mysis (late zoea) stages. Heldt (1955) mens of A. antennatus (the two smallest juveniles collected to date in the described the development of A. antennatus from the second protozoea to Balearic Basin) were collected, one of them being the first-settled stage the first mysis stage based on alive specimens collected in surface waters described herein. This specimen was collected south off Formentera from the Balearic Sea. More recently, a complete description of the (Balearic Islands, NW Mediterranean) during the QUIMERA1 cruise second mysis stage was provided by Torres et al. (2013) based on a single (October of 1996 at 1594 m depth, coordinates: 38◦ 12.63′ N ‒ 1◦ 47.74′ specimen found in plankton samples obtained at ca. 1000 m depth off E). The second specimen was collected off Barcelona during the ReTro2 the Balearic Islands (NW Mediterranean). Beyond this mysis stage, more survey (December of 1991 at 1258 m depth). Model characteristics for advanced phases of development for the family Aristeidae are unknown. this sampling gear can be found in Cartes et al. (1994b). Briefly, this The last larval type preceding the first juvenile instar is the decapodid, sledge is armed with 0.5 mm mesh size nets attached to three rectan­ which acquires juvenile characteristics gradually through a variable gular mouths of 40 × 80 cm arranged one above the other and equipped number of moults (Anger, 2001) before its bottom settlement. with an opening-close mechanism. Hence, thanks to a system of spring A. antennatus larvae have been recently documented and characterized and levers the mouths openings of the gear are open only when the molecularly off the Catalan coast (Carreton et al., 2019), confirming the sledge is in contact with the seafloor, while when the sledge leaves the adequacy of Heldt (1955) description for larval stages of this species. bottom they are closed. This diminishes the probability of sample As mentioned, the decapodid and early juvenile stages are yet to be contamination in midwater, especially with quick swimming organisms 2 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 Fig. 1. First-settled stage of Aristeus antennatus (CL < 4.7 mm). A, whole specimen in lateral view. B, rostrum. C, antennule. D, antenna. E, maxillule. F, maxilla. such as shrimp larvae. It was during a recent revision of these samples 2.2. Morphological description of the first-settled stage of A. antennatus for the analyses of isopod communities, in 2020, when the A. antennatus specimen described herein was rediscovered and identified. For the morphological description of the first-settled stage of In order to complement the unique capture of this small specimen, A. antennatus, appendices of the single specimen available for exami­ the present study also includes the mapping by season of the distribution nation were carefully dissected and examined as temporary mounts in and abundance of 180 juvenile specimens (caparace length (CL, distilled water. Drawings were made with the aid of a camera lucida measured as the distance between the posterior margin of eye orbit to attached to an Olympus BH light microscope with Nomarski interference the posterior margin of pereion) < 16 mm) of A. antennatus captured in contrast. Measurements were obtained with a stage micrometer. The the Balearic Basin during several hauls performed between the years following measurements were taken: total length (TL, measured as the 2007 and 2020 (Table S1). Briefly, a total of 80 hauls (16 between distance between the anterior tip of the rostrum to the posterior margin October and December, 31 between March and May, and 34 between of pleon) and CL (defined above). Nomenclature used for integumental June and July) were performed at depths comprised between 423 and elements follows Garm and Watling (2013). The specimen is deposited 2233 m in the context of different research projects. All these hauls were at the Institut de Ciències del Mar (ICM-CSIC) biological collection (Col. carried out using a OSTB-14 bottom trawl with an average horizontal leccions Biològiques Marines de Referència, Ref.: ICMD002714). width of 7 m, a vertical opening of 1.2 m and a codend of 6 mm mesh size, being captures of juvenile A. antennatus thus comparable across sampled seasons and depths. After capture, specimens were counted, 2.3. Data analysis measured (CL) and weighed to the nearest 0.01 g. The abundance and density (nº individuals/ha) of small specimens of A. antennatus (CL < 16 mm) collected during OTSB-14 samplings in the Balearic Basin between the years 2007 and 2020 was calculated and mapped seasonally according to haul locations using the mapping 3 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 software SURFER. The locality of the second small juvenile specimen (Fig. 1B); eyes well developed. Antennal and pterygostomian spines captured during Macer-GIROQ suprabenthic hauls, apart from the observed (Fig. 1A); no carinae appreciated. specimen described herein, was also mapped. Antennule (Fig. 1A, C): first segment bearing numerous plumosese­ Using the same individuals, a theoretical life history for juveniles of tae along ventral, dorsal and anterior margins, small ventral spine on A. antennatus was reconstructed, starting from the base of theoretical anterior margin; stylocerite sharp, length about two thirds of first hatching and setting settlement at a size of 4.74 mm CL, using as segment, with a row of sparse plumose setae on ventral margin; second reference the individual described herein. segment length about one half of first one in length, bearing a row of ca. 20 and plumose setae on ventral margin and some sparse plumose setae 3. Results on dorsal side; third segment naked and short, length about one third of second one. Outer flagellum segmented, bearing a few short simple setae 3.1. Morphological description of the first settled-stage of A. antennatus and ca. 30 aesthetascs (between two and four per segment except in the first and last segments that don’t have these structures). Aesthetascs Description (Figs. 1–4). single or in pairs, originating in joints between segments or at mid-level [Based on a single specimen fixed in buffered formaldehyde and of segments, ranging from ca. 100–800 μm in length, irregularly further preserved in ethanol]. distributed regarding size, although longest ones located in the middle Size: 17.59 mm TL and 4.74 mm CL. or distal region of the outer flagellum. Inner flagellum with four plumose Rostrum (Fig. 1A and B) short, pointing anteriorly, about one fourth setae on its base, full length not observed. of CL, with two dorsal spines projected anteriorly and located in the first Antenna (Fig. 1D): protopod naked; scaphocerite width:length ratio two thirds of its length and a group of ventral pappose setae on the 1:3.9, bearing approximately 75 plumose setae along inner and distal middle region. Orbit bearing a few simple setae at the level of eyes margins and a small spine on distal outer margin. Flagellum apparently Fig. 2. First-settled stage of Aristeus antennatus (CL < 4.7 mm). A, mandible. B, mandible palp. C, first maxilliped. D, second maxilliped. E, third maxilliped. F, telson and uropods. G, telson tip. 4 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 Fig. 3. First-settled stage of Aristeus antennatus (CL < 4.7 mm). A, second pleopod. B, third pleopod. C, fourth pleopod. D, fifth pleopod. bearing ca. 30 plumose and composite setae along margins and with ca. 30 composite setae on inner and outer surfaces; second segment length about two thirds of second one; with ca. 22 composite setae along margins and ca. 30 composite setae on inner and outer surfaces. Maxillule (Fig. 1E): coxal endite oval-shaped, with a proximal pro­ tuberance, bearing ca. 22 simple setae along lateral margins and eight faceted cuspidate setae along distal margin. Basial endite broadening towards distal part, with ca. 17 simple setae on inner surface and several (more than 20) cuspidae setae (either with or without small setules on distal region) along distal margin. Endopod unsegmented, bearing a few simple, pappose or plumose setae. Maxilla (Fig. 1F): coxal and basial endites bilobed and elongated, bearing a row of composite setae along distal margins (ca. 25 and 35 setae on coxal and basial endites, respectively) and some sparse com­ posite setae on inner surface; proximal lobe of coxal endite with a few simple setae on posterior margin; distal lobe of basial endite with a few composite setae along anterior margin. Endopod unsegmented, with a few composite and pappose setae along its inner and outer margins, respectively, and five stout, curved and naked cuspidate setae on its distal margin. Scaphognathite bearing ca. 120 plumose setae along its margin. First maxilliped (Fig. 2C): protopod irregular, with two compact protuberances bearing ca. 20 plumose setae on outer margin and several plumose and pappose setae on inner and outer surfaces, and an enlarged and flattened oval-shaped extension with ca. 73 composite setae along outer margin and several composite setae scattered on inner and outer surfaces. Endopod unsegmented, with ca. 30 plumose setae increasing in density towards distal region, bearing a row of five simple setae followed by two cuspidate curved setae on inner margin of proximal region. Exopod unsegmented, approximately equal in length as endopod, slightly curved and flattened, bearing a row of ca. 35 plumose setae Fig. 4. Image of the first-settled stage of Aristeus antennatus (CL < 4.7 mm) along its outer margin, four plumose setae along its inner margin and described herein (A) before its dissection. Colour can be compared to that of two terminal plumose setae. small juveniles (CL ≥ 6.4 mm) and adults collected in recent cruises (B). Second maxilliped (Fig. 2D): basis with ca. 11 pappose-composite setae along inner margin and a few composite setae on inner surface naked, full length not observed. and on outer margin. Endopod flattened, with five segments; first Mandibles (Fig. 2A): symmetrical, incisor part of mandible covering segment with ca. 10 pappose-composite setae along inner margin and a all the outer part, with a single, intermediate, rather dull tooth; molar few composite setae on inner surface; second segment with ca. 48 process long, not very protruding, as illustrated. Mandible palp (Fig. 2B) composite setae along inner margin and a row of few composite and two-segmented, with two small naked setae on its basis; first segment simple setae on inner surface; third segment with five and four 5 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 composite setae along inner and on outer distal margins, respectively; of the central spine. fourth segment with eight composite setae along inner margin, ca. 12 The specimen was pale orange-apricot in colour (Fig. 4A), as the first composite setae on inner surface, generally grouped by pairs, and with a fully developed juvenile stages (Fig. 4B) for which CL was >4.7 mm. row of at least nine serrate setae along second half of outer margin; fifth segment with seven composite and simple setae along inner margin, five 3.2. Other observations on the first-settled stage of A. antennatus composite setae on inner surface, generally grouped by pairs, at least 16 described herein serrate setae along outer margin and three large cuspidate setae on its distal region. Exopod unsegmented, slightly shorter than endopod, The content of the stomach, which was almost empty, only consisted bearing ca. 17 and nine plumose setae along outer and inner and mar­ of a few isolated fragments of copepods. gins, respectively, and two terminal plumose setae. Third maxilliped (Fig. 2E): coxa with ca. 20 composite and simple 3.3. Temporal and spatial distribution of small specimens of A. setae along inner and distal margins. Basis with ca. eight composite setae antennatus (CL < 16 mm) on inner distal region. Endopod with six segments; first and second segments with ca. four and 30, respectively, composite setae along inner Some temporal and spatial patterns in the distribution of the smallest margin and a few simple setae along outer margin; third to sixth seg­ (CL < 16 mm) specimens of A. antennatus collected with OTSB-14 in the ments with composite setae mostly along inner (ca, 20, 25, 17 and ten Balearic Basin during cruises performed between 2007 and 2020 were setae, respectively) and outer (ca. three, eight, five and three setae, identified. In first place, the seasonal distribution of the abundance of respectively) margins and a few sparse simple setae; fourth and fifth these specimens evidenced a significant increase in captures and asso­ segments with a patch of small spiniform projections on proximal inner ciated estimated densities from autumn to spring and summer (Fig. 5). region; sixth segment with a row of ca. ten serrate setae on proximal Additionally, a certain migration of these small individuals from the inner region and with four terminal composite setae. Exopod unseg­ inner to the outer regions of the Balearic Basin from autumn to the next mented, reaching to mid-length of third endopodal segment, bearing ca. spring and summer was observed. 16, plumose setae along second half of outer margin and two terminal plumose setae. 3.4. Theoretical growth from hatching of small specimens of A. Pereiopods: not available for examination. antennatus (CL < 16 mm) Pleon (Fig. 1A): unarmed, with similar length than the cephalotorax. First pleopod: not available for examination. Second to fifth pleopods The size and season of capture of the first-settled stage individual (Fig. 3A–D) progressively decreasing in length posteriorly, birramous, described in the present study fits in the plot displaying the theoretical with endopods increasingly developed posteriorly; endopods and exo­ growth trend of the smallest specimens of A. antennatus (Fig. 6), taking pods unsegmented. hatching (which occurs from mid-spring to the end of summer) as origin. Second pleopod (Fig. 3A): about 18% of specimen TL. Protopod with This reconstruction further suggests that within the 1st year of life a few sparse plumose and simple setae. Endopod ca. 8% of exopod A. antennatus specimens would reach an approximate size of 11–12 mm length, bearing two terminal small plumose setae. Exopod with ca. 24 CL. and 25 plumose setae along inner and outer margins, respectively, and two terminal plumose setae. 4. Discussion Third pleopod (Fig. 3B): protopod with a few sparse plumose and simple setae. Endopod ca. 20% of exopod length, bearing ca. four and 4.1. Identity and developmental stage of the first-settled stage described five plumose setae along inner and outer margins, respectively, and two herein terminal plumose setae. Exopod with ca. 21 and 17 plumose setae along inner and outer margins, respectively, two terminal plumose setae and a There are few descriptions of pre-settlement stages for deep-sea row of ca. 15 short composite setae along anterior margin. shrimps, and the knowledge on the developmental cycle for these spe­ Fourth pleopod (Fig. 3C): protopod with some sparse plumose and cies is, hence, still very fractioned. Both the lack of surveys performed simple setae and a row of ca. four plumose setae along the outer margin. during the specific time and in the habitat in which settlement occurs Endopod ca. 41% of exopod length, bearing ca. nine plumose setae along and, likely, an ephemeral existence prevent the study of these stages, inner and outer margins and two terminal plumose setae. Exopod with occurring between larval and adult phases. Captures like the present one ca. 20 and 22 plumose setae along inner and outer margins, respectively, mostly occur by chance. two terminal plumose setae and a row of ca. 13 short composite setae The specimen described herein was categorized as a juvenile stage in along anterior margin. a previous work based on the observation of its rostrum and telson Fifth pleopod (Fig. 3D): protopod with some sparse plumose setae morphology (Carbonell et al., 2020). However, after the dissection la­ and a row of ca. 12 plumose seatae along the outer and inferior margins. bour and thorough examination carried out in the present study, in can Endopod ca. 65% of exopod length, bearing ca. 15 plumose setae along be now more precisely identified as a transition phase between the inner and outer margins and two terminal plumose setae. Exopod with decapodid (the most advanced larva stage preceding metamorphosis to ca. 18 and 20 plumose setae along inner and outer margins, respectively, the first juvenile, formerly known as “post-larvae”) and an early juvenile two terminal plumose setae and a row of ca. 16 short composite and stage of Aristeidae. Actually, a clear distinction between these two simple setae along anterior margin. developmental stages cannot be made since, for the Dendrobranchiata, Uropods (Fig. 2F): protopod naked. Endopod with long plumose the transition between the two mentioned developmental phases is setae along whole margin. Exopod about 1.2 times longer than endopod, gradual (Anger, 2001). Given the absence of descriptions for Aristeidae with long plumose setae along inner and outer margins and a spine on decapodids, the characteristics of some specific anatomical elements distal outer region. such as the rostrum and telson are important diagnostic features to be Telson (Fig. 2F): shorter than uropods, reaching half the length of the taken into account when performing comparisons to early stages of endopods of the uropods, bearing plumose setae along margins of distal other shrimp species. In the case of the specimen described in the present half and a few simple setae along margins of middle region, with six study, the mentioned structures are very different to those shown by cuspidate setae along distal lateral margins, three on either side. Telson decapodids of Penaeidae distributed in deep and shallow waters of the tip (Fig. 2G) bearing two large (ca. 150 μm long) cuspidate setae on same area (e.g. genera Parapenaeus, Penaeus, Solenocera or Sergestes, see either side, one conical central spine and eight cuspidate setae with Calazans, 1993). sharp tips arranged in two groups of four setae, each group on either side The present specimen can be allocated within the superfamily 6 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 Fig. 5. Distribution of juveniles of Aristeus antennatus (CL < 16 mm) captured in the Balearic basin between the years 2007–2020 during OTSB-14 hauls. A buffer area proportional to estimated density is displayed for each sampling point. Largest buffer corresponds to a maximum density of 4.9 individuals/ha. Crosses indicate hauls without captures. ▴: Location of capture of the small juvenile collected in December of 1991 at 1258 m with a Macer-GIROQ suprabenthic sledge. CL: caparace length. barely reaches 700 m in the Mediterranean deep-sea, even considering the smallest juveniles (14 mm CL) collected (Belcari et al., 2003). Regarding the developmental stages of decapods, the decapodid phase is characterized by the existence of functional pleopods and by cephalic and anterior thoracic appendages assuming new functions as mouthparts (Anger, 2001). The presence of functional larval organs, which are also characteristic of decapodids, such as natatory exopods on the pereiopods, were unfortunately not verified in the present specimen due to the absence of these appendages. As already explained above, in the Dendrobranchiata the transition between the decapodid and first juvenile phase is gradual (a true metamorphosis does not occur) since juvenile characteristics are attained progressively over a variable num­ ber of moults (Anger, 2001). However, the general shape of the spec­ imen described here seems to be closer to an early juvenile than to a decapodid stage. A more specific indication of this is that pleopods, for example, were well developed and setose. Furthermore, and in relation to this, the morphology of the pleopodal endopods is of particular in­ Fig. 6. Theoretical reconstruction of the early life history of juvenile Aristeus terest since it provides evidence of this specimen being a transitional antennatus (CL < 16 mm), starting from the base of theoretical hatching and form. Indeed, the increasing development of such structures, which setting settlement at the size (CL of 4.74 mm) of the individual here described. display the same morphology on adult stages (Zariquiey, 1968), Bars represent the smallest sizes found in each of the seasons sampled at depths observed from the second to the fifth pleopod evidences the gradual >1000 m. Curve fitted to bars represents the theoretical growth that these small acquisition of juvenile morphology described for this group (Anger, specimens might follow. 2001). In comparison with the previous developmental stage for which a Penaeidea based on rostrum surpassing the orbital ring and on the description is available (i.e. mysis II, described by Torres et al., 2013), absence of stiliform projections in the middle part of orbital ring. Within the first-settled stage of A. antennatus described herein displays a num­ the Penaeidea, it can be further assigned to the family Aristeidae, dis­ ber of differential features. Most obvious differences consist in larger carding the possibility of belonging to Penaeidae, based, for example, in overall body size, an abdomen as large as or a little larger than the the lack of an inner antennular scale and in the presence of well- cephalothorax, more developed and complex general structures and developed exopods on the maxillipeds. Within the Aristeidae, an appendages and more numerous and diverse integumental structures (i. evident diagnostic feature for A. antennatus is the conspicuous spine e. setae or spines). Other, more specific features that distinguish present in the outer part of the scaphocerite, as observed in the specimen first-settled from mysis II stage are: proportionally shorter rostrum, described in the present work, which is less marked in other members of directed frontally, with two dorsal spines and a group of ventral pappose the family present in the Mediterranean deep-sea such as Aristaeomorpha setae (vs. longer rostrum, upward-pointing, with no dorsal spines or foliacea (Zariquiey, 1968). Both A. antennatus and A. foliacea show ventral setae), presence of antennal spine (vs. absence of such structure), antennal and branchiostegal spines, but only A. foliacea bears a hepatic absence of supraorbital spine (vs. presence of such structure), propor­ spine, which is effectively absent in the specimen described in the pre­ tionally longer stylocerite, mandible with different morphology (see sent work. Moreover, and still regarding morphological features, the Torres et al., 2013), developed pleopods (vs. only existing as small rostrum of A. foliacea bears five basal teeth and three distal teeth, the uniramous buds) and telson uniramous and almost equal in length than latter sparsely distributed, while the rostrum of A. antennatus only dis­ uropods (vs. telson biramous posteriorly and markedly shorter than plays three basal teeth. Over its still-developing rostrum the present uropods). specimen shows two teeth. In addition to the described morphological In comparison with the adult stage, the first-settled stage of aspects, the extreme depths (1700 m) inhabited by the specimen A. antennatus shows, as described above for the mysis II stage, less described herein are in accordance with the known characteristics and complex general structures and appendages and fewer integumental ecology of A. antennatus, whereas A. foliacea bathymetric distribution elements. In particular, some important differences between adult and 7 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 first-settled stages that can be remarked are: rostrum with three dorsal of knowledge about their ecology and the subsequent scarcity and dif­ spines (vs. with two spines), proportionally shorter uropods and telson ficulty of specially designed surveys to capture these stages. Probably, a and proportionally longer scaphocerite. The mentioned differences were preference by these organisms to find refuge in inaccessible or special also observed in early juveniles with respect to the adult stage by Sardà habitats (Montgomery et al., 2001) also contributes to this pattern. For and Cartes (1997), except for the three dorsal spines on the rostrum, instance, small specimens of A. antennatus were sometimes found asso­ already present in early juvenile stages of 6–7 cm TL (Sardà and Cartes, ciated to mature fields of Isidella elongata (Maynou and Cartes, 2012). 1997). Furthermore, in comparison with the smallest juveniles However, these first-year specimens can also be captured out of bamboo described, the abdomen of the first-settled stage is similar in length to coral fields, in flat muddy bottoms without generating-habitat at > the cephalothorax (vs. clearly longer than the cephalothorax). 1000 m. Therefore, and in our opinion, the lack of specifically-designed Despite the described specimen could suffer from a certain decolor­ samplings performed in particular areas and periods is the main obstacle ation by formaldehyde preservation, it still showed a pale orange- to fill the gap of first-settled phases. Remarkably, the two smallest in­ apricot colour, especially in the abdomen and in the anterior part of dividuals collected up to date in the Balearic Basin (including the cephalothorax (Fig. 4A), similar to the colour of the smallest fully- post-larvae described in the present study) were captured with supra­ developed juvenile stages (CL > 6.4–6.7 mm) regularly caught at > benthic sledges equipped with 0.5 mm plankton nets. 1000 m in the Balearic Basin (Fig. 4B). In light of these difficulties, the present description of a first-settled stage of A. antennatus represents an important and valuable contribution 4.2. What does occur beyond the first-settlement stage? to the knowledge on the life cycle of this species. In conjunction with the development and spatio-temporal distribution of first-year specimens, a Assuming a theoretical average time for hatching in July (Carbonell clearer vision on the life history of the red shrimp juveniles is presented. et al., 2008; Cartes et al., 2017), the life history and distribution of It is out of doubt that additional and more frequent surveys are smallest individuals of A. antennatus captured in the Balearic Basin can needed in deep waters to unravel life history traits and morphological be reconstructed during the first year of life. The age of the current features of a wide array of marine species. Early stages of many com­ specimen, representing the first-settlement stage, can vary, since this mercial species are yet to be discovered and characterized, an important species displays a relatively long reproductive period which extends task to be done in order to achieve the understanding required for the from April–May to September–October (Carbonell et al., 1999), and correct and sustainable management of commercially exploited natural larvae of quite different stages can be found in the water column at the stocks, as is the case of A. antennatus. same time (Mysis II and Protozoea II in July for example, see Torres et al., 2013). After settlement, the geographical occurrence of Funding A. antennatus smallest individuals (CL < 16 mm), compiled on the basis of a number of oceanographic cruises performed in the Balearic Basin This work was supported by the European Commission [grant between 2007 and 2020, evidenced temporal and spatial patterns in the number FAIR–CT95–0655] and by the Spanish Ministry of Science and distribution of these small shrimps (see Fig. 5). In October–December Innovation (BIOMARE project [grant number (minimum CL of 6.4 mm) these small specimens were not abundant, CTM2006–13508–C02–01MAR], ANTROMARE project [grants numbers which points to an initial phase of settlement. These specimens were CTM2009–12214–C02–01 and CTM2009–12214–C02–02] and RECO­ mainly distributed on the head of the large Valencia Trough, the MARES project [grant number RTI2018-094066-B-100]). southern part of the Balearic Basin, relatively close to the location where the first-settled specimen described in the present work was found. The Declaration of competing interest distribution and density of these smallest A. antennatus at the end of winter and spring (minimum CL of 6.7–8.2 mm) and in summer (mini­ The authors declare that they have no known competing financial mum CL of 10.9–11.5 mm) suggests a progressive displacement from the interests or personal relationships that could have appeared to influence south-west to the north-east of the Balearic Basin along the Valencia the work reported in this paper. Trough, with higher densities at deeper and insular areas, mostly on the eastern side of the Valencia Channel. The growth of the smallest in­ Data availability dividuals of A. antennatus was established by Cartes and Demestre (2003), and it is well-known that the distribution of juveniles of the 1st Data will be made available on request. year cohort is almost completely restricted to depths >1000 m, and thus within the western Mediterranean deep-water mass (Cartes et al., 2017). Acknowledgements These juveniles live in benthic habitats and feed on the benthos-suprabenthos (Sardà and Cartes, 1997). In the present case we We are indebted to all participants in the QUIMERA1 and ReTro2 can glimpse a temporal distribution pattern of “bigger-offshore” that cruises, as well as those of the projects BIOMARE, ANTROMARE and could be linked to seasonal changes in the water column conditions in RECOMARES. the study area, since the water mass (the Western Mediterranean Deep Water current, WMDW) is the same. During winter-spring the water Appendix A. Supplementary data column is homogeneous, but downwelling phenomena of winter waters in the north, from the Gulf of Lyons (Millot, 1999), could act as a barrier Supplementary data to this article can be found online at https://doi. for juvenile dispersion to deeper grounds, somehow limiting the distri­ org/10.1016/j.dsr.2023.104020. bution of juveniles in the central region of the Balearic Basin. By contrast, the flow of winter waters in the N is interrupted by the water References column stratification occurring by late spring-early summer, which would allow the displacement of small specimens of A. antennatus to Abelló, P., Valladares, F.J., Castellón, A., 1988. Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar. Biol. higher depths of the Balearic Basin valley. 98, 39–49. Anger, K., 2001. The biology of decapod crustacean larvae. Crustac. Issues 14, 420. CRC 5. Conclusions Press. Bastrikin, D.K., Gallego, A., Millar, C.P., Priede, I.G., Jones, E.G., 2014. Settlement length and temporal settlement patterns of juvenile cod (Gadus morhua), haddock The generalized scarcity of known first-settled stages for all deep-sea (Melanogrammus aeglefinus), and whiting (Merlangius merlangus) in a northern North fauna (including the red shrimp) is, in all likelihood, related to the lack Sea coastal nursery área. ICES J. Mar. Sci. 71, 2101–2113. 8 S. Dallarés et al. Deep-Sea Research Part I 196 (2023) 104020 Belcari, P., Viva, C., Mori, M., de Ranieri, S., 2003. Fishery and biology of Aristaeomorpha Sicynidae, Sergestidae, and Luciferidae). International Council for the Exploration of foliacea (risso, 1827) (Crustacea: Decapoda) in the northern tyrrhenian sea (western the Sea. ICES Identification leaflets for plankton 186. mediterranean). J. Northwest Atl. Fish. Sci. 31, 195–204. dos Santos, A., González-Gordillo, J.I., 2004. Illustrated keys for the identification of the Calazans, D.K., 1993. Key to the larvae and decapodids of genera of the infraorder Pleocyemata (Crustacea: Decapoda) zoeal stages, from the coastal region of south- Penaeidea from southern Brazilian coast. Nauplius 1, 45–62. western Europe. J. Mar. Ass. U.K. 84, 205–227. Carbonell, A., Carbonell, M., Demestre, M., Grau, A., Monserrat, S., 1999. The red shrimp Durden, J.M., Bett, B.J., Hufferd, ChL., Pebody, C., Ruhl, H.A., Smith Jr., K.L., 2020. Aristeus antennatus (risso, 1816) fishery and biology in the balearic Islands, western Response of deep-sea deposit-feeders to detrital inputs: a comparison of two abyssal mediterranean. Fish. Res. 44, 1–13. time-series sites. Deep-Sea Res. Part II 173, 104677. Carbonell, A., Grau, A., Lauronce, V., Gómez, C., 2006. Ovary development of the red Faillettaz, R., Voue, R., Irisson, J.O., Voué, R., Crec’hriou, R., Garsi, L.H., Lecaillon, G., shrimp, Aristeus antennatus (Risso, 1816) from the northwestern Mediterranean Sea. Agostini, S., Lenfant, P., 2020. Spatio-temporal patterns of larval fish settlement in Crustaceana 79 (6), 727–743. the northwestern Mediterranean Sea. Mar. Ecol. Prog. Ser. 650, 153–173. Carbonell, A., Lloret, J., Demestre, M., 2008. Relationship between condition and Felix-Hackradt, F.C., Hackradt, C.W., Garcia-Charton, J.A., Félix-Hackradt, F.C., Treviño- recruitment success of red shrimp (Aristeus antennatus) in the Balearic Sea Otón, J., Segovia-Viadero, M., Pérez-Ruzafa, A., García-Charton, J.A., 2013. (Northwestern Mediterranean). J. Mar. Syst. 71, 403–412. Environmental determinants on fish post-larval distribution in coastal areas of south- Carbonell, A., Aparicio-González, A., Papiol, V., Cartes, J.E., 2020. Composition and western Mediterranean Sea. Estuar. Coast Shelf Sci. 129, 59–72. distribution of larval decapod community in the deep-sea of the western The crustacean integument: setae, setules, and other ornamentation. In: Garm, A., mediterranean balearic sub basin. Fish. Oceanogr. 30, 205–218. Watling, L. (Eds.), 2013. The Natural History of the Crustacea. Functional Carreton, M., Company, J.B., Planella, L., Heras, S., García-Marín, J.-L., Agulló, M., Morphology and Diversity, I. Oxford University Press, USA. Clavel-Henry, M., Rotllant, G., dos Santos, A., Roldán, M.I., 2019. Morphological Heldt, J.H., 1955. Contribution à l’étude de la biologie des crevettes pénéides identification and molecular confirmation of the deep-sea blue and red shrimp Aristeomorpha foliacea (Risso) et Aristeus antennatus (Risso) (formes larvaires). Bull. Aristeus antennatus larvae. PeerJ 7, e6063. Soc. Sci. Nat. Tunis. VIII (1–2), 1–29. Cartes, J.E., 1994. Influence of depth and season on the diet of the deep-water aristeid Maynou, F., Cartes, J.E., 2012. Effects of trawling on fish and invertebrates from deep- Aristeus antennatus along the continental slope (400 to 2300 m) in the Catalan Sea. sea coral facies of Isidella elongata in the western Mediterranean. J. Mar. Biol. Assoc. Mar. Biol. 120, 639–648. U. K. 92 (7), 1501–1507. Cartes, J.E., Company, J.B., Maynou, F., 1994a. Deep-water decapod crustacean Millot, C., 1999. Circulation in the western Mediterranean Sea. J. Mar. Syst. 20, communities in the Northwestern Mediterranean: influence of submarine canyons 423–442. and seasons. Mar. Biol. 120, 221–229. Merrett, N.R., Marshall, N.B., 1981. Observations on the ecology of deep-sea bottom- Cartes, J.E., Sorbe, J.C., Sardà, F., 1994b. Spatial distribution of deep-sea decapods and living fishes collected off northwest Africa. Prog. Oceanogr. 9, 185–244. euphausiids near the bottom in the northwestern Mediterranean. J. Exp. Mar. Biol. Montgomery, J.C., Tolimieri, N., Haine, O.S., 2001. Active habitat selection by pre- Ecol. 179, 131–144. settlement reef fishes. Fish Fish. 2 (3), 261–277. Cartes, J.E., Demestre, M., 2003. Estimating secondary production in the deep-water Mullineaux, L.S., 1988. The role of settlement in structuring a hard-substratum shrimp Aristeus antennatus (risso, 1816) in the catalano-balearic basin (western community in the deep-sea. J. Exp. Mar. Biol. Ecol. 120, 247–261. mediterranean). J. Northwest Atl. Fish. Sci. 31, 355–361. Rohde, K. (Ed.), 2005. Marine Parasitology. CSIRO Publishing, Australia. Cartes, J.E., López-Pérez, C., Carbonell, A., 2017. Condition and recruitment of Aristeus Sardà, F., Cartes, J.E., 1997. Morphological features and ecological aspects of early antennatus at great depths (to 2,300 m) in the Mediterranean: relationship with juvenile specimens of the aristeid shrimp Aristeus antennatus (Risso, 1816). Mar. environmental factors. Fish. Oceanogr. 27 (2), 114–126. Freshw. Res. 48, 73–77. Cartes, J.E., Figueroa, D.F., 2020. Deep Sea isopods from the western mediterranean: Tamaki, A., Itoh, J.-I., Takeuchi, S., Takikawa, T., 2020. Semilunar postlarval settlement distribution and habitat. Prog. Oceanogr. 188, 102415. periodicity ensuing from semilunar larval reléase cycle in the Nihonotrypaea Dgpam, 2022. Departament d’Acció climàtica, pesca i agenda rural, generalitat de harmandi (Crustacea, Decapoda, Axiidea, Callianassidae) population on an intertidal Catalunya. Estadístiques de pesca. Available at: http://agricultura.gencat.cat/web/. sandflat in an open marine coastal embayment. Popul. Ecol. 62, 161–195. content/pe_pesca_aquicultura/pe09_captures_pesqueres/documents/fitxers_estatic Torres, A.P., Dos Santos, A., Alemany, F., Massutí, E., 2013. Larval stages of crustacean s/especies_llotja.xlsx. (Accessed 18 July 2022). species of interest for conservation and fishing exploitation in the western Di Muzio, G., Basile, R., Pessani, D., 2018. Description of the zoeal stages of Periclimenes Mediterranean. Sci. Mar. 77 (1), 149–160. aegylios Grippa & d’Udekem d’Acoz, 1996 (Crustacea: Decapoda: palaemonidae) Vinuesa, J.H., Varisco, M., Escriche, F., 2010. Settlement and recruitment of the crab reared in the laboratory. Zootaxa 4418 (3), 228–246. Halicarcinus planatus (Crustacea: Decapoda: hymenosomatidae) in golfo san jorge, dos Santos, A., Lindley, J.A. (Eds.), 2001. Crustacea. Decapoda: Larvae. II. Argentina. J. Mar. Biol. Assoc. U. K. 91, 685–690. Dendrobranchiata: (Aristeidae, Benthesicymidae, Penaeidae, Solenoceridae, Zariquiey, R., 1968. Crustáceos decápodos ibéricos. Invest. Pesq. 32, 1–510. 9